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 - GEN A1 - Zhang, Yunming A1 - Lenhard, Michael T1 - Exiting Already? Molecular Control of Cell-Proliferation Arrest in Leaves: Cutting Edge T2 - Molecular plant Y1 - 2017 U6 - https://doi.org/10.1016/j.molp.2017.05.004 SN - 1674-2052 SN - 1752-9867 VL - 10 SP - 909 EP - 911 PB - Cell Press CY - Cambridge ER - TY - JOUR A1 - Tsukaya, Hirokazu A1 - Byrne, Mary E. A1 - Horiguchi, Gorou A1 - Sugiyama, Munetaka A1 - Van Lijsebettens, Mieke A1 - Lenhard, Michael T1 - How do 'housekeeping' genes control organogenesis?-unexpected new findings on the role of housekeeping genes in cell and organ differentiation JF - Journal of plant research N2 - In recent years, an increasing number of mutations in what would appear to be 'housekeeping genes' have been identified as having unexpectedly specific defects in multicellular organogenesis. This is also the case for organogenesis in seed plants. Although it is not surprising that loss-of-function mutations in 'housekeeping' genes result in lethality or growth retardation, it is surprising when (1) the mutant phenotype results from the loss of function of a 'housekeeping' gene and (2) the mutant phenotype is specific. In this review, by defining housekeeping genes as those encoding proteins that work in basic metabolic and cellular functions, we discuss unexpected links between housekeeping genes and specific developmental processes. In a surprising number of cases housekeeping genes coding for enzymes or proteins with functions in basic cellular processes such as transcription, post-transcriptional modification, and translation affect plant development. KW - Development KW - Housekeeping genes KW - Post-transcriptional modification KW - RNAPII KW - Pre-mRNA splicing KW - Ribosome KW - 3 '-end processing KW - Transcription KW - Translation Y1 - 2013 U6 - https://doi.org/10.1007/s10265-012-0518-2 SN - 0918-9440 VL - 126 IS - 1 SP - 3 EP - 15 PB - Springer CY - Tokyo 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 - 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 - 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 - Sicard, Adrien A1 - Lenhard, Michael T1 - The selfing syndrome a model for studying the genetic and evolutionary basis of morphological adaptation in plants JF - Annals of botany N2 - Background In angiosperm evolution, autogamously selfing lineages have been derived from outbreeding ancestors multiple times, and this transition is regarded as one of the most common evolutionary tendencies in flowering plants. In most cases, it is accompanied by a characteristic set of morphological and functional changes to the flowers, together termed the selfing syndrome. Two major areas that have changed during evolution of the selfing syndrome are sex allocation to male vs. female function and flower morphology, in particular flower (mainly petal) size and the distance between anthers and stigma. Scope A rich body of theoretical, taxonomic, ecological and genetic studies have addressed the evolutionary modification of these two trait complexes during or after the transition to selfing. Here, we review our current knowledge about the genetics and evolution of the selfing syndrome. Conclusions We argue that because of its frequent parallel evolution, the selfing syndrome represents an ideal model for addressing basic questions about morphological evolution and adaptation in flowering plants, but that realizing this potential will require the molecular identification of more of the causal genes underlying relevant trait variation. KW - Evolution KW - selfing syndrome KW - autogamy KW - pollen-to-ovule ratio KW - flower size KW - herkogamy KW - quantitative trait loci KW - self-incompatibility Y1 - 2011 U6 - https://doi.org/10.1093/aob/mcr023 SN - 0305-7364 SN - 1095-8290 VL - 107 IS - 9 SP - 1433 EP - 1443 PB - Oxford Univ. Press CY - Oxford ER - TY - GEN A1 - Sicard, Adrien A1 - Lenhard, Michael T1 - Capsella T2 - Current biology Y1 - 2018 U6 - https://doi.org/10.1016/j.cub.2018.06.033 SN - 0960-9822 SN - 1879-0445 VL - 28 IS - 17 SP - R920 EP - R921 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 -