@article{StreubelFritzTeltowetal.2018, author = {Streubel, Susanna and Fritz, Michael Andre and Teltow, Melanie and Kappel, Christian and Sicard, Adrien}, title = {Successive duplication-divergence mechanisms at the RCO locus contributed to leaf shape diversity in the Brassicaceae}, series = {Development : Company of Biologists}, volume = {145}, journal = {Development : Company of Biologists}, number = {8}, publisher = {Company of Biologists}, address = {Cambridge}, issn = {0950-1991}, doi = {10.1242/dev.164301}, pages = {10}, year = {2018}, abstract = {Gene duplication is a major driver for the increase of biological complexity. The divergence of newly duplicated paralogs may allow novel functions to evolve, while maintaining the ancestral one. Alternatively, partitioning the ancestral function among paralogs may allow parts of that role to follow independent evolutionary trajectories. We studied the REDUCED COMPLEXITY (RCO) locus, which contains three paralogs that have evolved through two independent events of gene duplication, and which underlies repeated events of leaf shape evolution within the Brassicaceae. In particular, we took advantage of the presence of three potentially functional paralogs in Capsella to investigate the extent of functional divergence among them. We demonstrate that the RCO copies control growth in different areas of the leaf. Consequently, the copies that are retained active in the different Brassicaceae lineages contribute to define the leaf dissection pattern. Our results further illustrate how successive gene duplication events and subsequent functional divergence can increase trait evolvability by providing independent evolutionary trajectories to specialized functions that have an additive effect on a given trait.}, language = {en} } @article{BrzezinkaAltmannCzesnicketal.2016, author = {Brzezinka, Krzysztof and Altmann, Simone and Czesnick, Hj{\"o}rdis and Nicolas, Philippe and Gorka, Michal and Benke, Eileen and Kabelitz, Tina and J{\"a}hne, Felix and Graf, Alexander and Kappel, Christian and B{\"a}urle, Isabel}, title = {Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling}, series = {eLife}, volume = {5}, journal = {eLife}, publisher = {eLife Sciences Publications}, address = {Cambridge}, issn = {2050-084X}, doi = {10.7554/eLife.17061}, pages = {23}, year = {2016}, abstract = {Plants as sessile organisms can adapt to environmental stress to mitigate its adverse effects. As part of such adaptation they maintain an active memory of heat stress for several days that promotes a more efficient response to recurring stress. We show that this heat stress memory requires the activity of the FORGETTER1 (FGT1) locus, with fgt1 mutants displaying reduced maintenance of heat-induced gene expression. FGT1 encodes the Arabidopsis thaliana orthologue of Strawberry notch (Sno), and the protein globally associates with the promoter regions of actively expressed genes in a heat-dependent fashion. FGT1 interacts with chromatin remodelers of the SWI/ SNF and ISWI families, which also display reduced heat stress memory. Genomic targets of the BRM remodeler overlap significantly with FGT1 targets. Accordingly, nucleosome dynamics at loci with altered maintenance of heat-induced expression are affected in fgt1. Together, our results suggest that by modulating nucleosome occupancy, FGT1 mediates stress-induced chromatin memory.}, language = {en} } @article{KabelitzKappelHennebergeretal.2014, author = {Kabelitz, Tina and Kappel, Christian and Henneberger, Kirstin and Benke, Eileen and Noeh, Christiane and B{\"a}urle, Isabel}, title = {eQTL mapping of transposon silencing reveals a position-dependent stable escape from epigenetic silencing and transposition of AtMu1 in thee arabidopsis lineage}, series = {The plant cell}, volume = {26}, journal = {The plant cell}, number = {8}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {1040-4651}, doi = {10.1105/tpc.114.128512}, pages = {3261 -- 3271}, year = {2014}, abstract = {Transposons are massively abundant in all eukaryotic genomes and are suppressed by epigenetic silencing. Transposon activity contributes to the evolution of species; however, it is unclear how much transposition-induced variation exists at a smaller scale and how transposons are targeted for silencing. Here, we exploited differential silencing of the AtMu1c transposon in the Arabidopsis thaliana accessions Columbia (Col) and Landsberg erecta (Ler). The difference persisted in hybrids and recombinant inbred lines and was mapped to a single expression quantitative trait locus within a 20-kb interval. In Ler only, this interval contained a previously unidentified copy of AtMu1c, which was inserted at the 39 end of a protein-coding gene and showed features of expressed genes. By contrast, AtMu1c(Col) was intergenic and associated with heterochromatic features. Furthermore, we identified widespread natural AtMu1c transposition from the analysis of over 200 accessions, which was not evident from alignments to the reference genome. AtMu1c expression was highest for insertions within 39 untranslated regions, suggesting that this location provides protection from silencing. Taken together, our results provide a species-wide view of the activity of one transposable element at unprecedented resolution, showing that AtMu1c transposed in the Arabidopsis lineage and that transposons can escape epigenetic silencing by inserting into specific genomic locations, such as the 3' end of genes.}, language = {en} } @article{LecourieuxKappelPierietal.2017, author = {Lecourieux, Fatma and Kappel, Christian and Pieri, Philippe and Charon, Justine and Pillet, Jeremy and Hilbert, Ghislaine and Renaud, Christel and Gomes, Eric and Delrot, Serge and Lecourieux, David}, title = {Dissecting the Biochemical and Transcriptomic Effects of a Locally Applied Heat Treatment on Developing Cabernet Sauvignon Grape Berries}, series = {Frontiers in plant science}, volume = {8}, journal = {Frontiers in plant science}, publisher = {Frontiers Research Foundation}, address = {Lausanne}, issn = {1664-462X}, doi = {10.3389/fpls.2017.00053}, pages = {23}, year = {2017}, abstract = {Reproductive development of grapevine and berry composition are both strongly influenced by temperature. To date, the molecular mechanisms involved in grapevine berries response to high temperatures are poorly understood. Unlike recent data that addressed the effects on berry development of elevated temperatures applied at the whole plant level, the present work particularly focuses on the fruit responses triggered by direct exposure to heat treatment (HT). In the context of climate change, this work focusing on temperature effect at the microclimate level is of particular interest as it can help to better understand the consequences of leaf removal (a common viticultural practice) on berry development. HT (+8 degrees C) was locally applied to clusters from Cabernet Sauvignon fruiting cuttings at three different developmental stages (middle green, veraison and middle ripening). Samples were collected 1, 7, and 14 days after treatment and used for metabolic and transcriptomic analyses. The results showed dramatic and specific biochemical and transcriptomic changes in heat exposed berries, depending on the developmental stage and the stress duration. When applied at the herbaceous stage, HT delayed the onset of veraison. Heating also strongly altered the berry concentration of amino acids and organic acids (e.g., phenylalanine, raminobutyric acid and malate) and decreased the anthocyanin content at maturity. These physiological alterations could be partly explained by the deep remodeling of transcriptome in heated berries. More than 7000 genes were deregulated in at least one of the nine experimental conditions. The most affected processes belong to the categories "stress responses," protein metabolism" and "secondary metabolism," highlighting the intrinsic capacity of grape berries to perceive HT and to build adaptive responses. Additionally, important changes in processes related to "transport," "hormone" and "cell wall" might contribute to the postponing of veraison. Finally, opposite effects depending on heating duration were observed for genes encoding enzymes of the general phenylpropanoid pathway, suggesting that the HI induced decrease in anthocyanin content may result from a combination of transcript abundance and product degradation.}, language = {en} } @misc{TedderCarleialGołębiewskaetal.2015, author = {Tedder, Andrew and Carleial, Samuel and Gołębiewska, Martyna and Kappel, Christian and Shimizu, Kentaro K. and Stift, Marc}, title = {Evolution of the selfing syndrome in Arabis alpina (Brassicaceae)}, series = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe}, journal = {Postprints der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe}, number = {502}, issn = {1866-8372}, doi = {10.25932/publishup-40840}, url = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-408401}, pages = {17}, year = {2015}, abstract = {Introduction The transition from cross-fertilisation (outcrossing) to self-fertilisation (selfing) frequently coincides with changes towards a floral morphology that optimises self-pollination, the selfing syndrome. Population genetic studies have reported the existence of both outcrossing and selfing populations in Arabis alpina (Brassicaceae), which is an emerging model species for studying the molecular basis of perenniality and local adaptation. It is unknown whether its selfing populations have evolved a selfing syndrome. Methods Using macro-photography, microscopy and automated cell counting, we compared floral syndromes (size, herkogamy, pollen and ovule numbers) between three outcrossing populations from the Apuan Alps and three selfing populations from the Western and Central Alps (Maritime Alps and Dolomites). In addition, we genotyped the plants for 12 microsatellite loci to confirm previous measures of diversity and inbreeding coefficients based on allozymes, and performed Bayesian clustering. Results and Discussion Plants from the three selfing populations had markedly smaller flowers, less herkogamy and lower pollen production than plants from the three outcrossing populations, whereas pistil length and ovule number have remained constant. Compared to allozymes, microsatellite variation was higher, but revealed similar patterns of low diversity and high Fis in selfing populations. Bayesian clustering revealed two clusters. The first cluster contained the three outcrossing populations from the Apuan Alps, the second contained the three selfing populations from the Maritime Alps and Dolomites. Conclusion We conclude that in comparison to three outcrossing populations, three populations with high selfing rates are characterised by a flower morphology that is closer to the selfing syndrome. The presence of outcrossing and selfing floral syndromes within a single species will facilitate unravelling the genetic basis of the selfing syndrome, and addressing which selective forces drive its evolution.}, language = {en} } @article{TedderCarleialGolebiewskaetal.2015, author = {Tedder, Andrew and Carleial, Samuel and Golebiewska, Martyna and Kappel, Christian and Shimizu, Kentaro K. and Stift, Marc}, title = {Evolution of the Selfing Syndrome in Arabis alpina (Brassicaceae)}, series = {PLoS one}, volume = {10}, journal = {PLoS one}, number = {6}, publisher = {PLoS}, address = {San Fransisco}, issn = {1932-6203}, doi = {10.1371/journal.pone.0126618}, pages = {17}, year = {2015}, abstract = {Introduction The transition from cross-fertilisation (outcrossing) to self-fertilisation (selfing) frequently coincides with changes towards a floral morphology that optimises self-pollination, the selfing syndrome. Population genetic studies have reported the existence of both outcrossing and selfing populations in Arabis alpina (Brassicaceae), which is an emerging model species for studying the molecular basis of perenniality and local adaptation. It is unknown whether its selfing populations have evolved a selfing syndrome. Methods Using macro-photography, microscopy and automated cell counting, we compared floral syndromes (size, herkogamy, pollen and ovule numbers) between three outcrossing populations from the Apuan Alps and three selfing populations from the Western and Central Alps (Maritime Alps and Dolomites). In addition, we genotyped the plants for 12 microsatellite loci to confirm previous measures of diversity and inbreeding coefficients based on allozymes, and performed Bayesian clustering. Results and Discussion Plants from the three selfing populations had markedly smaller flowers, less herkogamy and lower pollen production than plants from the three outcrossing populations, whereas pistil length and ovule number have remained constant. Compared to allozymes, microsatellite variation was higher, but revealed similar patterns of low diversity and high Fis in selfing populations. Bayesian clustering revealed two clusters. The first cluster contained the three outcrossing populations from the Apuan Alps, the second contained the three selfing populations from the Maritime Alps and Dolomites. Conclusion We conclude that in comparison to three outcrossing populations, three populations with high selfing rates are characterised by a flower morphology that is closer to the selfing syndrome. The presence of outcrossing and selfing floral syndromes within a single species will facilitate unravelling the genetic basis of the selfing syndrome, and addressing which selective forces drive its evolution.}, language = {en} } @misc{LecourieuxKappelLecourieuxetal.2014, author = {Lecourieux, Fatma and Kappel, Christian and Lecourieux, David and Serrano, Alejandra and Torres, Elizabeth and Arce-Johnson, Patricio and Delrot, Serge}, title = {An update on sugar transport and signalling in grapevine}, series = {Journal of experimental botany}, volume = {65}, journal = {Journal of experimental botany}, number = {3}, publisher = {Oxford Univ. Press}, address = {Oxford}, issn = {0022-0957}, doi = {10.1093/jxb/ert394}, pages = {821 -- 832}, year = {2014}, abstract = {In addition to their role as a source of reduced carbon, sugars may directly or indirectly control a wide range of activities in plant cells, through transcriptional and post-translational regulation. This control has been studied in detail using Arabidopsis thaliana, where genetic analysis offers many possibilities. Much less is known about perennial woody species. For several years, various aspects of sugar sensing and signalling have been investigated in the grape (Vitis vinifera L.) berry, an organ that accumulates high concentrations of hexoses in the vacuoles of flesh cells. Here we review various aspects of this topic: the molecular basis of sugar transport and its regulation by sugars in grapevine; the functional analysis of several sugar-induced genes; the effects of some biotic and abiotic stresses on the sugar content of the berry; and finally the effects of exogenous sugar supply on the ripening process in field conditions. A picture of complex feedback and multiprocess regulation emerges from these data.}, language = {en} } @article{NicolasLecourieuxKappeletal.2014, author = {Nicolas, Philippe and Lecourieux, David and Kappel, Christian and Cluzet, Stephanie and Cramer, Grant and Delrot, Serge and Lecourieux, Fatma}, title = {The basic leucine zipper transcription factor abscisic acid responseelement-binding factor 2 is an important transcriptional regulator ofabscisic acid-dependent grape berry ripening processes}, series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, volume = {164}, journal = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, number = {1}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {0032-0889}, doi = {10.1104/pp.113.231977}, pages = {365 -- 383}, year = {2014}, abstract = {In grape (Vitis vinifera), abscisic acid (ABA) accumulates during fruit ripening and is thought to play a pivotal role in this process, but the molecular basis of this control is poorly understood. This work characterizes ABSCISIC ACID RESPONSE ELEMENT-BINDING FACTOR2 (VvABF2), a grape basic leucine zipper transcription factor belonging to a phylogenetic subgroup previously shown to be involved in ABA and abiotic stress signaling in other plant species. VvABF2 transcripts mainly accumulated in the berry, from the onset of ripening to the harvesting stage, and were up-regulated by ABA. Microarray analysis of transgenic grape cells overexpressing VvABF2 showed that this transcription factor up-regulates and/or modifies existing networks related to ABA responses. In addition, grape cells overexpressing VvABF2 exhibited enhanced responses to ABA treatment compared with control cells. Among the VvABF2-mediated responses highlighted in this study, the synthesis of phenolic compounds and cell wall softening were the most strongly affected. VvABF2 overexpression strongly increased the accumulation of stilbenes that play a role in plant defense and human health (resveratrol and piceid). In addition, the firmness of fruits from tomato (Solanum lycopersicum) plants overexpressing VvABF2 was strongly reduced. These data indicate that VvABF2 is an important transcriptional regulator of ABA-dependent grape berry ripening.}, language = {en} } @article{KabelitzBrzezinkaFriedrichetal.2016, author = {Kabelitz, Tina and Brzezinka, Krzysztof and Friedrich, Thomas and Gorka, Michal and Graf, Alexander and Kappel, Christian and B{\"a}urle, Isabel}, title = {A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis}, series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, volume = {171}, journal = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {0032-0889}, doi = {10.1104/pp.15.01688}, pages = {344 -- 358}, year = {2016}, abstract = {Transposable elements (TEs) make up a large proportion of eukaryotic genomes. As their mobilization creates genetic variation that threatens genome integrity, TEs are epigenetically silenced through several pathways, and this may spread to neighboring sequences. JUMONJI (JMJ) proteins can function as antisilencing factors and prevent silencing of genes next to TEs. Whether TE silencing is counterbalanced by the activity of antisilencing factors is still unclear. Here, we characterize JMJ24 as a regulator of TE silencing. We show that loss of JMJ24 results in increased silencing of the DNA transposon AtMu1c, while overexpression of JMJ24 reduces silencing. JMJ24 has a JumonjiC (JmjC) domain and two RING domains. JMJ24 autoubiquitinates in vitro, demonstrating E3 ligase activity of the RING domain(s). JMJ24-JmjC binds the N-terminal tail of histone H3, and full-length JMJ24 binds histone H3 in vivo. JMJ24 activity is anticorrelated with histone H3 Lys 9 dimethylation (H3K9me2) levels at AtMu1c. Double mutant analyses with epigenetic silencing mutants suggest that JMJ24 antagonizes histone H3K9me2 and requires H3K9 methyltransferases for its activity on AtMu1c. Genome-wide transcriptome analysis indicates that JMJ24 affects silencing at additional TEs. Our results suggest that the JmjC domain of JMJ24 has lost demethylase activity but has been retained as a binding domain for histone H3. This is in line with phylogenetic analyses indicating that JMJ24 (with the mutated JmjC domain) is widely conserved in angiosperms. Taken together, this study assigns a role in TE silencing to a conserved JmjC-domain protein with E3 ligase activity, but no demethylase activity.}, 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{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} } @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{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{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} } @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{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} } @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{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} }