Abstract
The highly variable and species-specific pollen surface patterns are formed by sporopollenin accumulation. The template for sporopollenin deposition and polymerization is the primexine that appears on the tetrad surface, but the mechanism(s) by which primexine guides exine patterning remain elusive. Here, we report that the Poaceae-specific EXINE PATTERN DESIGNER 1 (EPAD1), which encodes a nonspecific lipid transfer protein, is required for primexine integrity and pollen exine patterning in rice (Oryza sativa). Disruption of EPAD1 leads to abnormal exine pattern and complete male sterility, although sporopollenin biosynthesis is unaffected. EPAD1 is specifically expressed in male meiocytes, indicating that reproductive cells exert genetic control over exine patterning. EPAD1 possesses an N-terminal signal peptide and three redundant glycosylphosphatidylinositol (GPI)-anchor sites at its C terminus, segments required for its function and localization to the microspore plasma membrane. In vitro assays indicate that EPAD1 can bind phospholipids. We propose that plasma membrane lipids bound by EPAD1 may be involved in recruiting and arranging regulatory proteins in the primexine to drive correct exine deposition. Our results demonstrate that EPAD1 is a meiocyte-derived determinant that controls primexine patterning in rice, and its orthologs may play a conserved role in the formation of grass-specific exine pattern elements.
Highlights
Pollen is the male gametophyte of flowering plants and is enclosed within a multi-layered cell wall whose structure directs successful pollination and provides physical and chemical resistance against environmental stresses (Edlund et al, 2004; Jiang et al, 2013; Shi et al, 2015)
We identified the male-sterile mutant exine pattern designer 1 from a rice mutant library (Chen et al, 2006). epad1 plants exhibited normal vegetative development, and normal panicle and spikelet morphology (Figures 1A to 1C)
The epad1 mutation caused severe defects in pollen exine formation, the anther cuticle and Ubisch body looked similar to the wild type (Figure 4), suggesting that EXINE PATTERN DESIGNER 1 (EPAD1) is not required for biosynthesis and allocation of sporopollenin precursors
Summary
Pollen is the male gametophyte of flowering plants and is enclosed within a multi-layered cell wall whose structure directs successful pollination and provides physical and chemical resistance against environmental stresses (Edlund et al, 2004; Jiang et al, 2013; Shi et al, 2015). In rice (Oryza sativa), mutation in OsDEX1 impairs callose degradation and primexine formation (Yu et al, 2016), while DEFECTIVE POLLEN WALL 3 (DPW3) encodes a membrane alpha integrin-like protein whose loss of function affects callose deposition and primexine formation, resulting in pollen abortion (Mondol et al, 2020). Most of these genes are exclusively or predominantly expressed in the tapetum, indicating that the tapetum plays an essential role, in producing sporopollenin precursors, and in controlling sporopollenin deposition and assembly (Ariizumi and Toriyama, 2011; Quilichini et al, 2015). Our data provide substantial molecular evidence that the rice PMC plays an essential role in the species-specific exine pattern formation
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