IRREGULAR POLLEN EXINE1 Is a Novel Factor in Anther Cuticle and Pollen Exine Formation

Abstract

ORCID IDs: 0000-0002-4656-3189 (H.S.); 0000-0003-0518-5924 (C.Z.); 0000-0001-9320-9628 (W.J.).Anther cuticle and pollen exine are protective barriers for pollen development and fertilization. Despite that several regulators have been identified for anther cuticle and pollen exine development in rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana), few genes have been characterized in maize (Zea mays) and the underlying regulatory mechanism remains elusive. Here, we report a novel male-sterile mutant in maize, irregular pollen exine1 (ipe1), which exhibited a glossy outer anther surface, abnormal Ubisch bodies, and defective pollen exine. Using map-based cloning, the IPE1 gene was isolated as a putative glucose-methanolcholine oxidoreductase targeted to the endoplasmic reticulum. Transcripts of IPE1 were preferentially accumulated in the tapetum during the tetrad and early uninucleate microspore stage. A biochemical assay indicated that ipe1 anthers had altered constituents of wax and a significant reduction of cutin monomers and fatty acids. RNA sequencing data revealed that genes implicated in wax and flavonoid metabolism, fatty acid synthesis, and elongation were differentially expressed in ipe1 mutant anthers. In addition, the analysis of transfer DNA insertional lines of the orthologous gene in Arabidopsis suggested that IPE1 and their orthologs have a partially conserved function in male organ development. Our results showed that IPE1 participates in the putative oxidative pathway of C16/C18 v-hydroxy fatty acids and controls anther cuticle and pollen exine development together with MALE STERILITY26 and MALE STERILITY45 in maize.Male sterility is a common biological phenomenon in plants and widely used in the production of hybrid seeds, which can reduce costs and enhance seed purity (Tester and Langridge, 2010). According to inheritance or origin, male sterility includes three types: genic male sterility, cytoplasmic male sterility, and cytoplasmicgenic male sterility (Rhee et al., 2015). The generation of mature pollen grains relies on anther development. The start of anther formation occurs in differentiated flower tissues (floral meristem), which consist of three histogenic layers: L1, L2, and L3. After continuous cell division and differentiation, L1 forms the epidermis and the L3 layer develops into the stomium and vascular bundles. L2 is the most important layer; it undergoes a series of periclinal and anticlinal divisions and eventually grows into the endothecium, the middle layer, the tapetum, and the pollen mother cells. When anther morphogenesis is completed, the anther has centrally localized pollen mother cells enclosed by four somatic layers, which are, from the surface to the interior, the epidermis, endothecium, middle layer, and tapetum. Then, the pollen mother cells undergo meiosis and mitosis, resulting in trinucleate pollen grains, and the endothecium, middle layer, and tapetum are gradually degraded (Goldberg et al., 1993(Goldberg et al., , 1995Ma, 2005).The anther cuticle and poll...

Rice No Pollen 1 (NP1) is required for anther cuticle formation and pollen exine patterning

“…HOTHEAD ( HTH ) in Arabidopsis (Krolikowski et al ., ; Kurdyukov et al ., ) and ONI3 , the rice ortholog of HTH (Akiba et al ., ), affects cutin metabolism and organ genesis. The orthologous gene of NP1 in maize, IPE1 , is also involved in pollen exine and cuticle formation, suggesting a conserved role of NP1 and its orthologs in plant male reproduction (Chen et al ., ).…”

“…Another Arabidopsis GMC superfamily member, At1 g12570, is the NP1 ortholog, inducible by cutin regulator WIN1/SHN1 and supposed to be involved in cutin biosynthesis (Kannangara et al ., ). A recent report indicates that At1g12570 has a partially conserved role in male reproductive development (Chen et al ., ).…”

“…In addition, different cuticular lipid profiles obtained between hth and np1‐4 might be explained by variant functions of NP1‐like proteins in rice and Arabidopsis, and the different tissues used: anther in rice, inflorescence in Arabidopsis (Kurdyukov et al ., ). Our cuticular lipid profile of rice anther was similar to that observed in maize anther, and the change in cutin profile between wild‐type and np1‐4 in rice was also similar to that between wild‐type and ipe1 mutant in maize (Chen et al ., ), emphasizing different functions of NP1 proteins between monocot and dicot plants. Alternatively, NP1 may be involved in the production of other cross‐linking monomers such as epoxy‐fatty acids, which are among the dominant constituents of rice cutin; but here, technical difficulties prevent the gathering of biochemical evidence.…”

iTRAQ‐Based Proteomics Reveals that the Tomato ms1035 Gene Causes Male Sterility through Compromising Fat Acid Metabolism

“…We can infer that retarded PCD triggers fatty acid metabolic abnormalities, which in turn compromises normal pollen maturity and leads to total male sterility in the 2–517 line. Based on previous cytological studies and biochemical analysis on sporopollenin and cuticle synthesis mutants, [ 62,63 ] we designed a biological synthesis model of the anther cuticle and pollen exine in the pollen maturation process ( Figure ). After being transferred into the endoplasmic reticulum, the middle‐and long‐chain fatty acids which are synthesized in plastids, will be ω‐hydroxylated by CYP704, a member of the CYP gene family.…”

Focus on Flowering and Reproduction

“…These works also implicate the importance of arabinogalactan-protein in the construction of the pollen coat. Two other articles, Xu et al (2017) and Chen et al (2017), focus on crop plants and identified, respectively, an acyl transferase from rice (Oryza sativa) and an oxidoreductase from maize (Zea mays) as playing important roles in anther cuticle and wall formation and pollen viability. The importance of tapetal degeneration to pollen maturation is further underscored in two studies (Cui et al, 2017;Gao et al, 2017); they provide insight on the involvement by Cys and Asp proteases in tapetal cell death during the late stage of pollen development.…”