Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis

LEAFY COTYLEDON2 (LEC2) is a central regulator of embryogenesis sufficient to induce somatic cells to form embryos when expressed ectopically. Here, we analyze the cellular processes induced by LEC2, a B3 domain transcription factor, that may underlie its ability to promote somatic embryogenesis. We show auxin-responsive genes are induced after LEC2 activation in seedlings. Genes encoding enzymes involved in auxin biosynthesis, YUC2 and YUC4, are activated within 1 h after induction of LEC2 activity, and YUC4 appears to be a direct transcriptional target of LEC2. We also show ectopic LEC2 expression induces accumulation of seed storage protein and oil bodies in vegetative and reproductive organs, events that normally occur during the maturation phase of embryogenesis. Furthermore, LEC2 activates seed protein genes before an increase in RNAs encoding LEC1 or FUS3 is observed. Thus, LEC2 causes rapid changes in auxin responses and induces cellular differentiation characteristic of the maturation phase. The relevance of these changes to the ability of LEC2 to promote somatic embryogenesis is discussed.

[1]  R. Bicknell,et al.  Understanding Apomixis: Recent Advances and Remaining Conundrums , 2004, The Plant Cell Online.

[2]  A. Yamamoto,et al.  LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. , 2005, Plant & cell physiology.

[3]  D. Meinke,et al.  Leafy Cotyledon Mutants of Arabidopsis. , 1994, The Plant cell.

[4]  Yukihisa Shimada,et al.  Brassinolide Induces IAA5, IAA19, and DR5, a Synthetic Auxin Response Element in Arabidopsis, Implying a Cross Talk Point of Brassinosteroid and Auxin Signaling , 2003, Plant Physiology.

[5]  N. Nagata,et al.  TANMEI/EMB2757 Encodes a WD Repeat Protein Required for Embryo Development in Arabidopsis1 , 2005, Plant Physiology.

[6]  Sébastien Baud,et al.  An integrated overview of seed development in Arabidopsis thaliana ecotype WS , 2002 .

[7]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[8]  Xiaofeng Cao,et al.  Interplay between Two Epigenetic Marks DNA Methylation and Histone H3 Lysine 9 Methylation , 2002, Current Biology.

[9]  L. Kunst,et al.  The natural genetic variation of the fatty-acyl composition of seed oils in different ecotypes of Arabidopsis thaliana. , 1999, Phytochemistry.

[10]  J. Zimmerman.  Somatic Embryogenesis: A Model for Early Development in Higher Plants. , 1993, The Plant cell.

[11]  P. Hedden,et al.  Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. , 2000, Plant physiology.

[12]  Masanori Okamoto,et al.  The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. , 2004, Developmental cell.

[13]  Tobias Würschum,et al.  Genetic Regulation of Embryonic Pattern Formation , 2004, The Plant Cell Online.

[14]  S. E. Perry,et al.  Expression and Maintenance of Embryogenic Potential Is Enhanced through Constitutive Expression of AGAMOUS-Like 151 , 2003, Plant Physiology.

[15]  Rudolf Schmid,et al.  The study of plant structure: Principles and selected methods , 1981 .

[16]  R. Bronner.  Simultaneous demonstration of lipids and starch in plant tissues. , 1975, Stain Technology.

[17]  M. Gaj,et al.  Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh , 2007, Planta.

[18]  T. Laux,et al.  Somatic embryogenesis from Arabidopsis shoot apical meristem mutants , 2002, Planta.

[19]  L. Lepiniec,et al.  LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[20]  M. Koornneef,et al.  Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. , 1998, Genetics.

[21]  F. Parcy,et al.  AtGA3ox2, a Key Gene Responsible for Bioactive Gibberellin Biosynthesis, Is Regulated during Embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis1 , 2004, Plant Physiology.

[22]  L. Comai,et al.  Transcriptional activities in dry seed nuclei indicate the timing of the transition from embryogeny to germination. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Yunde Zhao,et al.  Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. , 2006, Genes & development.

[24]  Robert B Goldberg,et al.  Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Matthew R. Tucker,et al.  Sexual and Apomictic Reproduction in Hieracium subgenus Pilosella Are Closely Interrelated Developmental Pathways Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011742. , 2003, The Plant Cell Online.

[26]  M. Gaj.  Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana , 2004, Plant Cell, Tissue and Organ Culture.

[27]  H. Goodman,et al.  Isolation of the Arabidopsis ABI3 gene by positional cloning. , 1992, The Plant cell.

[28]  J. Chory,et al.  A role for flavin monooxygenase-like enzymes in auxin biosynthesis. , 2001, Science.

[29]  Robert B Goldberg,et al.  Arabidopsis LEAFY COTYLEDON1 Is Sufficient to Induce Embryo Development in Vegetative Cells , 1998, Cell.

[30]  J. Harada.  Role of Arabidopsis LEAFY COTYLEDON genes in seed development , 2001 .

[31]  A. Khan.  Gibberellins and seed development. , 1982 .

[32]  M. West,et al.  LEAFY COTYLEDON1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis. , 1994, The Plant cell.

[33]  Jon Penterman,et al.  DEMETER DNA Glycosylase Establishes MEDEA Polycomb Gene Self-Imprinting by Allele-Specific Demethylation , 2006, Cell.

[34]  Yunde Zhao,et al.  Auxin Synthesized by the YUCCA Flavin Monooxygenases Is Essential for Embryogenesis and Leaf Formation in Arabidopsis[W] , 2007, The Plant Cell Online.

[35]  Mikihisa Umehara,et al.  Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. , 2003, The Plant journal : for cell and molecular biology.

[36]  P. Herrmann,et al.  FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[37]  Huai Wang,et al.  The Embryo MADS Domain Protein AGAMOUS-Like 15 Directly Regulates Expression of a Gene Encoding an Enzyme Involved in Gibberellin Metabolism , 2004, The Plant Cell Online.

[38]  R. Dietrich,et al.  Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings. , 1992, The Plant cell.

[39]  H. Koop,et al.  Somatic embryogenesis in cultured immature zygotic embryos and leaf protoplasts of Arabidopsis thaliana ecotypes , 1997, Planta.

[40]  Thomas L. Reynolds.  Pollen embryogenesis , 2004, Plant Molecular Biology.

[41]  L. Lepiniec,et al.  LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves , 2005, FEBS letters.