TRIMETHYLGUANOSINE SYNTHASE1 mutations decanalize female germline development in Arabidopsis.

Here, we report the characterization of a plant RNA methyltransferase, orthologous to yeast trimethylguanosine synthase1 (Tgs1p) and whose downregulation was associated with apomixis in Paspalum grasses. Using phylogenetic analyses and yeast complementation, we determined that land plant genomes all encode a conserved, specific TGS1 protein. Next, we studied the role of TGS1 in female reproduction using reporter lines and loss-of-function mutants in Arabidopsis thaliana. pAtTGS1:AtTGS1 reporters showed a dynamic expression pattern. They were highly active in the placenta and ovule primordia at emergence but, subsequently, showed weak signals in the nucellus. Although expressed throughout gametophyte development, activity became restricted to the female gamete and was also detected after fertilization during embryogenesis. TGS1 depletion altered the specification of the precursor cells that give rise to the female gametophytic generation and to the sporophyte, resulting in the formation of a functional aposporous-like lineage. Our results indicate that TGS1 participates in the mechanisms restricting cell fate acquisition to a single cell at critical transitions throughout the female reproductive lineage and, thus, expand our current knowledge of the mechanisms governing female reproductive fate in plants.

[1]  J. Friml,et al.  Specification of female germline by microRNA orchestrated auxin signaling in Arabidopsis , 2022, Nature Communications.

[2]  L. Colombo,et al.  Pivotal role of STIP in ovule pattern formation and female germline development in Arabidopsis thaliana. , 2022, Development.

[3]  H. Robert,et al.  Transcriptional control of Arabidopsis seed development , 2022, Planta.

[4]  Yuan Qin,et al.  Brassinosteroid signaling regulates female germline specification in Arabidopsis , 2022, Current Biology.

[5]  K. Palme,et al.  Molecular Control of Sporophyte-Gametophyte Ontogeny and Transition in Plants , 2022, Frontiers in Plant Science.

[6]  E. Datema,et al.  A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce , 2022, Nature Genetics.

[7]  U. Grossniklaus,et al.  The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologs of BONOBO genes for cell specification. , 2021, The New phytologist.

[8]  Z. Lin,et al.  Loss-of-function alleles of ZmPLD3 cause haploid induction in maize , 2021, Nature plants.

[9]  J. Friml,et al.  Mutually opposing activity of PIN7 splicing isoforms is required for auxin-mediated tropic responses in Arabidopsis thaliana. , 2021, The New phytologist.

[10]  A. Schnittger,et al.  How to Switch from Mitosis to Meiosis: Regulation of Germline Entry in Plants. , 2021, Annual review of genetics.

[11]  Jianhua Zhang,et al.  Global Survey of Alternative Splicing in Rice by Direct RNA Sequencing During Reproductive Development: Landscape and Genetic Regulation , 2021, Rice.

[12]  K. Lee,et al.  The DME demethylase regulates sporophyte gene expression, cell proliferation, differentiation, and meristem resurrection , 2021, Proceedings of the National Academy of Sciences.

[13]  W. Cowling,et al.  A Trimethylguanosine Synthase1-like (TGS1) homologue is implicated in vernalisation and flowering time control , 2021, Theoretical and Applied Genetics.

[14]  Michael Borg,et al.  The epigenetic origin of life history transitions in plants and algae , 2021, Plant Reproduction.

[15]  L. Colombo,et al.  The emerging role of small RNAs in ovule development, a kind of magic , 2021, Plant Reproduction.

[16]  Maricel Podio,et al.  Differential Epigenetic Marks Are Associated with Apospory Expressivity in Diploid Hybrids of Paspalum rufum , 2021, Plants.

[17]  G. Jürgens,et al.  Comparative Embryogenesis in Angiosperms: Activation and Patterning of Embryonic Cell Lineages. , 2021, Annual review of plant biology.

[18]  A. Shimada,et al.  Trimethylguanosine synthase 1 (Tgs1) is involved in Swi6/HP1‐independent siRNA production and establishment of heterochromatin in fission yeast , 2021, Genes to cells : devoted to molecular & cellular mechanisms.

[19]  V. Sundaresan,et al.  Plant zygote development: recent insights and applications to clonal seeds. , 2021, Current opinion in plant biology.

[20]  M. Kater,et al.  Alternative Splicing Generates a MONOPTEROS Isoform Required for Ovule Development , 2020, Current Biology.

[21]  L. Colombo,et al.  The Importance of Cytokinins during Reproductive Development in Arabidopsis and Beyond , 2020, International journal of molecular sciences.

[22]  Y. Rong,et al.  Loss of the RNA trimethylguanosine cap is compatible with nuclear accumulation of spliceosomal snRNAs but not pre-mRNA splicing or snRNA processing during animal development , 2020, PLoS genetics.

[23]  G. Barcaccia,et al.  A Reappraisal of the Evolutionary and Developmental Pathway of Apomixis and Its Genetic Control in Angiosperms , 2020, Genes.

[24]  R. Groß-Hardt,et al.  Reproductive Multitasking: The Female Gametophyte. , 2020, Annual review of plant biology.

[25]  T. Higashiyama,et al.  Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis , 2020, bioRxiv.

[26]  A. Schmidt Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation , 2020, Genes.

[27]  S. Artandi,et al.  Loss of Human TGS1 Hypermethylase Promotes Increased Telomerase RNA and Telomere Elongation , 2020, Cell reports.

[28]  P. Ozias‐Akins,et al.  Clonal Reproduction through Seeds in Sight for Crops. , 2020, Trends in genetics : TIG.

[29]  Matthew R. Tucker,et al.  The RNA-dependent DNA methylation pathway is required to restrict SPOROCYTELESS/NOZZLE expression to specify a single female germ cell precursor in Arabidopsis , 2020, Development.

[30]  S. Pessino,et al.  A Plant-Specific TGS1 Homolog Influences Gametophyte Development in Sexual Tetraploid Paspalum notatum Ovules , 2019, Front. Plant Sci..

[31]  Xun Xu,et al.  One thousand plant transcriptomes and the phylogenomics of green plants , 2019, Nature.

[32]  T. Kohchi,et al.  Building new insights in plant gametogenesis from an evolutionary perspective , 2019, Nature Plants.

[33]  V. Brukhin,et al.  A brief note on genes that trigger components of apomixis , 2019, Journal of Biosciences.

[34]  G. Galla,et al.  Ovule Gene Expression Analysis in Sexual and Aposporous Apomictic Hypericum perforatum L. (Hypericaceae) Accessions , 2019, Front. Plant Sci..

[35]  Xiujuan Yang,et al.  Establishing a framework for female germline initiation in the plant ovule. , 2019, Journal of experimental botany.

[36]  Matthew R. Tucker,et al.  Revisiting the Female Germline and Its Expanding Toolbox. , 2019, Trends in plant science.

[37]  V. Sundaresan,et al.  A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds , 2018, Nature.

[38]  S. Pessino,et al.  The MAP3K-Coding QUI-GON JINN (QGJ) Gene Is Essential to the Formation of Unreduced Embryo Sacs in Paspalum , 2018, Front. Plant Sci..

[39]  C. Gillmor,et al.  The Times They Are A-Changin’: Heterochrony in Plant Development and Evolution , 2018, Front. Plant Sci..

[40]  Matthew R. Tucker,et al.  Asexual Female Gametogenesis Involves Contact with a Sexually-Fated Megaspore in Apomictic Hieracium1[OPEN] , 2018, Plant Physiology.

[41]  Prakash Venglat,et al.  Arabidopsis ICK/KRP cyclin-dependent kinase inhibitors function to ensure the formation of one megaspore mother cell and one functional megaspore per ovule , 2018, PLoS genetics.

[42]  K. Nakajima Be my baby: patterning toward plant germ cells. , 2018, Current opinion in plant biology.

[43]  M. Yanofsky,et al.  Ovule identity mediated by pre-mRNA processing in Arabidopsis , 2018, PLoS genetics.

[44]  J. M. Rodrigo,et al.  Temporal and spatial expression of genes involved in DNA methylation during reproductive development of sexual and apomictic Eragrostis curvula , 2017, Scientific Reports.

[45]  J. Steitz,et al.  An Exportin-1–dependent microRNA biogenesis pathway during human cell quiescence , 2017, Proceedings of the National Academy of Sciences.

[46]  Xuemei Chen,et al.  The THO Complex Non-Cell-Autonomously Represses Female Germline Specification through the TAS3-ARF3 Module , 2017, Current Biology.

[47]  J. Browse,et al.  Trimethylguanosine Synthase1 (TGS1) Is Essential for Chilling Tolerance1[OPEN] , 2017, Plant Physiology.

[48]  L. Altschmied,et al.  RWP-RK domain-containing transcription factors control cell differentiation during female gametophyte development in Arabidopsis. , 2017, The New phytologist.

[49]  P. Ozias‐Akins,et al.  Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes , 2017, Plant Reproduction.

[50]  J. Bowman,et al.  Evolution in the Cycles of Life. , 2016, Annual review of genetics.

[51]  P. Ozias‐Akins,et al.  A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant , 2015, Proceedings of the National Academy of Sciences.

[52]  G. Jürgens,et al.  Twin Plants from Supernumerary Egg Cells in Arabidopsis , 2015, Current Biology.

[53]  U. Grossniklaus,et al.  Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction , 2015, Development.

[54]  A. Aharoni,et al.  SEEDSTICK is a Master Regulator of Development and Metabolism in the Arabidopsis Seed Coat , 2014, PLoS genetics.

[55]  S. Pessino,et al.  PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway , 2014, BMC Plant Biology.

[56]  F. Martin,et al.  Hypermethylated-capped selenoprotein mRNAs in mammals , 2014, Nucleic acids research.

[57]  T. Sharbel,et al.  A Conserved Apomixis-Specific Polymorphism Is Correlated with Exclusive Exonuclease Expression in Premeiotic Ovules of Apomictic Boechera Species1[W][OPEN] , 2013, Plant Physiology.

[58]  R. Groß-Hardt,et al.  Ethylene signaling is required for synergid degeneration and the establishment of a pollen tube block. , 2013, Developmental cell.

[59]  J. Vielle-Calzada,et al.  The Classical Arabinogalactan Protein AGP18 Mediates Megaspore Selection in Arabidopsis[W][OA] , 2013, Plant Cell.

[60]  J. Bowman,et al.  KNOX2 Genes Regulate the Haploid-to-Diploid Morphological Transition in Land Plants , 2013, Science.

[61]  E. Benková,et al.  The Transcription Factors BEL1 and SPL Are Required for Cytokinin and Auxin Signaling During Ovule Development in Arabidopsis[W] , 2012, Plant Cell.

[62]  E. Bertrand,et al.  CRM1 plays a nuclear role in transporting snoRNPs to nucleoli in higher eukaryotes , 2012, Nucleus.

[63]  D. Grimanelli Epigenetic regulation of reproductive development and the emergence of apomixis in angiosperms. , 2012, Current opinion in plant biology.

[64]  Célia Baroux,et al.  Transcriptome Analysis of the Arabidopsis Megaspore Mother Cell Uncovers the Importance of RNA Helicases for Plant Germline Development , 2011, PLoS biology.

[65]  W. Friedman,et al.  Female gamete competition in an ancient angiosperm lineage , 2011, Proceedings of the National Academy of Sciences.

[66]  Ulrich C. Klostermeier,et al.  Maternal Epigenetic Pathways Control Parental Contributions to Arabidopsis Early Embryogenesis , 2011, Cell.

[67]  S. Shuman,et al.  An essential role for trimethylguanosine RNA caps in Saccharomyces cerevisiae meiosis and their requirement for splicing of SAE3 and PCH2 meiotic pre-mRNAs , 2011, Nucleic acids research.

[68]  Xiaochun Ge,et al.  Signaling and Transcriptional Control of Reproductive Development in Arabidopsis , 2010, Current Biology.

[69]  M. Lenhard,et al.  Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling , 2009, Proceedings of the National Academy of Sciences.

[70]  S. Rensing,et al.  Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution , 2009, Development.

[71]  John Chandler,et al.  DORNRÖSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo , 2009, Development.

[72]  M. Rao,et al.  Early embryonic lethality of mice with disrupted transcription cofactor PIMT/NCOA6IP/Tgs1 gene , 2009, Mechanisms of Development.

[73]  R. Groß-Hardt,et al.  Mutants with aberrant numbers of gametic cells shed new light on old questions. , 2008, Plant biology.

[74]  V. Sundaresan,et al.  Cell-Fate Switch of Synergid to Egg Cell in Arabidopsis eostre Mutant Embryo Sacs Arises from Misexpression of the BEL1-Like Homeodomain Gene BLH1[W] , 2007, The Plant Cell Online.

[75]  Cyrille Girard,et al.  Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. , 2006, Molecular biology of the cell.

[76]  T. Payne,et al.  KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium , 2004, Development.

[77]  J. Bujnicki,et al.  Sequence-structure-function relationships of Tgs1, the yeast snRNA/snoRNA cap hypermethylase. , 2003, Nucleic acids research.

[78]  M. Rao,et al.  Cloning and characterization of PIMT, a protein with a methyltransferase domain, which interacts with and enhances nuclear receptor coactivator PRIP function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[79]  S. Pessino,et al.  A rise of ploidy level induces the expression of apomixis in Paspalum notatum , 2001, Sexual Plant Reproduction.

[80]  R. Bicknell,et al.  Sexual and apomictic development in Hieracium , 1998, Sexual Plant Reproduction.

[81]  R. Schiestl,et al.  High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method , 2007, Nature Protocols.

[82]  A. Meister,et al.  An efficient screen for reproductive pathways using mature seeds of monocots and dicots. , 2000, The Plant journal : for cell and molecular biology.