The Boundary-Expressed EPIDERMAL PATTERNING FACTOR-LIKE2 Gene Encoding a Signaling Peptide Promotes Cotyledon Growth during Arabidopsis thaliana Embryogenesis

The shoot organ boundaries have important roles in plant growth and morphogenesis. It has been reported that a gene encoding a cysteine-rich secreted peptide of the EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) family, EPFL2, is expressed in the boundary domain between the two cotyledon primordia of Arabidopsis thaliana embryo. However, its developmental functions remain unknown. This study aimed to analyze the role of EPFL2 during embryogenesis. We found that cotyledon growth was reduced in its loss-of-function mutants, and this phenotype was associated with the reduction of auxin response peaks at the tips of the primordia. The reduced cotyledon size of the mutant embryo recovered in germinating seedlings, indicating the presence of a factor that acted redundantly with EPFL2 to promote cotyledon growth in late embryogenesis. Our analysis indicates that the boundary domain between the cotyledon primordia acts as a signaling center that organizes auxin response peaks and promotes cotyledon growth.

[1]  Mizuki Yamada,et al.  A ClearSee-Based Clearing Protocol for 3D Visualization of Arabidopsis thaliana Embryos , 2021, Plants.

[2]  M. Lenhard,et al.  Establishment of the Embryonic Shoot Meristem Involves Activation of Two Classes of Genes with Opposing Functions for Meristem Activities , 2020, International journal of molecular sciences.

[3]  R. Simon,et al.  A Peptide Pair Coordinates Regular Ovule Initiation Patterns with Seed Number and Fruit Size , 2019, Current Biology.

[4]  Michael D. Nodine,et al.  The embryonic transcriptome of Arabidopsis thaliana , 2018, bioRxiv.

[5]  E. Shpak,et al.  EPFL Signals in the Boundary Region of the SAM Restrict Its Size and Promote Leaf Initiation1[OPEN] , 2018, Plant Physiology.

[6]  K. Torii,et al.  Stem development through vascular tissues: EPFL-ERECTA family signaling that bounces in and out of phloem. , 2017, Journal of experimental botany.

[7]  D. Weijers,et al.  Tissue and Organ Initiation in the Plant Embryo: A First Time for Everything. , 2016, Annual review of cell and developmental biology.

[8]  K. Torii,et al.  A Secreted Peptide and Its Receptors Shape the Auxin Response Pattern and Leaf Margin Morphogenesis , 2016, Current Biology.

[9]  S. Hepworth,et al.  Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants , 2015, Front. Plant Sci..

[10]  E. Shpak,et al.  ERECTA family genes regulate development of cotyledons during embryogenesis , 2014, FEBS letters.

[11]  R. Simon,et al.  How boundaries control plant development. , 2014, Current opinion in plant biology.

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

[13]  S. Masiero,et al.  An integrative model of the control of ovule primordia formation. , 2013, The Plant journal : for cell and molecular biology.

[14]  K. Torii Mix-and-match: ligand-receptor pairs in stomatal development and beyond. , 2012, Trends in plant science.

[15]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[16]  M. Matsui,et al.  CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. , 2011, The Plant journal : for cell and molecular biology.

[17]  P. Prusinkiewicz,et al.  Model for the regulation of Arabidopsis thaliana leaf margin development , 2011, Proceedings of the National Academy of Sciences.

[18]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[19]  G. Horiguchi,et al.  Analysis of Leaf Development in fugu Mutants of Arabidopsis Reveals Three Compensation Modes That Modulate Cell Expansion in Determinate Organs1[W] , 2007, Plant Physiology.

[20]  M. Aida,et al.  Genetic control of shoot organ boundaries. , 2006, Current opinion in plant biology.

[21]  E. Meyerowitz,et al.  Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem , 2005, Current Biology.

[22]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[23]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[24]  M. Aida,et al.  Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. , 1999, Development.

[25]  J. Long,et al.  The development of apical embryonic pattern in Arabidopsis. , 1998, Development.

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