Independent parental contributions initiate zygote polarization in Arabidopsis thaliana

Embryogenesis of flowering plants is initiated by polarization of the zygote, a prerequisite for correct axis formation in the embryo. Zygote polarity and the decision between embryonic and non-embryonic development in the daughter cells is controlled by a MITOGEN-ACTIVATING PROTEIN (MAP) kinase signaling pathway including the MAPKK kinase YODA (YDA). Upstream of YDA act two members of the BRASINOSTEROID SIGNALING KINASE (BSK) family, BSK1 and BSK2. These membrane-associated proteins serve as signaling relay linking receptor kinase complexes with intracellular signaling cascades. The receptor kinases acting upstream of BSK1 and BSK2 in the zygote, however, have so far not been identified. Instead, YDA can in part be activated by the non-canonical BSK family member SHORT SUSPENSOR (SSP) that is contributed by the sperm cell during fertilization. Here, we show that the receptor kinase ERECTA plays a crucial role in zygote polarization as maternally contributed part of the embryonic YDA pathway. SSP on the other hand provides an independent, paternal input to YDA activation, outlining a Y-shaped pathway. We conclude that two independent parental contributions initiate zygote polarization and control suspensor formation and embryonic development.

[1]  Yanru Ren,et al.  Equal parental contribution to the transcriptome is not equal control of embryogenesis , 2020, Nature Plants.

[2]  U. Gowik,et al.  Metabolic Labeling of RNAs Uncovers Hidden Features and Dynamics of the Arabidopsis Transcriptome[CC-BY] , 2020, Plant Cell.

[3]  Martin Bayer,et al.  Square one: zygote polarity and early embryogenesis in flowering plants. , 2019, Current opinion in plant biology.

[4]  Teva Vernoux,et al.  WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis , 2019, Nature Communications.

[5]  Yanbing Cheng,et al.  Two-Step Maternal-to-Zygotic Transition with Two-Phase Parental Genome Contributions. , 2019, Developmental cell.

[6]  W. Lukowitz,et al.  Constitutive signaling activity of a receptor-associated protein links fertilization with embryonic patterning in Arabidopsis thaliana , 2019, Proceedings of the National Academy of Sciences.

[7]  T. Laux,et al.  Maternal auxin supply contributes to early embryo patterning in Arabidopsis , 2018, Nature Plants.

[8]  W. Lukowitz,et al.  Maternal control of embryogenesis by MPK6 and its upstream MKK4/MKK5 in Arabidopsis , 2017, The Plant journal : for cell and molecular biology.

[9]  T. Laux,et al.  Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. , 2017, Genes & development.

[10]  K. Torii,et al.  Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling , 2017, eLife.

[11]  A. Fleming,et al.  An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens , 2016, Development.

[12]  D. Bergmann,et al.  Modulators of Stomatal Lineage Signal Transduction Alter Membrane Contact Sites and Reveal Specialization among ERECTA Kinases. , 2016, Developmental cell.

[13]  E. Shpak.  Diverse roles of ERECTA family genes in plant development. , 2013, Journal of integrative plant biology.

[14]  A. Henschen,et al.  Suspensor Length Determines Developmental Progression of the Embryo in Arabidopsis1[W][OA] , 2013, Plant Physiology.

[15]  Xiangzong Meng,et al.  A MAPK Cascade Downstream of ERECTA Receptor-Like Protein Kinase Regulates Arabidopsis Inflorescence Architecture by Promoting Localized Cell Proliferation[C][W] , 2012, Plant Cell.

[16]  M. Affolter,et al.  Fluorescent fusion protein knockout mediated by anti-GFP nanobody , 2011, Nature Structural &Molecular Biology.

[17]  Shao‐Lun Liu,et al.  Dramatic change in function and expression pattern of a gene duplicated by polyploidy created a paternal effect gene in the Brassicaceae. , 2010, Molecular biology and evolution.

[18]  Zhi-Yong Wang,et al.  Brassinosteroid signal transduction from receptor kinases to transcription factors. , 2010, Annual review of plant biology.

[19]  M. Galli,et al.  Paternal Control of Embryonic Patterning in Arabidopsis thaliana , 2009, Science.

[20]  K. Torii,et al.  The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. , 2007, Genes & development.

[21]  K. Torii,et al.  Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases , 2005, Science.

[22]  Dominique C Bergmann,et al.  Stomatal Development and Pattern Controlled by a MAPKK Kinase , 2004, Science.

[23]  K. Torii,et al.  Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation , 2004, Development.

[24]  W. Lukowitz,et al.  A MAPKK Kinase Gene Regulates Extra-Embryonic Cell Fate in Arabidopsis , 2004, Cell.

[25]  N. Mitsukawa,et al.  The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. , 1996, The Plant cell.

[26]  D. Haig.  Kin conflict in seed plants. , 1987, Trends in ecology & evolution.