New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana

Quilichini, Teagen D.; Douglas, Carl J.; Samuels, A. Lacey

doi:10.1093/aob/mcu042

Cited by 124 publications

(136 citation statements)

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“…Sporopollenin is synthesized in tapetal cells, secreted to locules, and transferred to the microspore surface (Owen and Makaroff 1995;Quilichini et al, 2014). Besides the failure of exine formation in kns4, we revealed that the sporopollenin is abnormally deposited on the surface of tapetal cell walls, which is in contact with the developing exine of microspores (Figs.…”

Section: Discussionmentioning

confidence: 88%

“…2, B and H, respectively). Moreover, the protoplast of the wild-type PMCs was often detached from the primary cell wall, although this is likely to be a sample preparation artifact frequently observed during this developmental stage in wild type (Quilichini et al, 2014). Interestingly, this was never observed in mutant PMCs, perhaps indicating some structural differences in connectivity between the plasma membrane-cell wall interface between wild type and mutants.…”

Section: Kns4 Is Required For Separation Of Pmcs and Microspores In Amentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 88%

Section: Kns4 Is Required For Separation Of Pmcs and Microspores In Amentioning

confidence: 99%

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

et al. 2016

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“…Tapetum-specific organelles, including the tapetosomes and elaioplasts, showed no difference in the wild type and mon1, excluding the possible involvement of MON1 in their biogenesis (Supplemental Fig. S5, B and C; Quilichini et al, 2014). These results suggest that MON1 is crucial for the proper timing of tapetal PCD.…”

Section: The Mon1 Mutation Causes Delayed Pcd In Tapetal Cellsmentioning

confidence: 83%

MONENSIN SENSITIVITY1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-Mediated Rab7 Activation Regulates Tapetal Programmed Cell Death and Pollen Development

et al. 2016

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Programmed cell death (PCD)-triggered degradation of plant tapetum is essential for microspore development and pollen coat formation; however, little is known about the cellular mechanism regulating tapetal PCD. Here, we demonstrate that Rab7-mediated vacuolar transport of tapetum degradation-related cysteine proteases is crucial for tapetal PCD and pollen development in Arabidopsis (Arabidopsis thaliana), with the following evidence: (1) The monensin sensitivity1 (mon1) mutants, which are defective in Rab7 activation, showed impaired male fertility due to a combined defect in both tapetum and male gametophyte development. (2) In anthers, MON1 showed preferential high level expression in tapetal cell layers and pollen. (3) The mon1 mutants exhibited delayed tapetum degeneration and tapetal PCD, resulting in abnormal pollen coat formation and decreased male fertility. (4) MON1/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-mediated Rab7 activation was indispensable for vacuolar trafficking of tapetum degradation-related cysteine proteases, supporting that PCD-triggered tapetum degeneration requires Rab7-mediated vacuolar trafficking of these cysteine proteases. (5) MON1 mutations also resulted in defective pollen germination and tube growth. Taken together, tapetal PCD and pollen development require successful MON1/CCZ1-mediated vacuolar transport in Arabidopsis.

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“…Sporopollenin precursors are synthesized in the tapetum, a metabolically active anther secretory tissue that surrounds the anther locule where microspores and pollen grains develop (Ariizumi and Toriyama, 2011;Quilichini et al, 2014aQuilichini et al, , 2015a. The morphological and cellular events involved in pollen and pollen wall development have been most thoroughly studied in Arabidopsis and rice (Oryza sativa; Sanders et al, 1999;Scott et al, 2004;Ariizumi and Toriyama, 2011;Shi et al, 2015).…”

mentioning

confidence: 99%

“…The morphological and cellular events involved in pollen and pollen wall development have been most thoroughly studied in Arabidopsis and rice (Oryza sativa; Sanders et al, 1999;Scott et al, 2004;Ariizumi and Toriyama, 2011;Shi et al, 2015). A recent detailed study of microspore and tapetum development over the course of Arabidopsis anther development has revealed the events in pollen wall formation at high resolution with greatly improved preservation of ultrastructural features (Quilichini et al, 2014a). Briefly, pollen wall formation is initiated after microspore mother cells undergo meiosis to generate haploid tetrads surrounded by callose.…”

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confidence: 99%

Role of Glycosyltransferases in Pollen Wall Primexine Formation and Exine Patterning

Liu

Douglas

2016

Plant Physiol.

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The pollen cell wall is important for protection of male sperm from physical stresses and consists of an inner gametophytederived intine layer and a sporophyte-derived exine layer. The polymeric constituents of the robust exine are termed sporopollenin. The mechanisms by which sporopollenin is anchored onto microspores and polymerized in specific patterns are unknown, but the primexine, a transient cell wall matrix formed on the surface of microspores at the late tetrad stage, is hypothesized to play a key role. Arabidopsis (Arabidopsis thaliana) spongy (spg) and uneven pattern of exine (upex) mutants exhibit defective and irregular exine patterns. SPG2 (synonymous with IRREGULAR XYLEM9-LIKE [IRX9L]) encodes a family GT43 glycosyltransferase involved in xylan backbone biosynthesis, while UPEX1 encodes a family GT31 glycosyltransferase likely involved in galactosylation of arabinogalactan proteins. Imaging of developing irx9l microspores showed that the earliest detectable defect was in primexine formation. Furthermore, wild-type microspores contained primexine-localized epitopes indicative of the presence of xylan, but these were absent in irx9l. These data, together with the spg phenotype of a mutant in IRX14L, which also plays a role in xylan backbone elongation, indicate the presence of xylan in pollen wall primexine, which plays a role in exine patterning on the microspore surface. We observed an aberrant primexine and irregular patterns of incipient sporopollenin deposition in upex1, suggesting that primexine-localized arabinogalactan proteins could play roles in sporopollenin adhesion and patterning early in microspore wall development. Our data provide new insights into the biochemical and functional properties of the primexine component of the microspore cell wall.

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New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana

Abstract: This high-quality structural information, interpreted in the context of recent functional studies, provides the groundwork for future mutant studies where tapetum and microspore ultrastructure is assessed.

Cited by 124 publications

References 51 publications

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

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

MONENSIN SENSITIVITY1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-Mediated Rab7 Activation Regulates Tapetal Programmed Cell Death and Pollen Development

Role of Glycosyltransferases in Pollen Wall Primexine Formation and Exine Patterning

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