TY - JOUR A1 - Zhang, Yunming A1 - Ramming, Anna A1 - Heinke, Lisa A1 - Altschmied, Lothar A1 - Slotkin, R. Keith A1 - Becker, Jörg D. A1 - Kappel, Christian A1 - Lenhard, Michael T1 - The poly(A) polymerase PAPS1 interacts with the RNA-directed DNA-methylation pathway in sporophyte and pollen development JF - The plant journal N2 - 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. KW - poly(A) polymerase KW - RNA-directed DNA methylation KW - pollen development KW - siRNAs KW - transposable elements KW - gynoecium development KW - Arabidopsis thaliana Y1 - 2019 U6 - https://doi.org/10.1111/tpj.14348 SN - 0960-7412 SN - 1365-313X VL - 99 IS - 4 SP - 655 EP - 672 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Vi, Son Lang A1 - Trost, Gerda A1 - Lange, Peggy A1 - Czesnick, Hjördis A1 - Rao, Nishta A1 - Lieber, Diana A1 - Laux, Thomas A1 - Gray, William M. A1 - Manley, James L. A1 - Groth, Detlef A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response JF - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA N2 - Polyadenylation of pre-mRNAs is critical for efficient nuclear export, stability, and translation of the mature mRNAs, and thus for gene expression. The bulk of pre-mRNAs are processed by canonical nuclear poly(A) polymerase (PAPS). Both vertebrate and higher-plant genomes encode more than one isoform of this enzyme, and these are coexpressed in different tissues. However, in neither case is it known whether the isoforms fulfill different functions or polyadenylate distinct subsets of pre-mRNAs. Here we show that the three canonical nuclear PAPS isoforms in Arabidopsis are functionally specialized owing to their evolutionarily divergent C-terminal domains. A strong loss-of-function mutation in PAPS1 causes a male gametophytic defect, whereas a weak allele leads to reduced leaf growth that results in part from a constitutive pathogen response. By contrast, plants lacking both PAPS2 and PAPS4 function are viable with wild-type leaf growth. Polyadenylation of SMALL AUXIN UP RNA (SAUR) mRNAs depends specifically on PAPS1 function. The resulting reduction in SAUR activity in paps1 mutants contributes to their reduced leaf growth, providing a causal link between polyadenylation of specific pre-mRNAs by a particular PAPS isoform and plant growth. This suggests the existence of an additional layer of regulation in plant and possibly vertebrate gene expression, whereby the relative activities of canonical nuclear PAPS isoforms control de novo synthesized poly(A) tail length and hence expression of specific subsets of mRNAs. Y1 - 2013 U6 - https://doi.org/10.1073/pnas.1303967110 SN - 0027-8424 VL - 110 IS - 34 SP - 13994 EP - 13999 PB - NATL ACAD SCIENCES CY - WASHINGTON ER - TY - JOUR A1 - Trost, Gerda A1 - Vi, Son Lang A1 - Czesnick, Hjördis A1 - Lange, Peggy A1 - Holton, Nick A1 - Giavalisco, Patrick A1 - Zipfel, Cyril A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Arabidopsis poly(A) polymerase PAPS1 limits founder-cell recruitment to organ primordia and suppresses the salicylic acid-independent immune response downstream of EDS1/PAD4 JF - The plant journal N2 - 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. KW - poly(A) polymerase KW - founder-cell recruitment KW - organ growth KW - polyadenylation Y1 - 2014 U6 - https://doi.org/10.1111/tpj.12421 SN - 0960-7412 SN - 1365-313X VL - 77 IS - 5 SP - 688 EP - 699 PB - Wiley-Blackwell CY - Hoboken ER - TY - JOUR A1 - Tran, Quan Hong A1 - Bui, Ngoc Hong A1 - Kappel, Christian A1 - Dau, Nga Thi Ngoc A1 - Nguyen, Loan Thi A1 - Tran, Thuy Thi A1 - Khanh, Tran Dang A1 - Trung, Khuat Huu A1 - Lenhard, Michael A1 - Vi, Son Lang T1 - 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 JF - Genes N2 - 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. KW - EMS KW - MutMap KW - mutagenesis KW - CLE7 KW - tropical maize KW - fasciation KW - mapping Y1 - 2020 U6 - https://doi.org/10.3390/genes11030281 SN - 2073-4425 VL - 11 IS - 3 SP - 1 EP - 14 PB - MDPI CY - Basel ER - TY - JOUR A1 - Tedder, Andrew A1 - Carleial, Samuel A1 - Golebiewska, Martyna A1 - Kappel, Christian A1 - Shimizu, Kentaro K. A1 - Stift, Marc T1 - Evolution of the Selfing Syndrome in Arabis alpina (Brassicaceae) JF - PLoS one N2 - 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. Y1 - 2015 U6 - https://doi.org/10.1371/journal.pone.0126618 SN - 1932-6203 VL - 10 IS - 6 PB - PLoS CY - San Fransisco 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 - 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 - 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 - 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 -