A Rice Glutamyl-tRNA Synthetase Modulates Early Anther Cell Division and Patterning.

Xiujuan Yang,Gang Li,Wanqi Liang,Dabing Zhang,Yuesheng Tian,Yu Song

doi:10.1104/pp.18.00110

Xiujuan Yang, Gang Li + Show 4 more

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https://doi.org/10.1104/pp.18.00110

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Abstract

Aminoacyl-tRNA synthetases (aaRSs) have housekeeping roles in protein synthesis, but little is known about how these aaRSs are involved in organ development. Here, we report that a rice (Oryza sativa) glutamyl-tRNA synthetase (OsERS1) maintains proper somatic cell organization and limits the overproliferation of male germ cells during early anther development. The expression of OsERS1 is specifically detectable in meristematic layer 2-derived cells of the early anther, and osers1 anthers exhibit overproliferation and disorganization of layer 2-derived cells, producing fused lobes and extra germ cells in early anthers. The conserved biochemical function of OsERS1 in ligating glutamate to tRNAGlu is enhanced by its cofactor aaRS OsARC. Furthermore, metabolomics profiling revealed that OsERS1 is an important node for multiple metabolic pathways, indicated by the accumulation of amino acids and tricarboxylic acid cycle components in osers1 anthers. Notably, the anther defects of the osers1 mutant are causally associated with the abnormal accumulation of hydrogen peroxide, which can reconstitute the osers1 phenotype when applied to wild-type anthers. Collectively, these findings demonstrate how aaRSs affect male organ development in plants, likely through protein synthesis, metabolic homeostasis, and redox status.

Highlights

Aminoacyl-tRNA synthetases have housekeeping roles in protein synthesis, but little is known about how these aaRSs are involved in organ development
To explore the mechanisms underlying anther development in the cereal model plant rice, we identified a new male-sterile mutant, oryza sativa glutamyl-tRNA synthetase, because of the mutation in GlutamyltRNA Synthetase1
At stage 3, transverse section analysis showed that each wild-type anther formed ∼6.3 archesporial cells (n = 11) enringed by a single layer of primary parietal cells (PPCs), while each osers1 anther produced ∼10 archesporial-like cells (n = 12) enringed by PPCs organized in an irregular mosaic pattern (Fig. 1, C, D, I, and K)

Summary

Introduction

Aminoacyl-tRNA synthetases (aaRSs) have housekeeping roles in protein synthesis, but little is known about how these aaRSs are involved in organ development. Rice MICROSPORELESS1 (MIL1) and maize Male Sterile Converted Anther (MSCA1) are homologs to two Arabidopsis GRXs, ROXY1 and ROXY2 These GRXs have been shown to regulate abaxial-adaxial anther lobe formation and the differentiation of microsporocytes, suggesting that GRXs trigger archesporial fate determination by controlling redox status. Recent studies have shown the function of cell surface-localized leucine-rich repeat receptor-like kinases (LRR-RLKs) and their ligands, such as rice MULTIPLE SPOROCYTE1 (MSP1) and TAPETAL DETERMINANT1-LIKE A (OsTDL1A)/MIL2, in determining early anther cell fate These are orthologous to Arabidopsis EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS and TAPETAL DETERMINANT1, respectively, and function in specifying anther cell identity and controlling cell numbers of tapetum and microsporocytes (Canales et al, 2002; Zhao et al, 2002, 2008; Nonomura et al, 2003; Yang et al, 2003; Hong et al, 2012a; Zhang and Yang, 2014). MSP1 and OsTDL1A were suggested to exert their effects in early anther cell differentiation via modulating redox status in rice (Yang et al, 2016)

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