The ATP‐binding Cassette Transporter OsABCG15 is Required for Anther Development and Pollen Fertility in Rice

Abstract

Plant male reproductive development is a complex biological process, but the underlying mechanism is not well understood. Here, we characterized a rice (Oryza sativa L.) male sterile mutant. Based on map‐based cloning and sequence analysis, we identified a 1,459‐bp deletion in an adenosine triphosphate (ATP)‐binding cassette (ABC) transporter gene, OsABCG15, causing abnormal anthers and male sterility. Therefore, we named this mutant osabcg15. Expression analysis showed that OsABCG15 is expressed specifically in developmental anthers from stage 8 (meiosis II stage) to stage 10 (late microspore stage). Two genes CYP704B2 and WDA1, involved in the biosynthesis of very‐long‐chain fatty acids for the establishment of the anther cuticle and pollen exine, were downregulated in osabcg15 mutant, suggesting that OsABCG15 may play a key function in the processes related to sporopollenin biosynthesis or sporopollenin transfer from tapetal cells to anther locules. Consistently, histological analysis showed that osabcg15 mutants developed obvious abnormality in postmeiotic tapetum degeneration, leading to rapid degredation of young microspores. The results suggest that OsABCG15 plays a critical role in exine formation and pollen development, similar to the homologous gene of AtABCG26 in Arabidopsis. This work is helpful to understand the regulatory network in rice anther development.

Two ATP Binding Cassette G (ABCG) Transporters, OsABCG26 and OsABCG15, Collaboratively Regulate Rice Male Reproduction

“…Our chemical and cytological data support that OsABCG26 is vital for the export of cuticle precursors from the tapetum to the anther surface, and the previously identified OsABCG15 (Niu et al, 2013a;Qin et al, 2013;Zhu et al, 2013;Wu et al, 2014) contributes to the development of both anther cuticle and pollen exine. Furthermore, OsABCG15 is epistatic to OsABCG26 in regulating the development of these anther lipidic structures.…”

“…The bHLH transcription factor Tapetum Degeneration Retardation (TDR) and its ortholog in Arabidopsis (Arabidopsis thaliana) ABORTED MICROSPORES (AMS) both play a critical role in directly promoting the expression of genes associated with sporopollenin biosynthesis and the secretion of materials for pollen wall patterning (Zhang et al, 2008;Xu et al, 2010Xu et al, , 2014Yang et al, 2014;Zhang and Li, 2014). Mutation or knockdown of all of these genes caused male sterility and defective anther cuticle and pollen exine (Li et al, 2010;Shi et al, 2011;Niu et al, 2013aNiu et al, , 2013bQin et al, 2013;Zhu et al, 2013;Wu et al, 2014;Yang et al, 2014). Up to now, the mechanism underlying the lipid metabolism, particularly lipid transport from tapetum, remains obscure.…”

“…In barley (Hordeum vulgare), HvABCG31, a full ABCG transporter, is involved in leaf cutin formation, and its rice ortholog OsABCG31 shows the similar function (Chen et al, 2011a). In rice, OsABCG5 is required for suberin formation (Shiono et al, 2014), and OsABCG15 is essential for the development of both anther cuticle and pollen exine (Niu et al, 2013a;Qin et al, 2013;Zhu et al, 2013;Wu et al, 2014). However, how these ABCG proteins cooperate and how they contribute to male reproductive development are not clear.…”

“…Up to date, some tapetum-expressed proteins, such as cytochrome P450s (CYP450s; Li et al, 2010;Yang et al, 2014), fatty acyl carrier protein (ACP) reductase (Shi et al, 2011), ABCG transporters (Niu et al, 2013a;Qin et al, 2013;Zhu et al, 2013;Wu et al, 2014), LTPs , and basic helix-loophelix (bHLH) transcription factors (Li et al, 2006;Zhang et al, 2008;Niu et al, 2013b), have been identified to be involved in anther cuticle and pollen exine development in rice. CYP704B2 functions as a v-hydroxylase in producing v-hydroxylated fatty acids with 16 and 18 carbon chains as the common precursors of two biopolymers: sporopollenin and cutin (Li et al, 2010).…”

“…The fatty ACP reductase, Defective Pollen Wall (DPW), is localized in tapetal plastids and produces 1-hexadecanol from palmiltoyl-ACP substrate for anther cuticle and pollen exine development (Shi et al, 2011). The tapetum-expressed ABCG protein, OsABCG15, is considered to be required for the transport of lipidic precursors from tapetal cells to anther cuticle and pollen wall (Niu et al, 2013a;Qin et al, 2013;Zhu et al, 2013;Wu et al, 2014). OsC6 (for locus [LOC]_Os11g37280) belongs to the small LTP protein family, and it is expressed in tapetal cells and involved in the mediation of lipidic distribution from the tapetal cytoplasm to the extracellular space among different anther cell wall layers and to the anther locules and anther cuticle .…”