TY - JOUR A1 - Jöst, Moritz A1 - Hensel, Goetz A1 - Kappel, Christian A1 - Druka, Arnis A1 - Sicard, Adrien A1 - Hohmann, Uwe A1 - Beier, Sebastian A1 - Himmelbach, Axel A1 - Waugh, Robbie A1 - Kumlehn, Jochen A1 - Stein, Nils A1 - Lenhard, Michael T1 - The INDETERMINATE DOMAIN Protein BROAD LEAF1 Limits Barley Leaf Width by Restricting Lateral Proliferation JF - Current biology N2 - 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. Y1 - 2016 U6 - https://doi.org/10.1016/j.cub.2016.01.047 SN - 0960-9822 SN - 1879-0445 VL - 26 SP - 903 EP - 909 PB - Cell Press CY - Cambridge ER - TY - JOUR A1 - Streubel, Susanna A1 - Fritz, Michael Andre A1 - Teltow, Melanie A1 - Kappel, Christian A1 - Sicard, Adrien T1 - Successive duplication-divergence mechanisms at the RCO locus contributed to leaf shape diversity in the Brassicaceae JF - Development : Company of Biologists N2 - 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. KW - Plant development KW - Gene duplication KW - Leaf shape KW - Morphological evolution KW - Capsella KW - Arabidopsis Y1 - 2018 U6 - https://doi.org/10.1242/dev.164301 SN - 0950-1991 SN - 1477-9129 VL - 145 IS - 8 PB - Company of Biologists CY - Cambridge ER - TY - JOUR A1 - Sicard, Adrien A1 - Kappel, Christian A1 - Lee, Young Wha A1 - Wozniak, Natalia Joanna A1 - Marona, Cindy A1 - Stinchcombe, John R. A1 - Wright, Stephen I. A1 - Lenhard, Michael T1 - Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella JF - Proceedings of the National Academy of Sciences of the United States of America N2 - 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. KW - morphological evolution KW - growth control KW - standing variation; organ-specific evolution KW - intronic cis-regulatory element Y1 - 2016 U6 - https://doi.org/10.1073/pnas.1613394113 SN - 0027-8424 VL - 113 SP - 13911 EP - 13916 PB - National Acad. of Sciences CY - Washington ER - TY - JOUR A1 - Lohmann, Daniel A1 - Stacey, Nicola A1 - Breuninger, Holger A1 - Jikumaru, Yusuke A1 - Müller, Dörte A1 - Sicard, Adrien A1 - Leyser, Ottoline A1 - Yamaguchi, Shinjiro A1 - Lenhard, Michael T1 - SLOW MOTION is required for within-plant auxin homeostasis and normal timing of lateral organ initiation at the shoot meristem in Arabidopsis Y1 - 2010 SN - 1040-4651 ER - TY - JOUR A1 - Sicard, Adrien A1 - Thamm, Anna A1 - Marona, Cindy A1 - Lee, Young Wha A1 - Wahl, Vanessa A1 - Stinchcombe, John R. A1 - Wright, Stephen I. A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene JF - Current biology N2 - 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. Y1 - 2014 U6 - https://doi.org/10.1016/j.cub.2014.06.061 SN - 0960-9822 SN - 1879-0445 VL - 24 IS - 16 SP - 1880 EP - 1886 PB - Cell Press CY - Cambridge ER - TY - JOUR A1 - Cuong Nguyen Huu, A1 - Kappel, Christian A1 - Keller, Barbara A1 - Sicard, Adrien A1 - Takebayashi, Yumiko A1 - Breuninger, Holger A1 - Nowak, Michael D. A1 - Bäurle, Isabel A1 - Himmelbach, Axel A1 - Burkart, Michael A1 - Ebbing-Lohaus, Thomas A1 - Sakakibara, Hitoshi A1 - Altschmied, Lothar A1 - Conti, Elena A1 - Lenhard, Michael T1 - Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses JF - eLife N2 - 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. Y1 - 2016 U6 - https://doi.org/10.7554/eLife.17956 SN - 2050-084X VL - 5 PB - eLife Sciences Publications CY - Cambridge ER - TY - JOUR A1 - Sicard, Adrien A1 - Stacey, Nicola A1 - Hermann, Katrin A1 - Dessoly, Jimmy A1 - Neuffer, Barbara A1 - Bäurle, Isabel A1 - Lenhard, Michael T1 - Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella JF - The plant cell N2 - 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. Y1 - 2011 U6 - https://doi.org/10.1105/tpc.111.088237 SN - 1040-4651 VL - 23 IS - 9 SP - 3156 EP - 3171 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Mathieu-Rivet, Elodie A1 - Gévaudant, Frédéric A1 - Sicard, Adrien A1 - Salar, Sophie A1 - Do, Phuc Thi A1 - Mouras, Armand A1 - Fernie, Alisdair R. A1 - Gibon, Yves A1 - Rothan, Christophe A1 - Chevalier, Christian A1 - Hernould, Michel T1 - Functional analysis of the anaphase promoting complex activator CCS52A highlights the crucial role of endo- reduplication for fruit growth in tomato Y1 - 2010 SN - 1365-313X ER - TY - JOUR A1 - Eldridge, Tilly A1 - Langowski, Lukasz A1 - Stacey, Nicola A1 - Jantzen, Friederike A1 - Moubayidin, Laila A1 - Sicard, Adrien A1 - Southam, Paul A1 - Kennaway, Richard A1 - Lenhard, Michael A1 - Coen, Enrico S. A1 - Ostergaard, Lars T1 - Fruit shape diversity in the Brassicaceae is generated by varying patterns of anisotropy JF - Development : Company of Biologists N2 - 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. KW - Brassicaceae KW - Capsella KW - Arabidopsis KW - Fruit shape KW - Modelling KW - Anisotropic growth Y1 - 2016 U6 - https://doi.org/10.1242/dev.135327 SN - 0950-1991 SN - 1477-9129 VL - 143 SP - 3394 EP - 3406 PB - Company of Biologists Limited CY - Cambridge ER - TY - JOUR A1 - Sicard, Adrien A1 - Kappel, Christian A1 - Josephs, Emily B. A1 - Wha Lee, Young A1 - Marona, Cindy A1 - Stinchcombe, John R. A1 - Wright, Stephen I. A1 - Lenhard, Michael T1 - Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella JF - Nature Communications N2 - 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. Y1 - 2015 U6 - https://doi.org/10.1038/ncomms8960 SN - 2041-1723 VL - 6 PB - Nature Publishing Group CY - London ER - TY - JOUR A1 - Sicard, Adrien A1 - Kappel, Christian A1 - Josephs, Emily B. A1 - Lee, Young Wha A1 - Marona, Cindy A1 - Stinchcombe, John R. A1 - Wright, Stephen I. A1 - Lenhard, Michael T1 - Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella JF - Nature Communications N2 - 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. Y1 - 2015 U6 - https://doi.org/10.1038/ncomms8960 SN - 2041-1723 VL - 6 PB - Nature Publ. Group CY - London ER - TY - JOUR A1 - Bollier, Norbert A1 - Sicard, Adrien A1 - Leblond, Julie A1 - Latrasse, David A1 - Gonzalez, Nathalie A1 - Gevaudant, Frederic A1 - Benhamed, Moussa A1 - Raynaud, Cecile A1 - Lenhard, Michael A1 - Chevalier, Christian A1 - Hernould, Michel A1 - Delmas, Frederic T1 - 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 JF - The plant cell N2 - 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. Y1 - 2018 U6 - https://doi.org/10.1105/tpc.17.00653 SN - 1040-4651 SN - 1532-298X VL - 30 IS - 1 SP - 83 EP - 100 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Jantzen, Friederike A1 - Wozniak, Natalia Joanna A1 - Kappel, Christian A1 - Sicard, Adrien A1 - Lenhard, Michael T1 - A high‑throughput amplicon‑based method for estimating outcrossing rates JF - Plant Methods N2 - 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. KW - Outcrossing KW - Mixed mating KW - Outcrossing rate KW - Capsella KW - Amplicon sequencing Y1 - 2019 U6 - https://doi.org/10.1186/s13007-019-0433-9 SN - 1746-4811 VL - 15 IS - 47 PB - BioMed Central CY - London ER -