The ABORTED MICROSPORES Regulatory Network Is Required for Postmeiotic Male Reproductive Development in Arabidopsis thaliana    

Abstract

The Arabidopsis thaliana ABORTED MICROSPORES (AMS) gene encodes a basic helix-loop-helix (bHLH) transcription factor that is required for tapetal cell development and postmeiotic microspore formation. However, the regulatory role of AMS in anther and pollen development has not been fully defined. Here, we show by microarray analysis that the expression of 549 anther-expressed genes was altered in ams buds and that these genes are associated with tapetal function and pollen wall formation. We demonstrate that AMS has the ability to bind in vitro to DNA containing a 6-bp consensus motif, CANNTG. Moreover, 13 genes involved in transportation of lipids, oligopeptides, and ions, fatty acid synthesis and metabolism, flavonol accumulation, substrate oxidation, methyl-modification, and pectin dynamics were identified as direct targets of AMS by chromatin immunoprecipitation. The functional importance of the AMS regulatory pathway was further demonstrated by analysis of an insertional mutant of one of these downstream AMS targets, an ABC transporter, WhiteBrown Complex homolog, which fails to undergo pollen development and is male sterile. Yeast two-hybrid screens and pulldown assays revealed that AMS has the ability to interact with two bHLH proteins (AtbHLH089 and AtbHLH091) and the ATA20 protein. These results provide insight into the regulatory role of the AMS network during anther development.

PERSISTENT TAPETAL CELL1Encodes a PHD-Finger Protein That Is Required for Tapetal Cell Death and Pollen Development in Rice

“…3). This phenotype is distinct from other tapetal mutants that have been described, such as Arabidopsis ams (Xu et al, 2010) and rice tdr (Li et al, 2006) mutants, which exhibit tapetal defects involving swelling of the tapetum as a consequence of vacuole increase rather than cytoplasmic proliferation. Subsequent to this proliferation, very rapid degeneration of the tapetum and microspores occurs in ptc1 via necrosis-like breakdown.…”

“…Tapetal cell development and differentiation are critical for the early events in male reproduction, including meiosis; however, during late pollen development, tapetal degeneration, triggered by an apoptosis-like process, is also vital for viable pollen formation (Papini et al, 1999;Varnier et al, 2005;Li et al, 2006;Aya et al, 2009). Currently, although several genes encoding putative transcription factors have been reported to be associated with tapetal function and degeneration, such as Arabidopsis (Arabidopsis thaliana) MYB33/MYB65 (Millar and Gubler, 2005), DYSFUNCTIONAL TAPETUM1 (DYT1; Zhang et al, 2006), ABORTED MICROSPORE (AMS; Sorensen et al, 2003;Xu et al, 2010), and MALE STERILITY1 (MS1; Wilson et al, 2001;Ito and Shinozaki, 2002) and rice (Oryza sativa) GAMYB (Kaneko et al, 2004;Aya et al, 2009;Liu et al, 2010), UNDEVELOPED TAPETUM1 (UDT1; Jung et al, 2005), TAPETUM DE-GENERATION RETARDATION (TDR; Li et al, 2006), and MADS3 (Hu et al, 2011), their detailed functional roles in regulating tapetal PCD during anther development are unclear. We have shown that the Arabidopsis ms1 mutant displays altered tapetal development, with a lack of normal PCD and abnormal tapetal degeneration associated with large autophagic vacuoles and mitochondrial swelling (Vizcay-Barrena and Wilson, 2006).…”

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

“…Given that AMS, the Arabidopsis ortholog of TDR, directly regulates the expression of AtABCG26, the Arabidopsis ortholog of OsABCG15 ( Xu et al, 2010), we propose that TDR may act as the direct regulator of OsABCG15, which remains to be elucidated.…”

“…Some plant ABCG proteins have been reported to contribute to the synthesis of extracellular barriers. In Arabidopsis, ABCG11 (Cuticular Defect and Organ Fusion1/DESPERADO/White-Brown Complex11; Bird et al, 2007;Panikashvili et al, 2007Panikashvili et al, , 2010, ABCG12 (Eceriferum5/WBC12; Pighin et al, 2004), ABCG13 (Panikashvili et al, 2010), ABCG29 (Alejandro et al, 2012), ABCG32 (Bessire et al, 2011), and ABCG26 (WBC27; Xu et al, 2010;Quilichini et al, 2010Quilichini et al, , 2014Choi et al, 2011;Dou et al, 2011) have been shown to be involved in transport of lipidic compounds. Notably, it has been reported that these ABCG proteins have a broad substrates spectrum (for example, ABCG11 transports both cutin and wax monomers, and ABCG13 and ABCG32 mainly transport cutin monomers, whereas ABCG12 mainly transports wax precursors, and ABCG29 mainly transports monolignol).…”

“…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 . 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).…”