@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{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{FriedrichOberkoflerTrindadeetal.2021, author = {Friedrich, Thomas and Oberkofler, Vicky and Trindade, In{\^e}s and Altmann, Simone and Brzezinka, Krzysztof and L{\"a}mke, J{\"o}rn S. and Gorka, Michal and Kappel, Christian and Sokolowska, Ewelina and Skirycz, Aleksandra and Graf, Alexander and B{\"a}urle, Isabel}, title = {Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis}, series = {Nature Communications}, volume = {12}, journal = {Nature Communications}, number = {1}, publisher = {Nature Publishing Group UK}, address = {[London]}, issn = {2041-1723}, doi = {10.1038/s41467-021-23786-6}, pages = {15}, year = {2021}, abstract = {Adaptive plasticity in stress responses is a key element of plant survival strategies. For instance, moderate heat stress (HS) primes a plant to acquire thermotolerance, which allows subsequent survival of more severe HS conditions. Acquired thermotolerance is actively maintained over several days (HS memory) and involves the sustained induction of memory-related genes. Here we show that FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) is specifically required for physiological HS memory and maintaining high memory-gene expression during the days following a HS exposure. HSFA3 mediates HS memory by direct transcriptional activation of memory-related genes after return to normal growth temperatures. HSFA3 binds HSFA2, and in vivo both proteins form heteromeric complexes with additional HSFs. Our results indicate that only complexes containing both HSFA2 and HSFA3 efficiently promote transcriptional memory by positively influencing histone H3 lysine 4 (H3K4) hyper-methylation. In summary, our work defines the major HSF complex controlling transcriptional memory and elucidates the in vivo dynamics of HSF complexes during somatic stress memory. Moderate heat stress primes plants to acquire tolerance to subsequent, more severe heat stress. Here the authors show that the HSFA3 transcription factor forms a heteromeric complex with HSFA2 to sustain activated transcription of genes required for acquired thermotolerance by promoting H3K4 hyper-methylation.}, 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{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} } @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} } @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{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} } @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{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} }