Defective Pollen Wall 2 (DPW2) Encodes an Acyl Transferase Required for Rice Pollen Development

Abstract

Aliphatic and aromatic lipids are both essential structural components of the plant cuticle, an important interface between the plant and environment. Although cross links between aromatic and aliphatic or other moieties are known to be associated with the formation of leaf cutin and root and seed suberin, the contribution of aromatic lipids to the biosynthesis of anther cuticles and pollen walls remains elusive. In this study, we characterized the rice (Oryza sativa) male sterile mutant, defective pollen wall 2 (dpw2), which showed an abnormal anther cuticle, a defective pollen wall, and complete male sterility. Compared with the wild type, dpw2 anthers have increased amounts of cutin and waxes and decreased levels of lipidic and phenolic compounds. DPW2 encodes a cytoplasmically localized BAHD acyltransferase. In vitro assays demonstrated that recombinant DPW2 specifically transfers hydroxycinnamic acid moieties, using v-hydroxy fatty acids as acyl acceptors and hydroxycinnamoyl-CoAs as acyl donors. Thus, The cytoplasmic hydroxycinnamoyl-CoA:v-hydroxy fatty acid transferase DPW2 plays a fundamental role in male reproduction via the biosynthesis of key components of the anther cuticle and pollen wall.In flowering plants, male reproductive development is a complex biological event that is essential to the survival and reproduction of the species. One distinctive feature of plant male development is the formation of the stamen, which consists of the anther and the supporting filament. The anther is composed of somatic anther wall layers and microspore mother cells (MMCs), which produces pollen grains via meiosis followed by two rounds of mitosis. After anther morphogenesis is complete, four centric layers are formed in the anther wall: the epidermis, endothecium, middle layer, and tapetum (

ABNORMAL POLLEN VACUOLATION1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize

“…MS26 encodes a cytochrome P450 monooxygenase and was found to function in the fatty acid metabolism pathway. Similarly, many tapetum‐expressed genes which are involved in fatty acid metabolism and lipid transporters are well known in rice, including WAX‐DEFICIENT ANTHER1 ( WDA1 ) (Jung et al ., ), DEFECTIVE POLLEN WALL ( DPW ) (Shi et al ., ), DPW2 (Xu et al ., ), CYP704B2 (Li et al ., ), POST‐MEIOTIC DEFICIENT ANTHER1 ( PDA1 ) (Hu et al ., ), CYP703A3 (Yang et al ., ), TAPETUM DEGENERATION RETARDATION ( TDR ) (Li et al ., ), DEFECTIVE TAPETUM CELL DEATH 1 ( DTC1 ) (Yi et al ., ), OsDEX1 (Yu et al ., ), OsC6 (Zhang et al ., ), OsABCG15 (Wu et al ., ), OsABCG26 (Zhao et al ., ), and MALE STERILITY2 ( MS2 ) (Chen et al ., ; Doan et al ., ), CYP704B1 (Dobritsa et al ., ), CYP703A2 (Morant et al ., ), Acyl‐CoA Synthetase ( ACOS5 ) (de Azevedo Souza et al ., ), and AtSEC31B (Zhao et al ., ) in Arabidopsis. The rice cyp703a3 mutant displays complete male sterility, whereas its Arabidopsis orthologous cyp703a2 mutant produces partially sterile pollen grains that display an abnormal exine with no obvious sporopollenin deposition.…”

Secretory COPII Protein SEC31B Is Required for Pollen Wall Development

“…FORMATION1 (NEF1), the recently reported SPONGY2 (SPG2), and UNEVEN PATTERN OF EXINE1 (UPEX1), which are all highly expressed in the tapetum and sporophyte-controlled tissues (Paxson-Sowders et al, 2001;Ariizumi et al, 2004Ariizumi et al, , 2008Guan et al, 2008;Chang et al, 2012;Li et al, 2016;Xu et al, 2016). After the microspores are released, tapetal cells constantly synthesize precursors of sporopollenin and release them into the locule to deposit on the surface of the pollen exine.…”

“…MS2, ACOS5, CYP703A2, and CYP704B2 are reportedly involved in the synthesis of sporopollenin precursors in Arabidopsis (Arabidopsis thaliana; Morant et al, 2007;de Azevedo Souza et al, 2009;Dobritsa et al, 2009;Chen et al, 2011). Additionally, DEFECTIVE POLLEN WALL2, encoding an acyltransferase, is required for rice (Oryza sativa) pollen development (Xu et al, 2016). Then, these precursors and other structural materials are transported outside tapetal cells via lipid transfer proteins or ATP-BINDING CASSETTE TRANSPORTER (ABCG) proteins (McFarlane et al, 2010;Quilichini et al, 2010;Choi et al, 2011Choi et al, , 2014Huang et al, 2013).…”

RiceAntherNet: a gene co‐expression network for identifying anther and pollen development genes

“…During the pollen wall formation stages, sporopollenin is synthesized in tapetal cells with associated high levels of gene expression observed. Lipid synthesis genes CYP704B2 , CYP703A3 (Yang et al ., ) and DPW ( DEFECTIVE POLLEN WALL ; Xu et al ., ) in rice, and the corresponding orthologs in Arabidopsis [ CYP704B1 (Dobritsa et al ., ,b), CYP703A2 (Morant et al ., ) and MS2 ( MALE STERILE2 ; Chen et al ., )] are required for the pollen wall formation. In addition, a biochemical pathway involving ACOS12 , PKS1 , TKPR1 ( TETRAKETIDE ALPHA‐PYRONE REDUCTASE 1 ) and TKPR2 ( TETRAKETIDE ALPHA‐PYRONE REDUCTASE 2 ) is conserved in rice, Arabidopsis, tobacco, Hypericum perforatum and canola (Qin et al ., ; Jepson et al ., ; Li et al ., ; Yang et al ., ).…”