RMS2 Encoding a GDSL Lipase Mediates Lipid Homeostasis in Anthers to Determine Rice Male Fertility.

Liqun Tang,Shufan Li,Xiaohong Tong,Zhiyong Li,Jialin Li,Juan Zhao,Jian Zhang,Yazhou Shu,Huimei Wang,Jinglin Li,Yifeng Wang,Xixi Liu,Tuan Long,Jie Tang,Hao Liu,Yongzhong Wu

doi:10.1104/pp.19.01487

Abstract

Plant male gametogenesis is a coordinated effort involving both reproductive tissues and sporophytic tissues, in which lipid metabolism plays an essential role. Although GDSL esterases/lipases have been well known as key enzymes for many plant developmental processes and stress responses, their functions in reproductive development remain unclear. Here, we report the identification of a rice male sterile2 (rms2) mutant in rice (Oryza sativa), which is completely male sterile due to the defects in tapetum degradation, cuticle formation in sporophytic tissues, and impaired exine and central vacuole development in pollen grains. RMS2 was map-based cloned as an endoplasmic reticulum-localized GDSL lipase gene, which is predominantly transcribed during early anther development. In rms2, a three-nucleotide deletion and one base substitution (TTGT to A) occurred within the GDSL domain, which reduced the lipid hydrolase activity of the resulting protein and led to significant changes in the content of 16 lipid components and numerous other metabolites, as revealed by a comparative metabolic analysis. Furthermore, RMS2 is directly targeted by the male fertility regulators Undeveloped Tapetum1 and Persistent Tapetal Cell1 both in vitro and in vivo, suggesting that RMS2 may serve as a key node in the rice male fertility regulatory network. These findings shed light on the function of GDSLs in reproductive development and provide a promising gene resource for hybrid rice breeding.

Highlights

Male fertility is essential for the sexual plant life cycle generational alternation as well as for crop production in agriculture
Our work suggests that Rice Male Sterile2 gene (RMS2) may serve as a key node in the rice male fertility regulatory network
This study described the map-based cloning of a GDSL motif-encoding gene, RMS2, in which a substitution of the 230th and 231st amino acid residues from LV to H within the GDSL domain led to abnormal anthers and complete male sterility

Summary

RESULTS

From a g-irradiation-induced mutant population (Long et al, 2016), we identified a male-sterile mutant denoted rms in the background of cv 9311 (indica rice). During the reproductive development stages, the mutant exhibited typical male-sterile phenotypes such as slightly delayed heading date, partly sheathed panicle, and conspicuous white and shrunken anthers (Fig. 1, B and C). Iodine potassium iodide (I2-KI) staining assay detected no viable pollen grains, which resulted in completely sterile plants (Fig. 1, D and E). We tested the female fertility of rms by reciprocal cross rms cv 9311 using rms as the maternal parent. The maternal parent plants and F1 plants produced seeds normally, suggesting viable female organ development in rms. The F2 population had an approximate 3:1 segregation ratio (sterility:fertility 5 106:336, x2 5 0.2443 , x20.05 5 3.84, x2 test used), which suggested that

A GDSL Lipase Functions in Rice Male Fertility

DISCUSSION

Findings

MATERIALS AND METHODS