Ultrastructure analysis reveals sporopollenin deposition and nexine formation at early stage of pollen wall development in Arabidopsis

Zhou, Qing; Zhu, Jun; Cui, Yong-Lan; Yang, Zhong‐Nan

doi:10.1007/s11434-014-0723-6

Cited by 21 publications

(19 citation statements)

References 10 publications

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“…Cytological evidence reveals that sporopollenin precursors are synthesized in the tapetum, secreted into the locule, and are finally deposited on the surface of microspores to form the sexine layer (Heslop‐Harrison, ; Zhou et al ., ). It has been reported that CYP703A2 function as a fatty acid hydroxylation monooxygenase in sporopollenin precursor synthesis.…”

Section: Discussionmentioning

confidence: 97%

The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana

Xiong

Lou

et al. 2016

The Plant Journal

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The sexine layer of pollen grain is mainly composed of sporopollenins. The sporophytic secretory tapetum is required for the biosynthesis of sporopollenin. Although several enzymes involved in sporopollenin biosynthesis have been reported, the regulatory mechanism of these enzymes in tapetal layer remains elusive. ABORTED MICROSPORES (AMS) and MALE STERILE 188/MYB103/MYB80 (MS188/MYB103/MYB80) are two tapetal cell-specific transcription factors required for pollen wall formation. AMS functions upstream of MS188. Here we report that AMS and MS188 target the CYP703A2 gene, which is involved in sporopollenin biosynthesis. We found that AMS and MS188 were localized in tapetum while CYP703A2 was localized in both tapetum and locule. Chromatin immunoprecipitation (ChIP) showed that MS188 directly bound to the promoter of CYP703A2 and luciferase-inducible assay showed that MS188 activated the expression of CYP703A2. Yeast two-hybrid and electrophoretic mobility shift assays (EMSAs) further demonstrated that MS188 complexed with AMS. The expression of CYP703A2 could be partially restored by the elevated levels of MS188 in the ams mutant. Therefore, our data reveal that MS188 coordinates with AMS to activate CYP703A2 in sporopollenin biosynthesis of plant tapetum.

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Section: Discussionmentioning

confidence: 97%

The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana

Xiong

Lou

et al. 2016

The Plant Journal

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“…Primexine is believed to act as a scaffold for the attachment of sporopollenin monomers (Ariizumi and Toriyama, 2011). After primexine formation, undulation of the microspore plasma membrane occurs, which contributes to determining the position of bacula formation (Paxson-Sowders et al, 1997;Zhou et al 2015). An Arabidopsis gene, DEFECTIVE IN EXINE FORMATION1 (DEX1), encodes a membrane-associated protein required for primexine development and plasma membrane undulation, and a mutation of the gene results in random deposition of sporopollenin at the plasma membrane surface (Paxson-Sowders et al, 1997;Paxson-Sowders et al, 2001).…”

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confidence: 99%

“…[ from the cells of the tapetum and the deposition pattern of the exine is determined during the tetrad stage (Zhou et al, 2015). Surrounding the outer exine layer is the pollen coat, containing proteins and lipids that accumulate in the exine cavities (Quilichini et al, 2015).…”

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“…A recent study suggests that arabinogalactan proteins (AGPs) are key constituents of nexine with expression of AtAGP6 in the nexinedeficient mutant transposable element silencing via athook (tek) partially restoring nexine formation (Jia et al, 2015). The materials comprising the exine are derived from the cells of the tapetum and the deposition pattern of the exine is determined during the tetrad stage (Zhou et al, 2015). Surrounding the outer exine layer is the pollen coat, containing proteins and lipids that accumulate in the exine cavities (Quilichini et al, 2015).…”

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KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

et al. 2016

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Pollen exine is essential for protection from the environment of the male gametes of seed-producing plants, but its assembly and composition remain poorly understood. We previously characterized Arabidopsis (Arabidopsis thaliana) mutants with abnormal pollen exine structure and morphology that we named kaonashi (kns). Here we describe the identification of the causal gene of kns4 that was found to be a member of the CAZy glycosyltransferase 31 gene family, identical to UNEVEN PATTERN OF EXINE1, and the biochemical characterization of the encoded protein. The characteristic exine phenotype in the kns4 mutant is related to an abnormality of the primexine matrix laid on the surface of developing microspores. Using light microscopy with a combination of type II arabinogalactan (AG) antibodies and staining with the arabinogalactan-protein (AGP)-specific b-Glc Yariv reagent, we show that the levels of AGPs in the kns4 microspore primexine are considerably diminished, and their location differs from that of wild type, as does the distribution of pectin labeling. Furthermore, kns4 mutants exhibit reduced fertility as indicated by shorter fruit lengths and lower seed set compared to the wild type, confirming that KNS4 is critical for pollen viability and development. KNS4 was heterologously expressed in Nicotiana benthamiana, and was shown to possess b-(1,3)-galactosyltransferase activity responsible for the synthesis of AG glycans that are present on both AGPs and/or the pectic polysaccharide rhamnogalacturonan I. These data demonstrate that defects in AGP/pectic glycans, caused by disruption of KNS4 function, impact pollen development and viability in Arabidopsis.Pollen, the male gametophyte of all seed plants, is crucial for reproductive success. Due to the harsh environmental conditions that pollen must survive in, it has developed an elaborate and specialized cell wall. However, despite its importance our knowledge of the fine structure and assembly of the pollen grain wall is poorly understood (Newbigin et al., 2009;Ariizumi and Toriyama, 2011;Quilichini et al., 2015;Shi et al., 2015). Arabidopsis (Arabidopsis thaliana) provides an ideal genetic and cell biological model to dissect the assembly of the components of the pollen grain wall. Arabidopsis pollen grains have a typical surface structure that consists of an inner intine layer, which is usually made up of cellulose and pectin, and the outer exine, which is largely composed of sporopollenin (Li et al., 1995). The exine is further subdivided into inner nexine and outer sexine. The sexine has a three-dimensional (3D) structure composed of many columns called baculae and a roof called tectum. These two structures give the Arabidopsis pollen surface a reticulate appearance with a uniform mesh size. The nexine is composed of outer nexine I (foot layer), which contains sporopollenin, and inner nexine II (endexine; Ariizumi and Toriyama, 2011;Jiang et al., 2013). A recent study suggests that arabinogalactan proteins (AGPs) are key constituents of nexine with express...

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“…The sporophytic tapetal cells synthesize precursor materials for the outer pollen wall. After secretion into the locule, these materials are directly deposited outside the developing microspore/male gametophyte (Heslop-Harrison, 1962;Scott et al, 2004;Zhou et al, 2015). The tapetal cells also provide various nutrients needed for development of the male gametophyte.…”

Section: Introductionmentioning

confidence: 99%

Magnesium Transporter 5 plays an important role in Mg transport for male gametophyte development in Arabidopsis

Wang

Lou

et al. 2015

The Plant Journal

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SUMMARYDuring anther development the male gametophyte develops inside the locule and the tapetal cells provide all nutrients for its development. Magnesium Transporter 5 (MGT5) is a member of the MGT family and has dual functions of Mg export and import. Here, we show that male gametophyte mitosis and intine formation are defective in a mgt5 mutant. The transient expression of GFP-MGT5 revealed that MGT5 is localized in the plasma membrane. These findings suggest that in the male gametophyte MGT5 plays a role in importing Mg from the locule and that Mg is essential for male gametophyte development. The expression of MGT5 in the knockout ABORTED MICROSPORES (AMS) mutant (AMS being an essential regulator of tapetum) is tremendously reduced. Chromatin immunoprecipitation and mobility shift assay experiments demonstrated that AMS can directly bind the promoter of MGT5. An immunoelectron microscopy assay revealed that MGT5-His is localized to the plasma membrane of the tapetum. These findings suggest that AMS directly regulates MGT5 in the tapetum and thus induces export of Mg into the locule. The mgt5 plant exhibits severe male sterility while the expression of MGT5 under the tapetum-specific promoter A9 partly rescued mgt5 fertility. mgt5 fertility was restored under high-Mg conditions. These findings suggest that the mgt5 tapetum still has the ability to export Mg and that a sufficient supply of Mg from the tapetum can improve the importation of Mg in the mgt5 male gametophyte. Therefore, MGT5 plays an important role in Mg transport from the tapetum to the microspore.

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Ultrastructure analysis reveals sporopollenin deposition and nexine formation at early stage of pollen wall development in Arabidopsis

Cited by 21 publications

References 10 publications

The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana

The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

Magnesium Transporter 5 plays an important role in Mg transport for male gametophyte development in Arabidopsis

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