@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{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{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{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{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}
}
@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}
}
@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}
}
@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}
}
@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{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}
}