OsGPAT3 Plays a Critical Role in Anther Wall Programmed Cell Death and Pollen Development in Rice

Sun, Lianping; Xiang, Xiaojiao; Yang, Zhengfu; Yü, Ping; Wen, Xiaoxia; Wang, Hong; Abbas, Adil; Khan, Riaz Muhammad; Zhang, Yingxin; Cheng, Shifeng

doi:10.3390/ijms19124017

Cited by 26 publications

(30 citation statements)

References 78 publications

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“…RMS2, in which a substitution of the 230th-231st amino acid residues from LH to V within the GDSL domain led to abnormal anthers and complete male sterility. Solid genetic evidence including genetic complementation and CRISPR/Cas9-derived allelic mutants supported this conclusion ( Jung et al, 2005;Shi et al, 2011;Niu et al, 2013;Xu et al, 2017;Sun et al, 2018).…”

Section: Rms2 Is Required For Anther Development By Affecting Tapetummentioning

confidence: 99%

RMS2 Encoding a GDSL Lipase Mediates Lipid Homeostasis in Anthers to Determine Rice Male Fertility

Zhao

Long²,

Wang

et al. 2020

Plant Physiol.

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Plant male gametogenesis is a coordinated effort involving both reproductive tissues and sporophytic tissues, in which lipid metabolism plays an essential role. Although GDSL esterases/lipases have been well known as key enzymes for many plant developmental processes and stress responses, their functions in reproductive development remain unclear. Here, we report the identification of a rice male sterile 2 (rms2) mutant in rice (Oryza sativa), which is completely male sterile due to the defects in tapetum degradation, cuticle formation in sporophytic tissues, and impaired exine and central vacuole development in pollen grains. RMS2 was map-based cloned as an endoplasmic reticulum-localized GDSL lipase gene, which is predominantly transcribed during early anther development. In rms2, a three-nucleotides deletion and one base substitution (TTGT to A) occurred within the GDSL domain, which reduced the lipid hydrolase activity of the resulting protein and led to significant changes in the content of 16 lipid components and numerous other metabolites as revealed by a comparative metabolic analysis. Furthermore, RMS2 is directly targeted by male fertility regulators Undeveloped Tapetum 1 (UDT1) and Persistent Tapetal Cell 1 (PTC1) both in vitro and in vivo, suggesting that RMS2 may serve as a key node in the rice male fertility regulatory network. These findings shed light on the function of GDSLs in reproductive development and provide a promising gene resource for hybrid rice breeding.

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Section: Rms2 Is Required For Anther Development By Affecting Tapetummentioning

confidence: 99%

RMS2 Encoding a GDSL Lipase Mediates Lipid Homeostasis in Anthers to Determine Rice Male Fertility

Zhao

Long²,

Wang

et al. 2020

Plant Physiol.

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“…Similarly, the tomato gpat6 mutant shows disturbed pollen formation (Petit et al, 2016). Rice OsGPAT3 and maize ZmMs33/ZmGPAT6 are involved in anther cuticle and pollen exine development (Men et al, 2017;Sun et al, 2018;Xie et al, 2018;Zhu et al, 2019) and are different from AtGPAT3 and AtGPAT6 in Arabidopsis (Li et al, 2012;Yang et al, 2012). In addition, the downstream products of the glycerolipid synthetic pathway, including glycolipids and phospholipids, are necessary structural components of cellular membranes (Boudiè re et al, 2014;Waschburger et al, 2018).…”

Section: Ros Including Superoxide (O 2 -mentioning

confidence: 99%

Normal Structure and Function of Endothecium Chloroplasts Maintained by ZmMs33-Mediated Lipid Biosynthesis in Tapetal Cells Are Critical for Anther Development in Maize

Zhu

et al. 2020

Molecular Plant

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Genic male sterility (GMS) is critical for heterosis utilization and hybrid seed production. Although GMS mutants and genes have been studied extensively in plants, it has remained unclear whether chloroplast-associated photosynthetic and metabolic activities are involved in the regulation of anther development. In this study, we characterized the function of ZmMs33/ZmGPAT6, which encodes a member of the glycerol-3-phosphate acyltransferase (GPAT) family that catalyzes the first step of the glycerolipid synthetic pathway. We found that normal structure and function of endothecium (En) chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in tapetal cells are crucial for maize anther development. ZmMs33 is expressed mainly in the tapetum at early anther developmental stages and critical for cell proliferation and expansion at late stages. Chloroplasts in En cells of wild-type anthers function as starch storage sites before stage 10 but as photosynthetic factories since stage 10 to enable starch metabolism and carbohydrate supply. Loss of ZmMs33 function inhibits the biosynthesis of glycolipids and phospholipids, which are major components of En chloroplast membranes, and disrupts the development and function of En chloroplasts, resulting in the formation of abnormal En chloroplasts containing numerous starch granules. Further analyses reveal that starch synthesis during the day and starch degradation at night are greatly suppressed in the mutant anthers, leading to carbon starvation and low energy status, as evidenced by low trehalose-6-phosphate content and a reduced ATP/AMP ratio. The energy sensor and inducer of autophagy, SnRK1, was activated to induce early and excessive autophagy, premature PCD, and metabolic reprogramming in tapetal cells, finally arresting the elongation and development of mutant anthers. Taken together, our results not only show that ZmMs33 is required for normal structure and function of En chloroplasts but also reveal that starch metabolism and photosynthetic activities of En chloroplasts at different developmental stages are essential for normal anther development. These findings provide novel insights for understanding how lipid biosynthesis in the tapetum, the structure and function of En chloroplasts, and energy and substance metabolism are coordinated to maintain maize anther development.

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“…Loss of AP1G function compromised dynamic vacuolar remodelling during pollen development and impaired vacuolar acidification of pollen, which resulted in male gametophytic lethality due to defective pollen development [22]. A conserved glycerol-3-phosphate acyltransferase gene OsGPAT3 plays an important role in regulating anther wall degradation and pollen exocrine formation in rice [23]. Gene…”

Section: Discussionmentioning

confidence: 99%

ARABIDOPSIS POLLEN ABORTION MUTANT 2, Encoding an Unknown Protein with Three WD40-Repeats, Is Essential for Late Pollen Mature in Arabidopsis thaliana

Zhang

Chen

et al. 2019

Preprint

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Background In flowering plants, pollen formation is a very complex process. It is strictly regulated by various genetic factors. Some of these factors have been identified, but the regulatory mechanism concerning the process of late pollen maturing remains unknown. Results Previously we identified and reported an ARABIDOPSIS POLLEN ABORTION MUTANT 2 (APAM2) gene which was required for pollen formation in Arabidopsis thaliana. In this study, we further analysed the phenotype of atapam2 and the subcellular localisation of AtAPAM2. Mutation in AtAPAM2 drastically affected male gametophytic function, impacted the late pollen mature process, and resulted in mature pollen grains from atapam2/+ plants being shrivelled and dead. It was expressed among seedlings, roots, stems, leaves, siliques, flowers, and pollen grains. However, its expression levels in flowers and pollen grains were much higher than in other tissues. Gene AtAPAM2 encodes an unknown protein with three WD40-repeats with localisation in plasma membrane and nucleus, and homologous proteins exist in many species. Conclusions We determined that AtAPAM2 may play a role in pollen formation and other development processes by interacting with other proteins, but we did not identify the protein that interacts with it.

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OsGPAT3 Plays a Critical Role in Anther Wall Programmed Cell Death and Pollen Development in Rice

Cited by 26 publications

References 78 publications

RMS2 Encoding a GDSL Lipase Mediates Lipid Homeostasis in Anthers to Determine Rice Male Fertility

RMS2 Encoding a GDSL Lipase Mediates Lipid Homeostasis in Anthers to Determine Rice Male Fertility

Normal Structure and Function of Endothecium Chloroplasts Maintained by ZmMs33-Mediated Lipid Biosynthesis in Tapetal Cells Are Critical for Anther Development in Maize

ARABIDOPSIS POLLEN ABORTION MUTANT 2, Encoding an Unknown Protein with Three WD40-Repeats, Is Essential for Late Pollen Mature in Arabidopsis thaliana

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