COPII Components Sar1b and Sar1c Play Distinct Yet Interchangeable Roles in Pollen Development.

Xin Liang,Shan-Wei Li,Yan Zhang,Li-Min Gong,Sha Li

doi:10.1104/pp.20.00159

Abstract

The development of pollen is a prerequisite for double fertilization in angiosperms. Coat protein complex II (COPII) mediates anterograde transport of vesicles from the endoplasmic reticulum to the Golgi. Components of the COPII complex have been reported to regulate either sporophytic or gametophytic control of pollen development. The Arabidopsis (Arabidopsis thaliana) genome encodes five Sar1 isoforms, the small GTPases essential for COPII formation. By using a dominant negative approach, Sar1 isoforms were proposed to have distinct cargo specificity despite their sequence similarity. Here, we examined the functions of three Sar1 isoforms through analysis of transfer DNA insertion mutants and CRISPR/Cas9-generated mutants. We report that functional loss of Sar1b caused malfunction of tapetum, leading to male sterility. Ectopic expression of Sar1c could compensate for Sar1b loss of function in sporophytic control of pollen development, suggesting that they are interchangeable. Functional distinction between Sar1b and Sar1c may have resulted from their different gene transcription levels based on expression analyses. On the other hand, Sar1b and Sar1c redundantly mediate male gametophytic development such that the sar1b;sar1c microspores aborted at anther developmental stage 10. This study uncovers the role of Sar1 isoforms in both sporophytic and gametophytic control of pollen development. It also suggests that distinct functions of Sar1 isoforms may be caused by their distinct transcription programs.

Highlights

Pollen development is synergistically controlled by sporophytic and gametophytic factors (McCormick, 2004; Chang et al, 2011)
Function of the tapetum is controlled by an evolutionarily conserved transcriptional cascade (Wilson and Zhang, 2009; Zhu et al, 2011; Zhu et al, 2015), as well as proteins involved in intercellular signaling, such as Receptor-like Protein Kinase 2 (RPK2), NO PRIMEXINE AND PLASMA MEMBRANE UNDULATION (NPU), the secreted small peptide CLAVATA3/ESR-RELATED19 (CLE19), ATP binding cassette (ABC)
Genes critical for the gametophytic control of pollen development (Borg et al, 2009) have been identified. They mostly encode proteins participating in endomembrane dynamics, such as proteins mediating PI3P-PI(3,5)P2 conversion (Whitley et al, 2009; Zhang et al, 2018), protein sorting (Van Damme et al, 2006; Backues et al, 2010; Wang et al, 2013; Feng et al, 2017), and vesicle trafficking (Backues et al, 2010; El-Kasmi et al, 2011)

Summary

Introduction

Pollen development is synergistically controlled by sporophytic and gametophytic factors (McCormick, 2004; Chang et al, 2011). The sporophytic tapetum, adjacent to developing microspores, is critical for pollen development through its secretion at early stages and programmed cell death (PCD) at late stages (Parish and Li, 2010). Genes critical for the gametophytic control of pollen development (Borg et al, 2009) have been identified. They mostly encode proteins participating in endomembrane dynamics, such as proteins mediating PI3P-PI(3,5)P2 conversion (Whitley et al, 2009; Zhang et al, 2018), protein sorting (Van Damme et al, 2006; Backues et al, 2010; Wang et al, 2013; Feng et al., 2017), and vesicle trafficking (Backues et al, 2010; El-Kasmi et al, 2011).

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