The Arabidopsis Receptor Kinase ZAR1 Is Required for Zygote Asymmetric Division and Its Daughter Cell Fate

Abstract

Asymmetric division of zygote is critical for pattern formation during early embryogenesis in plants and animals. It requires integration of the intrinsic and extrinsic cues prior to and/or after fertilization. How these cues are translated into developmental signals is poorly understood. Here through genetic screen for mutations affecting early embryogenesis, we identified an Arabidopsis mutant, zygotic arrest 1 (zar1), in which zygote asymmetric division and the cell fate of its daughter cells were impaired. ZAR1 encodes a member of the RLK/Pelle kinase family. We demonstrated that ZAR1 physically interacts with Calmodulin and the heterotrimeric G protein Gβ, and ZAR1 kinase is activated by their binding as well. ZAR1 is specifically expressed micropylarly in the embryo sac at eight-nucleate stage and then in central cell, egg cell and synergids in the mature embryo sac. After fertilization, ZAR1 is accumulated in zygote and endosperm. The disruption of ZAR1 and AGB1 results in short basal cell and an apical cell with basal cell fate. These data suggest that ZAR1 functions as a membrane integrator for extrinsic cues, Ca2+ signal and G protein signaling to regulate the division of zygote and the cell fate of its daughter cells in Arabidopsis.

Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote

“…The membrane-associated IRAK/Pelle kinase SSP, required for YDA/MPK3/6 activation, is thought to function in assembly of the receptor complex (based on the function of mammalian homologs) rather than as receptor itself (Bayer et al 2009). A recent study shows that the membrane receptor kinase ZAR1 is required for normal WRKY2 and WOX8 expression levels in the zygote and interacts physically with SSP in pull-down assays (Yu et al 2016), but whether ZAR1 might provide the receptor for YDA/MAPK signaling still needs to be addressed. The recently discovered ESF1 peptides that are produced mainly by the central cell and the endosperm (nutrient tissue that surrounds the embryo) promote WOX8 expression and zygote asymmetry (Costa et al 2014).…”

“…Activation of YDA/MPK signaling in the zygote requires the membrane-associated receptor-like kinase SHORT SUSPEN-SOR (SSP), whose mRNA is delivered from the sperm cell and translated in the zygote (Bayer et al 2009). In addition, the EMBRYO-SURROUNDING FACTOR1 (ESF1) peptide and the plasma membrane receptor kinase ZY-GOTE ARREST1 (ZAR1) are required for WOX8 expression and zygote development (Costa et al 2014;Yu et al 2016). These examples imply that zygote development depends on external cues.…”

ZYGOTE‐ARREST 3 that encodes the tRNA ligase is essential for zygote division in Arabidopsis

“…In flowering plants, division of the zygote after fusion of the egg and the sperm cells initiates embryogenesis. Several genes regulating zygote division have been identified, including factors in cell cycle regulation (Shen et al ; Xu et al ; Lin et al ; Ronceret et al ; Andreuzza et al ), protein degradation (Guo et al ), RNA editing and processing (Li et al ; Yu et al ) and signal transduction (Yu et al ). The zyg3‐1 mutant described in this study exhibits a tight zygote‐lethal phenotype, since no zygote division was observed in a large population of ovules examined.…”

Does Early Embryogenesis in Eudicots and Monocots Involve the Same Mechanism and Molecular Players?

“…Homozygous zar1 leads to embryo abortion, but does not affect male or female gametogenesis. Phenotype analysis revealed that zar1 zygote elongation is normal, but its division becomes symmetrical, resulting in the failure of embryogenesis (Yu et al, 2016). NtDRP, encoding a dynamin-related protein, was found to control zygote division orientation in tobacco.…”

“…Defective zar1 does not affect the process of zygote elongation but disrupts the first asymmetric division. Accordingly, both apical and basal cell fates were impaired, suggesting that intrinsic factors are required for asymmetrical division and the division itself is likely involved in daughter cell fate determination (Yu et al, 2016). Moreover, central cell-derived peptide ESF1 was recently shown to be required for basal cell lineage development acting through the YDA MAPK pathway in Arabidopsis.…”