@article{CuongNguyenHuuKappelKelleretal.2016,
  author    = {Cuong Nguyen Huu, and Kappel, Christian and Keller, Barbara and Sicard, Adrien and Takebayashi, Yumiko and Breuninger, Holger and Nowak, Michael D. and B{\"a}urle, Isabel and Himmelbach, Axel and Burkart, Michael and Ebbing-Lohaus, Thomas and Sakakibara, Hitoshi and Altschmied, Lothar and Conti, Elena and Lenhard, Michael},
  title     = {Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses},
  series = {eLife},
  volume    = {5},
  journal   = {eLife},
  publisher = {eLife Sciences Publications},
  address   = {Cambridge},
  issn      = {2050-084X},
  doi       = {10.7554/eLife.17956},
  pages     = {15},
  year      = {2016},
  abstract  = {Heterostyly is a wide-spread floral adaptation to promote outbreeding, yet its genetic basis and evolutionary origin remain poorly understood. In Primula (primroses), heterostyly is controlled by the S-locus supergene that determines the reciprocal arrangement of reproductive organs and incompatibility between the two morphs. However, the identities of the component genes remain unknown. Here, we identify the Primula CYP734A50 gene, encoding a putative brassinosteroid-degrading enzyme, as the G locus that determines the style-length dimorphism. CYP734A50 is only present on the short-styled S-morph haplotype, it is specifically expressed in S-morph styles, and its loss or inactivation leads to long styles. The gene arose by a duplication specific to the Primulaceae lineage and shows an accelerated rate of molecular evolution. Thus, our results provide a mechanistic explanation for the Primula style-length dimorphism and begin to shed light on the evolution of the S-locus as a prime model for a complex plant supergene.},
  language  = {en}
}
@misc{NowakRussoSchlapbachetal.2015,
  author    = {Nowak, Michael D. and Russo, Giancarlo and Schlapbach, Ralph and Huu, Cuong Nguyen and Lenhard, Michael and Conti, Elena},
  title     = {The draft genome of Primula veris yields insights into the molecular basis of heterostyly},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch Naturwissenschaftliche Reihe},
  number    = {879},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43508},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-435088},
  pages     = {19},
  year      = {2015},
  abstract  = {Background The flowering plant Primula veris is a common spring blooming perennial that is widely cultivated throughout Europe. This species is an established model system in the study of the genetics, evolution, and ecology of heterostylous floral polymorphisms. Despite the long history of research focused on this and related species, the continued development of this system has been restricted due the absence of genomic and transcriptomic resources. Results We present here a de novo draft genome assembly of P. veris covering 301.8 Mb, or approximately 63\% of the estimated 479.22 Mb genome, with an N50 contig size of 9.5 Kb, an N50 scaffold size of 164 Kb, and containing an estimated 19,507 genes. The results of a RADseq bulk segregant analysis allow for the confident identification of four genome scaffolds that are linked to the P. veris S-locus. RNAseq data from both P. veris and the closely related species P. vulgaris allow for the characterization of 113 candidate heterostyly genes that show significant floral morph-specific differential expression. One candidate gene of particular interest is a duplicated GLOBOSA homolog that may be unique to Primula (PveGLO2), and is completely silenced in L-morph flowers. Conclusions The P. veris genome represents the first genome assembled from a heterostylous species, and thus provides an immensely important resource for future studies focused on the evolution and genetic dissection of heterostyly. As the first genome assembled from the Primulaceae, the P. veris genome will also facilitate the expanded application of phylogenomic methods in this diverse family and the eudicots as a whole.},
  language  = {en}
}
@article{NowakRussoSchlapbachetal.2015,
  author    = {Nowak, Michael D. and Russo, Giancarlo and Schlapbach, Ralph and Cuong Nguyen Huu, and Lenhard, Michael and Conti, Elena},
  title     = {The draft genome of Primula veris yields insights into the molecular basis of heterostyly},
  series = {Genome biology : biology for the post-genomic era},
  volume    = {16},
  journal   = {Genome biology : biology for the post-genomic era},
  publisher = {BioMed Central},
  address   = {London},
  issn      = {1465-6906},
  doi       = {10.1186/s13059-014-0567-z},
  pages     = {16},
  year      = {2015},
  abstract  = {Background: The flowering plant Primula veris is a common spring blooming perennial that is widely cultivated throughout Europe. This species is an established model system in the study of the genetics, evolution, and ecology of heterostylous floral polymorphisms. Despite the long history of research focused on this and related species, the continued development of this system has been restricted due the absence of genomic and transcriptomic resources. Results: We present here a de novo draft genome assembly of P. veris covering 301.8 Mb, or approximately 63\% of the estimated 479.22 Mb genome, with an N50 contig size of 9.5 Kb, an N50 scaffold size of 164 Kb, and containing an estimated 19,507 genes. The results of a RADseq bulk segregant analysis allow for the confident identification of four genome scaffolds that are linked to the P. veris S-locus. RNAseq data from both P. veris and the closely related species P. vulgaris allow for the characterization of 113 candidate heterostyly genes that show significant floral morph-specific differential expression. One candidate gene of particular interest is a duplicated GLOBOSA homolog that may be unique to Primula (PveGLO2), and is completely silenced in L-morph flowers. Conclusions: The P. veris genome represents the first genome assembled from a heterostylous species, and thus provides an immensely important resource for future studies focused on the evolution and genetic dissection of heterostyly. As the first genome assembled from the Primulaceae, the P. veris genome will also facilitate the expanded application of phylogenomic methods in this diverse family and the eudicots as a whole.},
  language  = {en}
}
@misc{JohnsonRammKappeletal.2015,
  author    = {Johnson, Kim L. and Ramm, Sascha and Kappel, Christian and Ward, Sally and Leyser, Ottoline and Sakamoto, Tomoaki and Kurata, Tetsuya and Bevan, Michael W. and Lenhard, Michael},
  title     = {The tinkerbell (tink) mutation identifies the dual-specificity MAPK phosphatase INDOLE- 3-BUTYRIC ACID-RESPONSE5 (IBR5) as a novel regulator of organ size in Arabidopsis},
  series = {PLoS ONE},
  journal   = {PLoS ONE},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-410245},
  pages     = {17},
  year      = {2015},
  abstract  = {Mitogen-activated dual-specificity MAPK phosphatases are important negative regulators in the MAPK signalling pathways responsible for many essential processes in plants. In a screen for mutants with reduced organ size we have identified a mutation in the active site of the dual-specificity MAPK phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) that we named tinkerbell (tink) due to its small size. Analysis of the tink mutant indicates that IBR5 acts as a novel regulator of organ size that changes the rate of growth in petals and leaves. Organ size and shape regulation by IBR5 acts independently of the KLU growth-regulatory pathway. Microarray analysis of tink/ibr5-6 mutants identified a likely role for this phosphatase in male gametophyte development. We show that IBR5 may influence the size and shape of petals through auxin and TCP growth regulatory pathways.},
  language  = {en}
}
@article{KappelIllingHuuetal.2020,
  author    = {Kappel, Christian and Illing, Nicola and Huu, Cuong Nguyen and Barger, Nichole N. and Cramer, Michael D. and Lenhard, Michael and Midgley, Jeremy J.},
  title     = {Fairy circles in Namibia are assembled from genetically distinct grasses},
  series = {Communications biology},
  volume    = {3},
  journal   = {Communications biology},
  number    = {1},
  publisher = {Springer Nature},
  address   = {London},
  issn      = {2399-3642},
  doi       = {10.1038/s42003-020-01431-0},
  pages     = {8},
  year      = {2020},
  abstract  = {Fairy circles are striking regularly sized and spaced, bare circles surrounded by Stipagrostis grasses that occur over thousands of square kilometres in Namibia. The mechanisms explaining their origin, shape, persistence and regularity remain controversial. One hypothesis for the formation of vegetation rings is based on the centrifugal expansion of a single individual grass plant, via clonal growth and die-back in the centre. Clonality could explain FC origin, shape and long-term persistence as well as their regularity, if one clone competes with adjacent clones. Here, we show that for virtually all tested fairy circles the periphery is not exclusively made up of genetically identical grasses, but these peripheral grasses belong to more than one unrelated genet. These results do not support a clonal explanation for fairy circles. Lack of clonality implies that a biological reason for their origin, shape and regularity must emerge from competition between near neighbor individuals within each fairy circle. Such lack of clonality also suggests a mismatch between longevity of fairy circles versus their constituent plants. Furthermore, our findings of lack of clonality have implications for some models of spatial patterning of fairy circles that are based on self-organization. Christian Kappel et al. examine the genetic composition of fairy circles, regular circular patterns of grasses in the Namib Desert, using ddRAD-seq. They find that these grasses are made up of multiple unrelated genets rather than genetically identical grasses, suggesting non-clonality.},
  language  = {en}
}
@article{JohnsonRammKappeletal.2015,
  author    = {Johnson, Kim L. and Ramm, Sascha and Kappel, Christian and Ward, Sally and Leyser, Ottoline and Sakamoto, Tomoaki and Kurata, Tetsuya and Bevan, Michael W. and Lenhard, Michael},
  title     = {The Tinkerbell (Tink) Mutation Identifies the Dual-Specificity MAPK Phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) as a Novel Regulator of Organ Size in Arabidopsis},
  series = {PLoS one},
  volume    = {10},
  journal   = {PLoS one},
  number    = {7},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1932-6203},
  doi       = {10.1371/journal.pone.0131103},
  pages     = {17},
  year      = {2015},
  abstract  = {Mitogen-activated dual-specificity MAPK phosphatases are important negative regulators in the MAPK signalling pathways responsible for many essential processes in plants. In a screen for mutants with reduced organ size we have identified a mutation in the active site of the dual-specificity MAPK phosphatase INDOLE-3-BUTYRIC ACID-RESPONSE5 (IBR5) that we named tinkerbell (tink) due to its small size. Analysis of the tink mutant indicates that IBR5 acts as a novel regulator of organ size that changes the rate of growth in petals and leaves. Organ size and shape regulation by IBR5 acts independently of the KLU growth-regulatory pathway. Microarray analysis of tink/ibr5-6 mutants identified a likely role for this phosphatase in male gametophyte development. We show that IBR5 may influence the size and shape of petals through auxin and TCP growth regulatory pathways.},
  language  = {en}
}
@misc{GuentherScholzZimmermannetal.2016,
  author    = {G{\"u}nther, Oliver and Scholz, Jana and Zimmermann, Matthias and Lang, Agnetha and Kampe, Heike and Horn-Conrad, Antje and Eckardt, Barbara and Pohlmann, Markus and Engel, Silke and Hackel, Manuela and Lenhard, Michael and Schwarz, Wolfgang},
  title     = {Portal = Schillernd, sensibel, kraftvoll: Meere und Ozeane},
  number    = {03/2016},
  organization    = {Universit{\"a}t Potsdam, Referat f{\"u}r Presse- und {\"O}ffentlichkeitsarbeit},
  issn      = {1618-6893},
  doi       = {10.25932/publishup-44067},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-440678},
  pages     = {46},
  year      = {2016},
  abstract  = {Aus dem Inhalt: - Schillernd, sensibel, kraftvoll: Meere und Ozeane - Erdoberfl{\"a}che im Fokus - Reine Theorie},
  language  = {de}
}
@article{TsukayaByrneHoriguchietal.2013,
  author    = {Tsukaya, Hirokazu and Byrne, Mary E. and Horiguchi, Gorou and Sugiyama, Munetaka and Van Lijsebettens, Mieke and Lenhard, Michael},
  title     = {How do 'housekeeping' genes control organogenesis?-unexpected new findings on the role of housekeeping genes in cell and organ differentiation},
  series = {Journal of plant research},
  volume    = {126},
  journal   = {Journal of plant research},
  number    = {1},
  publisher = {Springer},
  address   = {Tokyo},
  issn      = {0918-9440},
  doi       = {10.1007/s10265-012-0518-2},
  pages     = {3 -- 15},
  year      = {2013},
  abstract  = {In recent years, an increasing number of mutations in what would appear to be 'housekeeping genes' have been identified as having unexpectedly specific defects in multicellular organogenesis. This is also the case for organogenesis in seed plants. Although it is not surprising that loss-of-function mutations in 'housekeeping' genes result in lethality or growth retardation, it is surprising when (1) the mutant phenotype results from the loss of function of a 'housekeeping' gene and (2) the mutant phenotype is specific. In this review, by defining housekeeping genes as those encoding proteins that work in basic metabolic and cellular functions, we discuss unexpected links between housekeeping genes and specific developmental processes. In a surprising number of cases housekeeping genes coding for enzymes or proteins with functions in basic cellular processes such as transcription, post-transcriptional modification, and translation affect plant development.},
  language  = {en}
}
@misc{SicardLenhard2011,
  author    = {Sicard, Adrien and Lenhard, Michael},
  title     = {The selfing syndrome a model for studying the genetic and evolutionary basis of morphological adaptation in plants},
  series = {Annals of botany},
  volume    = {107},
  journal   = {Annals of botany},
  number    = {9},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0305-7364},
  doi       = {10.1093/aob/mcr023},
  pages     = {1433 -- 1443},
  year      = {2011},
  abstract  = {Background In angiosperm evolution, autogamously selfing lineages have been derived from outbreeding ancestors multiple times, and this transition is regarded as one of the most common evolutionary tendencies in flowering plants. In most cases, it is accompanied by a characteristic set of morphological and functional changes to the flowers, together termed the selfing syndrome. Two major areas that have changed during evolution of the selfing syndrome are sex allocation to male vs. female function and flower morphology, in particular flower (mainly petal) size and the distance between anthers and stigma. Scope A rich body of theoretical, taxonomic, ecological and genetic studies have addressed the evolutionary modification of these two trait complexes during or after the transition to selfing. Here, we review our current knowledge about the genetics and evolution of the selfing syndrome. Conclusions We argue that because of its frequent parallel evolution, the selfing syndrome represents an ideal model for addressing basic questions about morphological evolution and adaptation in flowering plants, but that realizing this potential will require the molecular identification of more of the causal genes underlying relevant trait variation.},
  language  = {en}
}
@misc{EldridgeŁangowskiStaceyetal.2016,
  author    = {Eldridge, Tilly and Łangowski, Łukasz and Stacey, Nicola and Jantzen, Friederike and Moubayidin, Laila and Sicard, Adrien and Southam, Paul and Kennaway, Richard and Lenhard, Michael and Coen, Enrico S. and {\O}stergaard, Lars},
  title     = {Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  number    = {986},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43804},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-438041},
  pages     = {3394 -- 3406},
  year      = {2016},
  abstract  = {Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity.},
  language  = {en}
}
@article{SicardKappelLeeetal.2016,
  author    = {Sicard, Adrien and Kappel, Christian and Lee, Young Wha and Wozniak, Natalia Joanna and Marona, Cindy and Stinchcombe, John R. and Wright, Stephen I. and Lenhard, Michael},
  title     = {Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella},
  series = {Proceedings of the National Academy of Sciences of the United States of America},
  volume    = {113},
  journal   = {Proceedings of the National Academy of Sciences of the United States of America},
  publisher = {National Acad. of Sciences},
  address   = {Washington},
  issn      = {0027-8424},
  doi       = {10.1073/pnas.1613394113},
  pages     = {13911 -- 13916},
  year      = {2016},
  abstract  = {Mating system shifts recurrently drive specific changes in organ dimensions. The shift in mating system from out-breeding to selfing is one of the most frequent evolutionary transitions in flowering plants and is often associated with an organ-specific reduction in flower size. However, the evolutionary paths along which polygenic traits, such as size, evolve are poorly understood. In particular, it is unclear how natural selection can specifically modulate the size of one organ despite the pleiotropic action of most known growth regulators. Here, we demonstrate that allelic variation in the intron of a general growth regulator contributed to the specific reduction of petal size after the transition to selfing in the genus Capsella. Variation within this intron affects an organ-specific enhancer that regulates the level of STERILE APETALA (SAP) protein in the developing petals. The resulting decrease in SAP activity leads to a shortening of the cell proliferation period and reduced number of petal cells. The absence of private polymorphisms at the causal region in the selfing species suggests that the small-petal allele was captured from standing genetic variation in the ancestral out-crossing population. Petal-size variation in the current out-crossing population indicates that several small-effect mutations have contributed to reduce petal-size. These data demonstrate how tissue-specific regulatory elements in pleiotropic genes contribute to organ-specific evolution. In addition, they provide a plausible evolutionary explanation for the rapid evolution of flower size after the out-breeding-to-selfing transition based on additive effects of segregating alleles.},
  language  = {en}
}
@article{AbdirashidLenhard2020,
  author    = {Abdirashid, Hashim and Lenhard, Michael},
  title     = {Say it with double flowers},
  series = {Journal of experimental botany},
  volume    = {71},
  journal   = {Journal of experimental botany},
  number    = {9},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0022-0957},
  doi       = {10.1093/jxb/eraa109},
  pages     = {2469 -- 2471},
  year      = {2020},
  abstract  = {Every year, lovers world-wide rely on mutants to show their feelings on Valentine's Day. This is because many of the most popular ornamental flowering plants have been selected to form extra petals at the expense of reproductive organs to enhance their attractiveness and aesthetic value to humans. This so-called 'double flower' (DF) phenotype, first described more than 2000 years ago (Meyerowitz et al., 1989) is present, for example, in many modern roses, carnations, peonies, and camellias. Gattolin et al. (2020) now identify a unifying explanation for the molecular basis of many of these DF cultivars.},
  language  = {en}
}
@article{BreuningerLenhard2010,
  author    = {Breuninger, Holger and Lenhard, Michael},
  title     = {Control of tissue and organ growth in plants},
  issn      = {0070-2153},
  year      = {2010},
  language  = {en}
}
@article{HuuKellerContietal.2020,
  author    = {Huu, Cuong Nguyen and Keller, Barbara and Conti, Elena and Kappel, Christian and Lenhard, Michael},
  title     = {Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene},
  series = {Proceedings of the National Academy of Sciences of the United States of America (PNAS)},
  volume    = {117},
  journal   = {Proceedings of the National Academy of Sciences of the United States of America (PNAS)},
  number    = {37},
  publisher = {National Academy of Sciences},
  address   = {Washington},
  issn      = {0027-8424},
  doi       = {10.1073/pnas.2006296117},
  pages     = {23148 -- 23157},
  year      = {2020},
  abstract  = {Heterostyly represents a fascinating adaptation to promote outbreeding in plants that evolved multiple times independently. While L-morph individuals form flowers with long styles, short anthers, and small pollen grains, S-morph individuals have flowers with short styles, long anthers, and large pollen grains. The difference between the morphs is controlled by an S-locus "supergene" consisting of several distinct genes that determine different traits of the syndrome and are held together, because recombination between them is suppressed. In Primula, the S locus is a roughly 300-kb hemizygous region containing five predicted genes. However, with one exception, their roles remain unclear, as does the evolutionary buildup of the S locus. Here we demonstrate that the MADS-box GLOBOSA2 (GLO2) gene at the S locus determines anther position. In Primula forbesii S-morph plants, GLO2 promotes growth by cell expansion in the fused tube of petals and stamen filaments beneath the anther insertion point; by contrast, neither pollen size nor male incompatibility is affected by GLO2 activity. The paralogue GLO1, from which GLO2 arose by duplication, has maintained the ancestral B-class function in specifying petal and stamen identity, indicating that GLO2 underwent neofunctionalization, likely at the level of the encoded protein. Genetic mapping and phylogenetic analysis indicate that the duplications giving rise to the style-length-determining gene CYP734A50 and to GLO2 occurred sequentially, with the CYP734A50 duplication likely the first. Together these results provide the most detailed insight into the assembly of a plant supergene yet and have important implications for the evolution of heterostyly.},
  language  = {en}
}
@article{FujikuraJingHanadaetal.2018,
  author    = {Fujikura, Ushio and Jing, Runchun and Hanada, Atsushi and Takebayashi, Yumiko and Sakakibara, Hitoshi and Yamaguchi, Shinjiro and Kappel, Christian and Lenhard, Michael},
  title     = {Variation in splicing efficiency underlies morphological evolution in capsella},
  series = {Developmental cell},
  volume    = {44},
  journal   = {Developmental cell},
  number    = {2},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {1534-5807},
  doi       = {10.1016/j.devcel.2017.11.022},
  pages     = {192 -- 203},
  year      = {2018},
  abstract  = {Understanding the molecular basis of morphological change remains a central challenge in evolutionary-developmental biology. The transition from outbreeding to selfing is often associated with a dramatic reduction in reproductive structures and functions, such as the loss of attractive pheromones in hermaphroditic Caenorhabditis elegans and a reduced flower size in plants. Here, we demonstrate that variation in the level of the brassinosteroid-biosynthesis enzyme CYP724A1 contributes to the reduced flower size of selfing Capsella rubella compared with its outbreeding ancestor Capsella grandiflora. The primary transcript of the C. rubella allele is spliced more efficiently than that of C. grandiflora, resulting in higher brassinosteroid levels. These restrict organ growth by limiting cell proliferation. More efficient splicing of the C. rubella allele results from two de novo mutations in the selfing lineage. Thus, our results highlight the potentially widespread importance of differential splicing efficiency and higher-than-optimal hormone levels in generating phenotypic variation.},
  language  = {en}
}
@misc{BreuningerLenhard2017,
  author    = {Breuninger, Holger and Lenhard, Michael},
  title     = {Expression of the central growth regulator BIG BROTHER is regulated by multiple cis-elements},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-400971},
  pages     = {10},
  year      = {2017},
  abstract  = {Background Much of the organismal variation we observe in nature is due to differences in organ size. The observation that even closely related species can show large, stably inherited differences in organ size indicates a strong genetic component to the control of organ size. Despite recent progress in identifying factors controlling organ growth in plants, our overall understanding of this process remains limited, partly because the individual factors have not yet been connected into larger regulatory pathways or networks. To begin addressing this aim, we have studied the upstream regulation of expression of BIG BROTHER (BB), a central growth-control gene in Arabidopsis thaliana that prevents overgrowth of organs. Final organ size and BB expression levels are tightly correlated, implying the need for precise control of its expression. BB expression mirrors proliferative activity, yet the gene functions to limit proliferation, suggesting that it acts in an incoherent feedforward loop downstream of growth activators to prevent over-proliferation. Results To investigate the upstream regulation of BB we combined a promoter deletion analysis with a phylogenetic footprinting approach. We were able to narrow down important, highly conserved, cis-regulatory elements within the BB promoter. Promoter sequences of other Brassicaceae species were able to partially complement the A. thaliana bb-1 mutant, suggesting that at least within the Brassicaceae family the regulatory pathways are conserved. Conclusions This work underlines the complexity involved in precise quantitative control of gene expression and lays the foundation for identifying important upstream regulators that determine BB expression levels and thus final organ size.},
  language  = {en}
}
@article{BollierSicardLeblondetal.2018,
  author    = {Bollier, Norbert and Sicard, Adrien and Leblond, Julie and Latrasse, David and Gonzalez, Nathalie and Gevaudant, Frederic and Benhamed, Moussa and Raynaud, Cecile and Lenhard, Michael and Chevalier, Christian and Hernould, Michel and Delmas, Frederic},
  title     = {At-MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM ACTIVITY, a Conserved Missing Link in the Regulation of Floral Meristem Termination in Arabidopsis and Tomato},
  series = {The plant cell},
  volume    = {30},
  journal   = {The plant cell},
  number    = {1},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {1040-4651},
  doi       = {10.1105/tpc.17.00653},
  pages     = {83 -- 100},
  year      = {2018},
  abstract  = {In angiosperms, the gynoecium is the last structure to develop within the flower due to the determinate fate of floral meristem (FM) stem cells. The maintenance of stem cell activity before its arrest at the stage called FM termination affects the number of carpels that develop. The necessary inhibition at this stage of WUSCHEL (WUS), which is responsible for stem cell maintenance, involves a two-step mechanism. Direct repression mediated by the MADS domain transcription factor AGAMOUS (AG), followed by indirect repression requiring the C2H2 zinc-finger protein KNUCKLES (KNU), allow for the complete termination of floral stem cell activity. Here, we show that Arabidopsis thaliana MINI ZINC FINGER2 (AtMIF2) and its homolog in tomato (Solanum lycopersicum), INHIBITOR OF MERISTEM ACTIVITY (SlIMA), participate in the FM termination process by functioning as adaptor proteins. AtMIF2 and SlIMA recruit AtKNU and SlKNU, respectively, to form a transcriptional repressor complex together with TOPLESS and HISTONE DEACETYLASE19. AtMIF2 and SlIMA bind to the WUS and SIWUS loci in the respective plants, leading to their repression. These results provide important insights into the molecular mechanisms governing (FM) termination and highlight the essential role of AtMIF2/SlIMA during this developmental step, which determines carpel number and therefore fruit size.},
  language  = {en}
}
@article{LohmannStaceyBreuningeretal.2010,
  author    = {Lohmann, Daniel and Stacey, Nicola and Breuninger, Holger and Jikumaru, Yusuke and M{\"u}ller, D{\"o}rte and Sicard, Adrien and Leyser, Ottoline and Yamaguchi, Shinjiro and Lenhard, Michael},
  title     = {SLOW MOTION is required for within-plant auxin homeostasis and normal timing of lateral organ initiation at the shoot meristem in Arabidopsis},
  issn      = {1040-4651},
  year      = {2010},
  language  = {en}
}
@article{ErikssonStransfeldAdamskietal.2010,
  author    = {Eriksson, Sven and Stransfeld, Lena and Adamski, Nikolai Maria and Breuninger, Holger and Lenhard, Michael},
  title     = {KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis},
  issn      = {0960-9822},
  year      = {2010},
  language  = {en}
}
@article{GrafDolzblaszWuerschumetal.2010,
  author    = {Graf, Philipp and Dolzblasz, Alicja and W{\"u}rschum, Tobias and Lenhard, Michael and Pfreundt, Ulrike and Laux, Thomas},
  title     = {MGOUN1 encodes an Arabidopsis type Ib DNA topoisomerase required in stem cell regulation and to maintain develpmentally regulated gene silencing},
  issn      = {1040-4651},
  year      = {2010},
  language  = {en}
}
@article{Lenhard2012,
  author    = {Lenhard, Michael},
  title     = {Expression of the central growth regulator BIG Brother is regulated by multiple cis-elements},
  editor    = {Breuninger, Holger},
  issn      = {1471-2229},
  doi       = {10.1186/1471-2229-12-41},
  year      = {2012},
  language  = {en}
}
@misc{PowellLenhard2012,
  author    = {Powell, Anahid E. and Lenhard, Michael},
  title     = {Control of organ size in plants},
  series = {Current biology},
  volume    = {22},
  journal   = {Current biology},
  number    = {9},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2012.02.010},
  pages     = {R360 -- R367},
  year      = {2012},
  abstract  = {The size of plant organs, such as leaves and flowers, is determined by an interaction of genotype and environmental influences. Organ growth occurs through the two successive processes of cell proliferation followed by cell expansion. A number of genes influencing either or both of these processes and thus contributing to the control of final organ size have been identified in the last decade. Although the overall picture of the genetic regulation of organ size remains fragmentary, two transcription factor/microRNA-based genetic pathways are emerging in the control of cell proliferation. However, despite this progress, fundamental questions remain unanswered, such as the problem of how the size of a growing organ could be monitored to determine the appropriate time for terminating growth. While genetic analysis will undoubtedly continue to advance our knowledge about size control in plants, a deeper understanding of this and other basic questions will require including advanced live-imaging and mathematical modeling, as impressively demonstrated by some recent examples. This should ultimately allow the comparison of the mechanisms underlying size control in plants and in animals to extract common principles and lineage-specific solutions.},
  language  = {en}
}
@unpublished{Lenhard2012,
  author    = {Lenhard, Michael},
  title     = {Plant Growth: Jogging the Cell Cycle with JAG},
  series = {Current biology},
  volume    = {22},
  journal   = {Current biology},
  number    = {19},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2012.07.033},
  pages     = {R838 -- R840},
  year      = {2012},
  language  = {en}
}
@article{TrostViCzesnicketal.2014,
  author    = {Trost, Gerda and Vi, Son Lang and Czesnick, Hj{\"o}rdis and Lange, Peggy and Holton, Nick and Giavalisco, Patrick and Zipfel, Cyril and Kappel, Christian and Lenhard, Michael},
  title     = {Arabidopsis poly(A) polymerase PAPS1 limits founder-cell recruitment to organ primordia and suppresses the salicylic acid-independent immune response downstream of EDS1/PAD4},
  series = {The plant journal},
  volume    = {77},
  journal   = {The plant journal},
  number    = {5},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.12421},
  pages     = {688 -- 699},
  year      = {2014},
  abstract  = {Polyadenylation of pre-mRNAs by poly(A) polymerase (PAPS) is a critical process in eukaryotic gene expression. As found in vertebrates, plant genomes encode several isoforms of canonical nuclear PAPS enzymes. In Arabidopsis thaliana these isoforms are functionally specialized, with PAPS1 affecting both organ growth and immune response, at least in part by the preferential polyadenylation of subsets of pre-mRNAs. Here, we demonstrate that the opposite effects of PAPS1 on leaf and flower growth reflect the different identities of these organs, and identify a role for PAPS1 in the elusive connection between organ identity and growth patterns. The overgrowth of paps1 mutant petals is due to increased recruitment of founder cells into early organ primordia, and suggests that PAPS1 activity plays unique roles in influencing organ growth. By contrast, the leaf phenotype of paps1 mutants is dominated by a constitutive immune response that leads to increased resistance to the biotrophic oomycete Hyaloperonospora arabidopsidis and reflects activation of the salicylic acid-independent signalling pathway downstream of ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1)/PHYTOALEXIN DEFICIENT4 (PAD4). These findings provide an insight into the developmental and physiological basis of the functional specialization amongst plant PAPS isoforms.},
  language  = {en}
}
@misc{JohnsonLenhard2011,
  author    = {Johnson, Kim L. and Lenhard, Michael},
  title     = {Genetic control of plant organ growth},
  series = {New phytologist : international journal of plant science},
  volume    = {191},
  journal   = {New phytologist : international journal of plant science},
  number    = {2},
  publisher = {Wiley-Blackwell},
  address   = {Malden},
  issn      = {0028-646X},
  doi       = {10.1111/j.1469-8137.2011.03737.x},
  pages     = {319 -- 333},
  year      = {2011},
  abstract  = {The growth of plant organs is under genetic control. Work in model species has identified a considerable number of genes that regulate different aspects of organ growth. This has led to an increasingly detailed knowledge about how the basic cellular processes underlying organ growth are controlled, and which factors determine when proliferation gives way to expansion, with this transition emerging as a critical decision point during primordium growth. Progress has been made in elucidating the genetic basis of allometric growth and the role of tissue polarity in shaping organs. We are also beginning to understand how the mechanisms that determine organ identity influence local growth behaviour to generate organs with characteristic sizes and shapes. Lastly, growth needs to be coordinated at several levels, for example between different cell layers and different regions within one organ, and the genetic basis for such coordination is being elucidated. However, despite these impressive advances, a number of basic questions are still not fully answered, for example, whether and how a growing primordium keeps track of its size. Answering these questions will likely depend on including additional approaches that are gaining in power and popularity, such as combined live imaging and modelling.},
  language  = {en}
}
@misc{HepworthLenhard2014,
  author    = {Hepworth, Jo and Lenhard, Michael},
  title     = {Regulation of plant lateral-organ growth by modulating cell number and size},
  series = {Current opinion in plant biology},
  volume    = {17},
  journal   = {Current opinion in plant biology},
  publisher = {Elsevier},
  address   = {London},
  issn      = {1369-5266},
  doi       = {10.1016/j.pbi.2013.11.005},
  pages     = {36 -- 42},
  year      = {2014},
  abstract  = {Leaves and floral organs grow to distinct, species-specific sizes and shapes. Research over the last few years has increased our understanding of how genetic pathways modulate cell proliferation and cell expansion to determine these sizes and shapes. In particular, the timing of proliferation arrest is an important point of control for organ size, and work on the regulators involved is showing how this control is achieved mechanistically and integrates environmental information. We are also beginning to understand how growth differs in different organs to produce their characteristic shapes, and how growth is integrated between different tissues that make up plant organs. Lastly, components of the general machinery in eukaryotic cells have been identified as having important roles in growth control.},
  language  = {en}
}
@misc{KappelCuongNguyenHuuLenhard2017,
  author    = {Kappel, Christian and Cuong Nguyen Huu, and Lenhard, Michael},
  title     = {A short story gets longer: recent insights into the molecular basis of heterostyly},
  series = {Journal of experimental botany},
  volume    = {68},
  journal   = {Journal of experimental botany},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0022-0957},
  doi       = {10.1093/jxb/erx387},
  pages     = {5719 -- 5730},
  year      = {2017},
  abstract  = {Heterostyly is a fascinating adaptation to promote outbreeding and a classical paradigm of botany. In the most common type of heterostyly, plants either form flowers with long styles and short stamens, or short styles and long stamens. This reciprocal organ positioning reduces pollen wastage and promotes cross-pollination, thus increasing male fitness. In addition, in many heterostylous species selfing and the generation of unfit progeny due to inbreeding depression is limited by a self-incompatibility system, thus promoting female fitness. The two floral forms are genetically determined by the S locus as a complex supergene, namely a chromosomal region containing several individual genes that control the different traits, such as style or stamen length, and are held together by very tight linkage due to suppressed recombination. Recent molecular-genetic studies in several systems, including Turnera, Fagopyrum, Linum, and Primula have begun to identify and characterize the causal heterostyly genes residing at the S locus. An emerging theme from several families is that the dominant S haplotype represents a hemizygous region not present on the recessive s haplotype. This provides an explanation for the suppressed recombination and suggests a scenario for the chromosomal evolution of the S locus. In this review, we discuss the results from recent molecular-genetic analyses in light of the classical models on the genetics and evolution of heterostyly.},
  language  = {en}
}
@misc{ZhangLenhard2017,
  author    = {Zhang, Yunming and Lenhard, Michael},
  title     = {Exiting Already? Molecular Control of Cell-Proliferation Arrest in Leaves: Cutting Edge},
  series = {Molecular plant},
  volume    = {10},
  journal   = {Molecular plant},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {1674-2052},
  doi       = {10.1016/j.molp.2017.05.004},
  pages     = {909 -- 911},
  year      = {2017},
  language  = {en}
}
@misc{Lenhard2017,
  author    = {Lenhard, Michael},
  title     = {Plant Development: Keeping on the Straight and Narrow and Flat},
  series = {Current biology},
  volume    = {27},
  journal   = {Current biology},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2017.10.030},
  pages     = {R1277 -- R1280},
  year      = {2017},
  language  = {en}
}
@article{KahlLenhardJoshi2019,
  author    = {Kahl, Sandra M. and Lenhard, Michael and Joshi, Jasmin Radha},
  title     = {Compensatory mechanisms to climate change in the widely distributed species Silene vulgaris},
  series = {The journal of ecology},
  volume    = {107},
  journal   = {The journal of ecology},
  number    = {4},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0022-0477},
  doi       = {10.1111/1365-2745.13133},
  pages     = {1918 -- 1930},
  year      = {2019},
  abstract  = {The adaptation of plants to future climatic conditions is crucial for their survival. Not surprisingly, phenotypic responses to climate change have already been observed in many plant populations. These responses may be due to evolutionary adaptive changes or phenotypic plasticity. Especially plant species with a wide geographic range are either expected to show genetic differentiation in response to differing climate conditions or to have a high phenotypic plasticity. We investigated phenotypic responses and plasticity as an estimate of the adaptive potential in the widespread species Silene vulgaris. In a greenhouse experiment, 25 European populations covering a geographic range from the Canary Islands to Sweden were exposed to three experimental precipitation and two temperature regimes mimicking a possible climate-change scenario for central Europe. We hypothesized that southern populations have a better performance under high temperature and drought conditions, as they are already adapted to a comparable environment. We found that our treatments significantly influenced the plants, but did not reveal a latitudinal difference in response to climate treatments for most plant traits. Only flower number showed a stronger plasticity in northern European populations (e.g. Swedish populations) where numbers decreased more drastically with increased temperature and decreased precipitation treatment. Synthesis. The significant treatment response in Silene vulgaris, independent of population origin - except for the number of flowers produced - suggests a high degree of universal phenotypic plasticity in this widely distributed species. This reflects the likely adaptation strategy of the species and forms the basis for a successful survival strategy during upcoming climatic changes. However, as flower number, a strongly fitness-related trait, decreased more strongly in northern populations under a climate-change scenario, there might be limits to adaptation even in this widespread, plastic species.},
  language  = {en}
}
@misc{BartholomaeusLenhard2019,
  author    = {Bartholom{\"a}us, Lisa and Lenhard, Michael},
  title     = {Plant Biology: Learning to Love Yourself},
  series = {Current biology},
  volume    = {29},
  journal   = {Current biology},
  number    = {14},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2019.06.015},
  pages     = {R695 -- R697},
  year      = {2019},
  abstract  = {In self-incompatible plants the female style rejects self pollen, yet the extent to which the female style in the many self-compatible species can still select between different pollen genotypes and thus bias fertilization success is unclear. A new study identifies the molecular basis for how styles of the self-compatible coyote tobacco bias the fertilization success of pollen genotypes using matching gene expression patterns in a manner analogous to cryptic female choice in animals.},
  language  = {en}
}
@misc{HuuPlaschilHimmelbachetal.2022,
  author    = {Huu, Cuong Nguyen and Plaschil, Sylvia and Himmelbach, Axel and Kappel, Christian and Lenhard, Michael},
  title     = {Female self-incompatibility type in heterostylous Primula is determined by the brassinosteroid-inactivating cytochrome P450 CYP734A50},
  series = {Current biology},
  volume    = {32},
  journal   = {Current biology},
  number    = {3},
  publisher = {Cell Press},
  address   = {Cambridge, Mass.},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2021.11.046},
  pages     = {671 -- 676, E1-E5},
  year      = {2022},
  abstract  = {Most flowering plants are hermaphrodites, with flowers having both male and female reproductive organs. One widespread adaptation to limit self-fertilization is self-incompatibility (SI), where self-pollen fails to fertilize ovules.(1,2) In homomorphic SI, many morphologically indistinguishable mating types are found, although in heteromorphic SI, the two or three mating types are associated with different floral morphologies.(3-6) In heterostylous Primula, a hemizygous supergene determines a short-styled S-morph and a long-styled L-morph, corresponding to two different mating types, and full seed set only results from inter morph crosses.(7-9) Style length is controlled by the brassinosteroid (BR)-inactivating cytochrome P450 CYP734A50,(10) yet it remains unclear what defines the male and female incompatibility types. Here, we show that CYP734A50 also determines the female incompatibility type. Inactivating CYP734A50 converts short S-morph styles into long styles with the same incompatibility behavior as L-morph styles, and this effect can be mimicked by exogenous BR treatment. In vitro responses of S-and L-morph pollen grains and pollen tubes to increasing BR levels could only partly explain their different in vivo behavior, suggesting both direct and indirect effects of the different BR levels in S-versus L-morph stigmas and styles in controlling pollen performance. This BR-mediated SI provides a novel mechanism for preventing self-fertilization. The joint control of morphology and SI by CYP734A50 has important implications for the evolutionary buildup of the heterostylous syndrome and provides a straightforward explanation for why essentially all of the derived self-compatible homostylous Primula species are long homostyles.(11)},
  subject      = {heteromorphic self-incompatibility},
  language  = {en}
}
@article{JoestHenselKappeletal.2016,
  author    = {J{\"o}st, Moritz and Hensel, Goetz and Kappel, Christian and Druka, Arnis and Sicard, Adrien and Hohmann, Uwe and Beier, Sebastian and Himmelbach, Axel and Waugh, Robbie and Kumlehn, Jochen and Stein, Nils and Lenhard, Michael},
  title     = {The INDETERMINATE DOMAIN Protein BROAD LEAF1 Limits Barley Leaf Width by Restricting Lateral Proliferation},
  series = {Current biology},
  volume    = {26},
  journal   = {Current biology},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2016.01.047},
  pages     = {903 -- 909},
  year      = {2016},
  abstract  = {Variation in the size, shape, and positioning of leaves as the major photosynthetic organs strongly impacts crop yield, and optimizing these aspects is a central aim of cereal breeding [1, 2]. Leaf growth in grasses is driven by cell proliferation and cell expansion in a basal growth zone [3]. Although several factors influencing final leaf size and shape have been identified from rice and maize [4-14], what limits grass leaf growth in the longitudinal or transverse directions during leaf development remains poorly understood. To identify factors involved in this process, we characterized the barley mutant broad leaf1 (blf1). Mutants form wider but slightly shorter leaves due to changes in the numbers of longitudinal cell files and of cells along the leaf length. These differences arise during primordia outgrowth because of more cell divisions in the width direction increasing the number of cell files. Positional cloning, analysis of independent alleles, and transgenic complementation confirm that BLF1 encodes a presumed transcriptional regulator of the INDETERMINATE DOMAIN family. In contrast to loss-of-function mutants, moderate overexpression of BLF1 decreases leaf width below wild-type levels. A functional BLF1-vYFP fusion protein expressed from the endogenous promoter shows a dynamic expression pattern in the shoot apical meristem and young leaf primordia. Thus, we propose that the BLF1 gene regulates barley leaf size by restricting cell proliferation in the leaf-width direction. Given the agronomic importance of canopy traits in cereals, identifying functionally different BLF1 alleles promises to allow for the generation of optimized cereal ideotypes.},
  language  = {en}
}
@article{ZhangRammingHeinkeetal.2019,
  author    = {Zhang, Yunming and Ramming, Anna and Heinke, Lisa and Altschmied, Lothar and Slotkin, R. Keith and Becker, J{\"o}rg D. and Kappel, Christian and Lenhard, Michael},
  title     = {The poly(A) polymerase PAPS1 interacts with the RNA-directed DNA-methylation pathway in sporophyte and pollen development},
  series = {The plant journal},
  volume    = {99},
  journal   = {The plant journal},
  number    = {4},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.14348},
  pages     = {655 -- 672},
  year      = {2019},
  abstract  = {RNA-based processes play key roles in the regulation of eukaryotic gene expression. This includes both the processing of pre-mRNAs into mature mRNAs ready for translation and RNA-based silencing processes, such as RNA-directed DNA methylation (RdDM). Polyadenylation of pre-mRNAs is one important step in their processing and is carried out by three functionally specialized canonical nuclear poly(A) polymerases in Arabidopsis thaliana. Null mutations in one of these, termed PAPS1, result in a male gametophytic defect. Using a fluorescence-labelling strategy, we have characterized this defect in more detail using RNA and small-RNA sequencing. In addition to global defects in the expression of pollen-differentiation genes, paps1 null-mutant pollen shows a strong overaccumulation of transposable element (TE) transcripts, yet a depletion of 21- and particularly 24-nucleotide-long short interfering RNAs (siRNAs) and microRNAs (miRNAs) targeting the corresponding TEs. Double-mutant analyses support a specific functional interaction between PAPS1 and components of the RdDM pathway, as evident from strong synergistic phenotypes in mutant combinations involving paps1, but not paps2 paps4, mutations. In particular, the double-mutant of paps1 and rna-dependent rna polymerase 6 (rdr6) shows a synergistic developmental phenotype disrupting the formation of the transmitting tract in the female gynoecium. Thus, our findings in A. thaliana uncover a potentially general link between canonical poly(A) polymerases as components of mRNA processing and RdDM, reflecting an analogous interaction in fission yeast.},
  language  = {en}
}
@article{SicardThammMaronaetal.2014,
  author    = {Sicard, Adrien and Thamm, Anna and Marona, Cindy and Lee, Young Wha and Wahl, Vanessa and Stinchcombe, John R. and Wright, Stephen I. and Kappel, Christian and Lenhard, Michael},
  title     = {Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene},
  series = {Current biology},
  volume    = {24},
  journal   = {Current biology},
  number    = {16},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2014.06.061},
  pages     = {1880 -- 1886},
  year      = {2014},
  abstract  = {Elucidating the genetic basis of morphological changes in evolution remains a major challenge in biology [1-3]. Repeated independent trait changes are of particular interest because they can indicate adaptation in different lineages or genetic and developmental constraints on generating morphological variation [4-6]. In animals, changes to "hot spot" genes with minimal pleiotropy and large phenotypic effects underlie many cases of repeated morphological transitions [4-8]. By contrast, only few such genes have been identified from plants [8-11], limiting cross-kingdom comparisons of the principles of morphological evolution. Here, we demonstrate that the REDUCED COMPLEXITY (RCO) locus [12] underlies more than one naturally evolved change in leaf shape in the Brassicaceae. We show that the difference in leaf margin dissection between the sister species Capsella rubella and Capsella grandiflora is caused by cis-regulatory variation in the homeobox gene RCO-A, which alters its activity in the developing lobes of the leaf. Population genetic analyses in the ancestral C. grandiflora indicate that the more-active C. rubella haplotype is derived from a now rare or lost C. grandiflora haplotype via additional mutations. In Arabidopsis thaliana, the deletion of the RCO-A and RCO-B genes has contributed to its evolutionarily derived smooth leaf margin [12], suggesting the RCO locus as a candidate for an evolutionary hot spot. We also find that temperature-responsive expression of RCO-A can explain the phenotypic plasticity of leaf shape to ambient temperature in Capsella, suggesting a molecular basis for the well-known negative correlation between temperature and leaf margin dissection.},
  language  = {en}
}
@article{ViTrostLangeetal.2013,
  author    = {Vi, Son Lang and Trost, Gerda and Lange, Peggy and Czesnick, Hj{\"o}rdis and Rao, Nishta and Lieber, Diana and Laux, Thomas and Gray, William M. and Manley, James L. and Groth, Detlef and Kappel, Christian and Lenhard, Michael},
  title     = {Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response},
  series = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  volume    = {110},
  journal   = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  number    = {34},
  publisher = {NATL ACAD SCIENCES},
  address   = {WASHINGTON},
  issn      = {0027-8424},
  doi       = {10.1073/pnas.1303967110},
  pages     = {13994 -- 13999},
  year      = {2013},
  abstract  = {Polyadenylation of pre-mRNAs is critical for efficient nuclear export, stability, and translation of the mature mRNAs, and thus for gene expression. The bulk of pre-mRNAs are processed by canonical nuclear poly(A) polymerase (PAPS). Both vertebrate and higher-plant genomes encode more than one isoform of this enzyme, and these are coexpressed in different tissues. However, in neither case is it known whether the isoforms fulfill different functions or polyadenylate distinct subsets of pre-mRNAs. Here we show that the three canonical nuclear PAPS isoforms in Arabidopsis are functionally specialized owing to their evolutionarily divergent C-terminal domains. A strong loss-of-function mutation in PAPS1 causes a male gametophytic defect, whereas a weak allele leads to reduced leaf growth that results in part from a constitutive pathogen response. By contrast, plants lacking both PAPS2 and PAPS4 function are viable with wild-type leaf growth. Polyadenylation of SMALL AUXIN UP RNA (SAUR) mRNAs depends specifically on PAPS1 function. The resulting reduction in SAUR activity in paps1 mutants contributes to their reduced leaf growth, providing a causal link between polyadenylation of specific pre-mRNAs by a particular PAPS isoform and plant growth. This suggests the existence of an additional layer of regulation in plant and possibly vertebrate gene expression, whereby the relative activities of canonical nuclear PAPS isoforms control de novo synthesized poly(A) tail length and hence expression of specific subsets of mRNAs.},
  language  = {en}
}
@article{KierzkowskiLenhardSmithetal.2013,
  author    = {Kierzkowski, Daniel and Lenhard, Michael and Smith, Richard and Kuhlemeier, Cris},
  title     = {Interaction between meristem tissue layers controls phyllotaxis},
  series = {Developmental cell},
  volume    = {26},
  journal   = {Developmental cell},
  number    = {6},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {1534-5807},
  doi       = {10.1016/j.devcel.2013.08.017},
  pages     = {616 -- 628},
  year      = {2013},
  abstract  = {Phyllotaxis and vein formation are among the most conspicuous patterning processes in plants. The expression and polarization of the auxin efflux carrier PIN1 is the earliest marker for both processes, with mathematical models indicating that PIN1 can respond to auxin gradients and/or auxin flux. Here, we use cell-layer-specific PIN1 knockouts and partial complementation of auxin transport mutants to examine the interaction between phyllotactic patterning, which occurs primarily in the L1 surface layer of the meristem, and midvein specification in the inner tissues. We show that PIN1 expression in the L1 is sufficient for correct organ positioning, as long as the L1-specific influx carriers are present. Thus, differentiation of inner tissues can proceed without PIN1 or any of the known polar transporters. On theoretical grounds, we suggest that canalization of auxin flux between an auxin source and an auxin sink may involve facilitated diffusion rather than polar transport.},
  language  = {en}
}
@article{SicardStaceyHermannetal.2011,
  author    = {Sicard, Adrien and Stacey, Nicola and Hermann, Katrin and Dessoly, Jimmy and Neuffer, Barbara and B{\"a}urle, Isabel and Lenhard, Michael},
  title     = {Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella},
  series = {The plant cell},
  volume    = {23},
  journal   = {The plant cell},
  number    = {9},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {1040-4651},
  doi       = {10.1105/tpc.111.088237},
  pages     = {3156 -- 3171},
  year      = {2011},
  abstract  = {The change from outbreeding to selfing is one of the most frequent evolutionary transitions in flowering plants. It is often accompanied by characteristic morphological and functional changes to the flowers (the selfing syndrome), including reduced flower size and opening. Little is known about the developmental and genetic basis of the selfing syndrome, as well as its adaptive significance. Here, we address these issues using the two closely related species Capsella grandiflora (the ancestral outbreeder) and red shepherd's purse (Capsella rubella, the derived selfer). In C. rubella, petal size has been decreased by shortening the period of proliferative growth. Using interspecific recombinant inbred lines, we show that differences in petal size and flower opening between the two species each have a complex genetic basis involving allelic differences at multiple loci. An intraspecific cross within C. rubella suggests that flower size and opening have been decreased in the C. rubella lineage before its extensive geographical spread. Lastly, by generating plants that likely resemble the earliest ancestors of the C. rubella lineage, we provide evidence that evolution of the selfing syndrome was at least partly driven by selection for efficient self-pollination. Thus, our studies pave the way for a molecular dissection of selfing-syndrome evolution.},
  language  = {en}
}
@unpublished{Lenhard2012,
  author    = {Lenhard, Michael},
  title     = {All's well that ends well arresting cell proliferation in leaves},
  series = {Developmental cell},
  volume    = {22},
  journal   = {Developmental cell},
  number    = {1},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {1534-5807},
  doi       = {10.1016/j.devcel.2011.12.004},
  pages     = {9 -- 11},
  year      = {2012},
  abstract  = {The transition from cell proliferation to cell expansion is critical for determining leaf size. Andriankaja et al. (2012) demonstrate that in leaves of dicotyledonous plants, a basal proliferation zone is maintained for several days before abruptly disappearing, and that chloroplast differentiation is required to trigger the onset of cell expansion.},
  language  = {en}
}
@article{KappelTrostCzesnicketal.2015,
  author    = {Kappel, Christian and Trost, Gerda and Czesnick, Hj{\"o}rdis and Ramming, Anna and Kolbe, Benjamin and Vi, Son Lang and Bispo, Claudia and Becker, J{\"o}rg D. and de Moor, Cornelia and Lenhard, Michael},
  title     = {Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana},
  series = {PLoS Genetics : a peer-reviewed, open-access journal},
  volume    = {11},
  journal   = {PLoS Genetics : a peer-reviewed, open-access journal},
  number    = {8},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1553-7390},
  doi       = {10.1371/journal.pgen.1005474},
  pages     = {30},
  year      = {2015},
  abstract  = {The poly(A) tail at 3' ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases, PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptome-wide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale co-expression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression.},
  language  = {en}
}
@article{SicardKappelJosephsetal.2015,
  author    = {Sicard, Adrien and Kappel, Christian and Josephs, Emily B. and Lee, Young Wha and Marona, Cindy and Stinchcombe, John R. and Wright, Stephen I. and Lenhard, Michael},
  title     = {Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella},
  series = {Nature Communications},
  volume    = {6},
  journal   = {Nature Communications},
  publisher = {Nature Publ. Group},
  address   = {London},
  issn      = {2041-1723},
  doi       = {10.1038/ncomms8960},
  pages     = {10},
  year      = {2015},
  abstract  = {In the Bateson-Dobzhansky-Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.},
  language  = {en}
}
@article{CzesnickLenhard2015,
  author    = {Czesnick, Hj{\"o}rdis and Lenhard, Michael},
  title     = {Size Control in Plants-Lessons from Leaves and Flowers},
  series = {Cold Spring Harbor perspectives in biology},
  volume    = {7},
  journal   = {Cold Spring Harbor perspectives in biology},
  number    = {8},
  publisher = {Cold Spring Harbor Laboratory Press},
  address   = {Cold Spring Harbor, NY},
  issn      = {1943-0264},
  doi       = {10.1101/cshperspect.a019190},
  pages     = {16},
  year      = {2015},
  abstract  = {To achieve optimal functionality, plant organs like leaves and petals have to grow to a certain size. Beginning with a limited number of undifferentiated cells, the final size of an organ is attained by a complex interplay of cell proliferation and subsequent cell expansion. Regulatory mechanisms that integrate intrinsic growth signals and environmental cues are required to enable optimal leaf and flower development. This review focuses on plant-specific principles of growth reaching from the cellular to the organ level. The currently known genetic pathways underlying these principles are summarized and network connections are highlighted. Putative non-cell autonomously acting mechanisms that might coordinate plant-cell growth are discussed.},
  language  = {en}
}
@article{EldridgeLangowskiStaceyetal.2016,
  author    = {Eldridge, Tilly and Langowski, Lukasz and Stacey, Nicola and Jantzen, Friederike and Moubayidin, Laila and Sicard, Adrien and Southam, Paul and Kennaway, Richard and Lenhard, Michael and Coen, Enrico S. and Ostergaard, Lars},
  title     = {Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy},
  series = {Development : Company of Biologists},
  volume    = {143},
  journal   = {Development : Company of Biologists},
  publisher = {Company of Biologists Limited},
  address   = {Cambridge},
  issn      = {0950-1991},
  doi       = {10.1242/dev.135327},
  pages     = {3394 -- 3406},
  year      = {2016},
  abstract  = {Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity.},
  language  = {en}
}
@misc{KahlKappelJoshietal.2021,
  author    = {Kahl, Sandra and Kappel, Christian and Joshi, Jasmin Radha and Lenhard, Michael},
  title     = {Phylogeography of a widely distributed plant species reveals cryptic genetic lineages with parallel phenotypic responses to warming and drought conditions},
  series = {Zweitver{\"o}ffentlichungen der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Zweitver{\"o}ffentlichungen der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-53003},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-530035},
  pages     = {13986 -- 14002},
  year      = {2021},
  abstract  = {To predict how widely distributed species will perform under future climate change, it is crucial to understand and reveal their underlying phylogenetics. However, detailed information about plant adaptation and its genetic basis and history remains scarce and especially widely distributed species receive little attention despite their putatively high adaptability. To examine the adaptation potential of a widely distributed species, we sampled the model plant Silene vulgaris across Europe. In a greenhouse experiment, we exposed the offspring of these populations to a climate change scenario for central Europe and revealed the population structure through whole-genome sequencing. Plants were grown under two temperatures (18°C and 21°C) and three precipitation regimes (65, 75, and 90 mm) to measure their response in biomass and fecundity-related traits. To reveal the population genetic structure, ddRAD sequencing was employed for a whole-genome approach. We found three major genetic clusters in S. vulgaris from Europe: one cluster comprising Southern European populations, one cluster of Western European populations, and another cluster containing central European populations. Population genetic diversity decreased with increasing latitude, and a Mantel test revealed significant correlations between FST and geographic distances as well as between genetic and environmental distances. Our trait analysis showed that the genetic clusters significantly differed in biomass-related traits and in the days to flowering. However, half of the traits showed parallel response patterns to the experimental climate change scenario. Due to the differentiated but parallel response patterns, we assume that phenotypic plasticity plays an important role for the adaptation of the widely distributed species S. vulgaris and its intraspecific genetic lineages.},
  language  = {en}
}
@article{KahlKappelJoshietal.2021,
  author    = {Kahl, Sandra and Kappel, Christian and Joshi, Jasmin Radha and Lenhard, Michael},
  title     = {Phylogeography of a widely distributed plant species reveals cryptic genetic lineages with parallel phenotypic responses to warming and drought conditions},
  series = {Ecology and Evolution},
  volume    = {11},
  journal   = {Ecology and Evolution},
  number    = {20},
  publisher = {John Wiley \& Sons, Inc.},
  address   = {Hoboken},
  issn      = {2045-7758},
  doi       = {10.1002/ece3.8103},
  pages     = {13986 -- 14002},
  year      = {2021},
  abstract  = {To predict how widely distributed species will perform under future climate change, it is crucial to understand and reveal their underlying phylogenetics. However, detailed information about plant adaptation and its genetic basis and history remains scarce and especially widely distributed species receive little attention despite their putatively high adaptability. To examine the adaptation potential of a widely distributed species, we sampled the model plant Silene vulgaris across Europe. In a greenhouse experiment, we exposed the offspring of these populations to a climate change scenario for central Europe and revealed the population structure through whole-genome sequencing. Plants were grown under two temperatures (18°C and 21°C) and three precipitation regimes (65, 75, and 90 mm) to measure their response in biomass and fecundity-related traits. To reveal the population genetic structure, ddRAD sequencing was employed for a whole-genome approach. We found three major genetic clusters in S. vulgaris from Europe: one cluster comprising Southern European populations, one cluster of Western European populations, and another cluster containing central European populations. Population genetic diversity decreased with increasing latitude, and a Mantel test revealed significant correlations between FST and geographic distances as well as between genetic and environmental distances. Our trait analysis showed that the genetic clusters significantly differed in biomass-related traits and in the days to flowering. However, half of the traits showed parallel response patterns to the experimental climate change scenario. Due to the differentiated but parallel response patterns, we assume that phenotypic plasticity plays an important role for the adaptation of the widely distributed species S. vulgaris and its intraspecific genetic lineages.},
  language  = {en}
}
@article{BreuningerLenhard2012,
  author    = {Breuninger, Holger and Lenhard, Michael},
  title     = {Expression of the central growth regulator BIG BROTHER is regulated by multiple cis-elements},
  series = {BMC PLANT BIOLOGY},
  volume    = {12},
  journal   = {BMC PLANT BIOLOGY},
  publisher = {BIOMED CENTRAL LTD},
  address   = {LONDON},
  issn      = {1471-2229},
  doi       = {10.1186/1471-2229-12-41},
  pages     = {10},
  year      = {2012},
  abstract  = {Background: Much of the organismal variation we observe in nature is due to differences in organ size. The observation that even closely related species can show large, stably inherited differences in organ size indicates a strong genetic component to the control of organ size. Despite recent progress in identifying factors controlling organ growth in plants, our overall understanding of this process remains limited, partly because the individual factors have not yet been connected into larger regulatory pathways or networks. To begin addressing this aim, we have studied the upstream regulation of expression of BIG BROTHER (BB), a central growth-control gene in Arabidopsis thaliana that prevents overgrowth of organs. Final organ size and BB expression levels are tightly correlated, implying the need for precise control of its expression. BB expression mirrors proliferative activity, yet the gene functions to limit proliferation, suggesting that it acts in an incoherent feedforward loop downstream of growth activators to prevent over-proliferation. Results: To investigate the upstream regulation of BB we combined a promoter deletion analysis with a phylogenetic footprinting approach. We were able to narrow down important, highly conserved, cis-regulatory elements within the BB promoter. Promoter sequences of other Brassicaceae species were able to partially complement the A. thaliana bb-1 mutant, suggesting that at least within the Brassicaceae family the regulatory pathways are conserved. Conclusions: This work underlines the complexity involved in precise quantitative control of gene expression and lays the foundation for identifying important upstream regulators that determine BB expression levels and thus final organ size.},
  language  = {en}
}
@misc{KappelTrostCzesnicketal.2015,
  author    = {Kappel, Christian and Trost, Gerda and Czesnick, Hj{\"o}rdis and Ramming, Anna and Kolbe, Benjamin and Vi, Song Lang and Bispo, Cl{\´a}udia and Becker, J{\"o}rg D. and de Moor, Cornelia and Lenhard, Michael},
  title     = {Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-96400},
  pages     = {1 -- 30},
  year      = {2015},
  abstract  = {The poly(A) tail at 3' ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases, PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptome-wide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale co-expression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression.},
  language  = {en}
}
@misc{SicardKappelJosephsetal.2015,
  author    = {Sicard, Adrien and Kappel, Christian and Josephs, Emily B. and Wha Lee, Young and Marona, Cindy and Stinchcombe, John R. and Wright, Stephen I. and Lenhard, Michael},
  title     = {Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-93568},
  year      = {2015},
  abstract  = {In the Bateson-Dobzhansky-Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.},
  language  = {en}
}
@article{KappelTrostCzesnicketal.2015,
  author    = {Kappel, Christian and Trost, Gerda and Czesnick, Hj{\"o}rdis and Ramming, Anna and Kolbe, Benjamin and Vi, Son Lang and Bispo, Cl{\´a}udia and Becker, J{\"o}rg D. and de Moor, Cornelia and Lenhard, Michael},
  title     = {Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana},
  series = {PLoS Genetics : a peer-reviewed, open-access journal},
  volume    = {11},
  journal   = {PLoS Genetics : a peer-reviewed, open-access journal},
  number    = {8},
  publisher = {Public Library of Science},
  address   = {San Francisco},
  issn      = {1553-7390},
  doi       = {10.1371/journal.pgen.1005474},
  pages     = {30},
  year      = {2015},
  abstract  = {The poly(A) tail at 3' ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases, PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptome-wide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale co-expression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression.},
  language  = {en}
}
@article{SicardKappelJosephsetal.2015,
  author    = {Sicard, Adrien and Kappel, Christian and Josephs, Emily B. and Wha Lee, Young and Marona, Cindy and Stinchcombe, John R. and Wright, Stephen I. and Lenhard, Michael},
  title     = {Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella},
  series = {Nature Communications},
  volume    = {6},
  journal   = {Nature Communications},
  publisher = {Nature Publishing Group},
  address   = {London},
  issn      = {2041-1723},
  doi       = {10.1038/ncomms8960},
  year      = {2015},
  abstract  = {In the Bateson-Dobzhansky-Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.},
  language  = {en}
}
@misc{JantzenWozniakKappeletal.2019,
  author    = {Jantzen, Friederike and Wozniak, Natalia Joanna and Kappel, Christian and Sicard, Adrien and Lenhard, Michael},
  title     = {A high‑throughput amplicon‑based method for estimating outcrossing rates},
  series = {Postprints der Universit{\"a}t Potsdam Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam Mathematisch-Naturwissenschaftliche Reihe},
  number    = {745},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43565},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-435657},
  pages     = {14},
  year      = {2019},
  abstract  = {Background: The outcrossing rate is a key determinant of the population-genetic structure of species and their long-term evolutionary trajectories. However, determining the outcrossing rate using current methods based on PCRgenotyping individual offspring of focal plants for multiple polymorphic markers is laborious and time-consuming. Results: We have developed an amplicon-based, high-throughput enabled method for estimating the outcrossing rate and have applied this to an example of scented versus non-scented Capsella (Shepherd's Purse) genotypes. Our results show that the method is able to robustly capture differences in outcrossing rates. They also highlight potential biases in the estimates resulting from differential haplotype sharing of the focal plants with the pollen-donor population at individual amplicons. Conclusions: This novel method for estimating outcrossing rates will allow determining this key population-genetic parameter with high-throughput across many genotypes in a population, enabling studies into the genetic determinants of successful pollinator attraction and outcrossing.},
  language  = {en}
}
@misc{JantzenLynchKappeletal.2019,
  author    = {Jantzen, Friederike and Lynch, Joseph H. and Kappel, Christian and H{\"o}fflin, Jona and Skaliter, Oded and Wozniak, Natalia Joanna and Sicard, Adrien and Sas, Claudia and Adebesin, Funmilayo and Ravid, Jasmin and Vainstein, Alexander and Hilker, Monika and Dudareva, Natalia and Lenhard, Michael},
  title     = {Retracing the molecular basis and evolutionary history of the loss of benzaldehyde emission in the genus Capsella},
  series = {Postprints der Universit{\"a}t Potsdam Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam Mathematisch-Naturwissenschaftliche Reihe},
  number    = {775},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43754},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-437542},
  pages     = {1349 -- 1360},
  year      = {2019},
  abstract  = {The transition from pollinator-mediated outbreeding to selfing has occurred many times in angiosperms. This is generally accompanied by a reduction in traits attracting pollinators, including reduced emission of floral scent. In Capsella, emission of benzaldehyde as a main component of floral scent has been lost in selfing C. rubella by mutation of cinnamate-CoA ligase CNL1. However, the biochemical basis and evolutionary history of this loss remain unknown, as does the reason for the absence of benzaldehyde emission in the independently derived selfer Capsella orientalis. We used plant transformation, in vitro enzyme assays, population genetics and quantitative genetics to address these questions. CNL1 has been inactivated twice independently by point mutations in C. rubella, causing a loss of enzymatic activity. Both inactive haplotypes are found within and outside of Greece, the centre of origin of C. rubella, indicating that they arose before its geographical spread. By contrast, the loss of benzaldehyde emission in C. orientalis is not due to an inactivating mutation in CNL1. CNL1 represents a hotspot for mutations that eliminate benzaldehyde emission, potentially reflecting the limited pleiotropy and large effect of its inactivation. Nevertheless, even closely related species have followed different evolutionary routes in reducing floral scent.},
  language  = {en}
}
@misc{SasMuellerKappeletal.2016,
  author    = {Sas, Claudia and M{\"u}ller, Frank and Kappel, Christian and Kent, Tyler V. and Wright, Stephen I. and Hilker, Monika and Lenhard, Michael},
  title     = {Repeated inactivation of the first committed enzyme underlies the loss of benzaldehyde emission after the selfing transition in Capsella},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  number    = {904},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43801},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-438018},
  pages     = {3313 -- 3319},
  year      = {2016},
  abstract  = {The enormous species richness of flowering plants is at least partly due to floral diversification driven by interactions between plants and their animal pollinators [1, 2]. Specific pollinator attraction relies on visual and olfactory floral cues [3-5]; floral scent can not only attract pollinators but also attract or repel herbivorous insects [6-8]. However, despite its central role for plant-animal interactions, the genetic control of floral scent production and its evolutionary modification remain incompletely understood [9-13]. Benzenoids are an important class of floral scent compounds that are generated from phenylalanine via several enzymatic pathways [14-17]. Here we address the genetic basis of the loss of floral scent associated with the transition from outbreeding to selfing in the genus Capsella. While the outbreeding C. grandiflora emits benzaldehyde as a major constituent of its floral scent, this has been lost in the selfing C. rubella. We identify the Capsella CNL1 gene encoding cinnamate: CoA ligase as responsible for this variation. Population genetic analysis indicates that CNL1 has been inactivated twice independently in C. rubella via different novel mutations to its coding sequence. Together with a recent study in Petunia [18], this identifies cinnamate: CoA ligase as an evolutionary hotspot for mutations causing the loss of benzenoid scent compounds in association with a shift in the reproductive strategy of Capsella from pollination by insects to self-fertilization.},
  language  = {en}
}
@article{JantzenWozniakKappeletal.2019,
  author    = {Jantzen, Friederike and Wozniak, Natalia Joanna and Kappel, Christian and Sicard, Adrien and Lenhard, Michael},
  title     = {A high‑throughput amplicon‑based method for estimating outcrossing rates},
  series = {Plant Methods},
  volume    = {15},
  journal   = {Plant Methods},
  number    = {47},
  publisher = {BioMed Central},
  address   = {London},
  issn      = {1746-4811},
  doi       = {10.1186/s13007-019-0433-9},
  pages     = {14},
  year      = {2019},
  abstract  = {Background: The outcrossing rate is a key determinant of the population-genetic structure of species and their long-term evolutionary trajectories. However, determining the outcrossing rate using current methods based on PCRgenotyping individual offspring of focal plants for multiple polymorphic markers is laborious and time-consuming. Results: We have developed an amplicon-based, high-throughput enabled method for estimating the outcrossing rate and have applied this to an example of scented versus non-scented Capsella (Shepherd's Purse) genotypes. Our results show that the method is able to robustly capture differences in outcrossing rates. They also highlight potential biases in the estimates resulting from differential haplotype sharing of the focal plants with the pollen-donor population at individual amplicons. Conclusions: This novel method for estimating outcrossing rates will allow determining this key population-genetic parameter with high-throughput across many genotypes in a population, enabling studies into the genetic determinants of successful pollinator attraction and outcrossing.},
  language  = {en}
}
@misc{KramerLenhard2017,
  author    = {Kramer, Elena M. and Lenhard, Michael},
  title     = {Shape and form in plant development},
  series = {Seminars in cell \& developmental biology},
  volume    = {79},
  journal   = {Seminars in cell \& developmental biology},
  publisher = {Elsevier},
  address   = {London},
  issn      = {1084-9521},
  doi       = {10.1016/j.semcdb.2017.11.004},
  pages     = {1 -- 2},
  year      = {2017},
  language  = {en}
}
@misc{SicardLenhard2018,
  author    = {Sicard, Adrien and Lenhard, Michael},
  title     = {Capsella},
  series = {Current biology},
  volume    = {28},
  journal   = {Current biology},
  number    = {17},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2018.06.033},
  pages     = {R920 -- R921},
  year      = {2018},
  language  = {en}
}
@article{FujikuraElsaesserBreuningeretal.2014,
  author    = {Fujikura, Ushio and Elsaesser, Lore and Breuninger, Holger and Sanchez-Rodriguez, Clara and Ivakov, Alexander and Laux, Thomas and Findlay, Kim and Persson, Staffan and Lenhard, Michael},
  title     = {Atkinesin-13A modulates cell-wall synthesis and cell expansion in arabidopsis thaliana via the THESEUS1 pathway},
  series = {PLoS Genetics : a peer-reviewed, open-access journal},
  volume    = {10},
  journal   = {PLoS Genetics : a peer-reviewed, open-access journal},
  number    = {9},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1553-7390},
  doi       = {10.1371/journal.pgen.1004627},
  pages     = {15},
  year      = {2014},
  abstract  = {Growth of plant organs relies on cell proliferation and expansion. While an increasingly detailed picture about the control of cell proliferation is emerging, our knowledge about the control of cell expansion remains more limited. We demonstrate the internal-motor kinesin AtKINESIN-13A (AtKIN13A) limits cell expansion and cell size in Arabidopsis thaliana, ion atkinl3a mutants forming larger petals with larger cells. The homolog, AtKINESIN-13B, also affects cell expansion and double mutants display growth, gametophytic and early embryonic defects, indicating a redundant role of he two genes. AtKIN13A is known to depolymerize microtubules and influence Golgi motility and distribution. Consistent his function, AtKIN13A interacts genetically with ANGUSTIFOLIA, encoding a regulator of Golgi dynamics. Reduced AtIGN13A activity alters cell wall structure as assessed by Fourier-transformed infrared-spectroscopy and triggers signalling he THESEUS1-dependent cell-wall integrity pathway, which in turn promotes the excess cell expansion in the atkinl3a mutant. Thus, our results indicate that the intracellular activity of AtKIN13A regulates cell expansion and wall architecture via THESEUS1, providing a compelling case of interplay between cell wall integrity sensing and expansion.},
  language  = {en}
}
@misc{PowellLenhard2012,
  author    = {Powell, Anahid E. and Lenhard, Michael},
  title     = {Control of organ size in plants},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch Naturwissenschaftliche Reihe},
  number    = {898},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43802},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-438029},
  pages     = {10},
  year      = {2012},
  abstract  = {The size of plant organs, such as leaves and flowers, is determined by an interaction of genotype and environmental influences. Organ growth occurs through the two successive processes of cell proliferation followed by cell expansion. A number of genes influencing either or both of these processes and thus contributing to the control of final organ size have been identified in the last decade. Although the overall picture of the genetic regulation of organ size remains fragmentary, two transcription factor/microRNA-based genetic pathways are emerging in the control of cell proliferation. However, despite this progress, fundamental questions remain unanswered, such as the problem of how the size of a growing organ could be monitored to determine the appropriate time for terminating growth. While genetic analysis will undoubtedly continue to advance our knowledge about size control in plants, a deeper understanding of this and other basic questions will require including advanced live-imaging and mathematical modeling, as impressively demonstrated by some recent examples. This should ultimately allow the comparison of the mechanisms underlying size control in plants and in animals to extract common principles and lineage-specific solutions.},
  language  = {en}
}
@misc{Lenhard2012,
  author    = {Lenhard, Michael},
  title     = {All's well that ends well},
  series = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  journal   = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe},
  number    = {906},
  issn      = {1866-8372},
  doi       = {10.25932/publishup-43803},
  url       = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-438035},
  pages     = {9 -- 11},
  year      = {2012},
  abstract  = {The transition from cell proliferation to cell expansion is critical for determining leaf size. Andriankaja et al. (2012) demonstrate that in leaves of dicotyledonous plants, a basal proliferation zone is maintained for several days before abruptly disappearing, and that chloroplast differentiation is required to trigger the onset of cell expansion.},
  language  = {en}
}
@article{SasMuellerKappeletal.2016,
  author    = {Sas, Claudia and Mueller, Frank and Kappel, Christian and Kent, Tyler V. and Wright, Stephen I. and Hilker, Monika and Lenhard, Michael},
  title     = {Repeated Inactivation of the First Committed Enzyme Underlies the Loss of Benzaldehyde Emission after the Selfing Transition in Capsella},
  series = {Current biology},
  volume    = {26},
  journal   = {Current biology},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {0960-9822},
  doi       = {10.1016/j.cub.2016.10.026},
  pages     = {3313 -- 3319},
  year      = {2016},
  abstract  = {The enormous species richness of flowering plants is at least partly due to floral diversification driven by interactions between plants and their animal pollinators [1, 2]. Specific pollinator attraction relies on visual and olfactory floral cues [3-5]; floral scent can not only attract pollinators but also attract or repel herbivorous insects [6-8]. However, despite its central role for plant-animal interactions, the genetic control of floral scent production and its evolutionary modification remain incompletely understood [9-13]. Benzenoids are an important class of floral scent compounds that are generated from phenylalanine via several enzymatic pathways [14-17]. Here we address the genetic basis of the loss of floral scent associated with the transition from outbreeding to selfing in the genus Capsella. While the outbreeding C. grandiflora emits benzaldehyde as a major constituent of its floral scent, this has been lost in the selfing C. rubella. We identify the Capsella CNL1 gene encoding cinnamate: CoA ligase as responsible for this variation. Population genetic analysis indicates that CNL1 has been inactivated twice independently in C. rubella via different novel mutations to its coding sequence. Together with a recent study in Petunia [18], this identifies cinnamate: CoA ligase as an evolutionary hotspot for mutations causing the loss of benzenoid scent compounds in association with a shift in the reproductive strategy of Capsella from pollination by insects to self-fertilization.},
  language  = {en}
}
@article{CzesnickLenhard2016,
  author    = {Czesnick, Hj{\"o}rdis and Lenhard, Michael},
  title     = {Antagonistic control of flowering time by functionally specialized poly(A) polymerases in Arabidopsis thaliana},
  series = {The plant journal},
  volume    = {88},
  journal   = {The plant journal},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.13280},
  pages     = {570 -- 583},
  year      = {2016},
  abstract  = {Polyadenylation is a critical 3-end processing step during maturation of pre-mRNAs, and the length of the poly(A) tail affects mRNA stability, nuclear export and translation efficiency. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerase (PAPS) isoforms fulfilling specialized functions, as reflected by their different mutant phenotypes. While PAPS1 affects several processes, such as the immune response, organ growth and male gametophyte development, the roles of PAPS2 and PAPS4 are largely unknown. Here we demonstrate that PAPS2 and PAPS4 promote flowering in a partially redundant manner. The enzymes act antagonistically to PAPS1, which delays the transition to flowering. The opposite flowering-time phenotypes in paps1 and paps2 paps4 mutants are at least partly due to decreased or increased FLC activity, respectively. In contrast to paps2 paps4 mutants, plants with increased PAPS4 activity flower earlier than the wild-type, concomitant with reduced FLC expression. Double mutant analyses suggest that PAPS2 and PAPS4 act independently of the autonomous pathway components FCA, FY and CstF64. The direct polyadenylation targets of the three PAPS isoforms that mediate their effects on flowering time do not include FLC sense mRNA and remain to be identified. Thus, our results uncover a role for canonical PAPS isoforms in flowering-time control, raising the possibility that modulating the balance of the isoform activities could be used to fine tune the transition to flowering. Significance Statement The length of the poly(A) tail affects mRNA stability, nuclear export and translation efficiency. Arabidopsis has three isoforms of nuclear poly(A) polymerase (PAPS): PAPS1 plays a major role in organ growth and plant defence. Here we show that PAPS2 and PAPS4 redundantly promote flowering and act antagonistically to PAPS1, which delays flowering. We suggest that modulating the activity of these isoforms fine-tunes the transition to flowering.},
  language  = {en}
}
@article{TranBuiKappeletal.2020,
  author    = {Tran, Quan Hong and Bui, Ngoc Hong and Kappel, Christian and Dau, Nga Thi Ngoc and Nguyen, Loan Thi and Tran, Thuy Thi and Khanh, Tran Dang and Trung, Khuat Huu and Lenhard, Michael and Vi, Son Lang},
  title     = {Mapping-by-sequencing via MutMap identifies a mutation in ZmCLE7 underlying fasciation in a newly developed EMS mutant population in an elite tropical maize inbred},
  series = {Genes},
  volume    = {11},
  journal   = {Genes},
  number    = {3},
  publisher = {MDPI},
  address   = {Basel},
  issn      = {2073-4425},
  doi       = {10.3390/genes11030281},
  pages     = {1 -- 14},
  year      = {2020},
  abstract  = {Induced point mutations are important genetic resources for their ability to create hypo- and hypermorphic alleles that are useful for understanding gene functions and breeding. However, such mutant populations have only been developed for a few temperate maize varieties, mainly B73 and W22, yet no tropical maize inbred lines have been mutagenized and made available to the public to date. We developed a novel Ethyl Methanesulfonate (EMS) induced mutation resource in maize comprising 2050 independent M2 mutant families in the elite tropical maize inbred ML10. By phenotypic screening, we showed that this population is of comparable quality with other mutagenized populations in maize. To illustrate the usefulness of this population for gene discovery, we performed rapid mapping-by-sequencing to clone a fasciated-ear mutant and identify a causal promoter deletion in ZmCLE7 (CLE7). Our mapping procedure does not require crossing to an unrelated parent, thus is suitable for mapping subtle traits and ones affected by heterosis. This first EMS population in tropical maize is expected to be very useful for the maize research community. Also, the EMS mutagenesis and rapid mapping-by-sequencing pipeline described here illustrate the power of performing forward genetics in diverse maize germplasms of choice, which can lead to novel gene discovery due to divergent genetic backgrounds.},
  language  = {en}
}
@article{PotenteLeveilleBourretYousefietal.2022,
  author    = {Potente, Giacomo and L{\´e}veill{\´e}-Bourret, {\´E}tienne and Yousefi, Narjes and Choudhury, Rimjhim Roy and Keller, Barbara and Diop, Seydina Issa and Duijsings, Dani{\"e}l and Pirovano, Walter and Lenhard, Michael and Sz{\"o}v{\´e}nyi, P{\´e}ter and Conti, Elena},
  title     = {Comparative genomics elucidates the origin of a supergene controlling floral heteromorphism},
  series = {Molecular biology and evolution : MBE},
  volume    = {39},
  journal   = {Molecular biology and evolution : MBE},
  number    = {2},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0737-4038},
  doi       = {10.1093/molbev/msac035},
  pages     = {16},
  year      = {2022},
  abstract  = {Supergenes are nonrecombining genomic regions ensuring the coinheritance of multiple, coadapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterostyly is characterized by the cooccurrence of two complementary, self-incompatible floral morphs and is controlled by five genes clustered in the hemizygous, ca. 300-kb S locus. Here, we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula?},
  language  = {en}
}