Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development

Zhang, Lei; Luo, Huai‐Rong; Zhao, Yue; Chen, Xiaoyang; Huang, Yuxin; Yan, Shuangshuang; Li, Suxing; Liu, Meishan; Huang, Wei; Zhang, Xiaolan; Jin, Weiwei

doi:10.1186/s12870-018-1543-7

Cited by 14 publications

(19 citation statements)

References 73 publications

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“…In the present study, SEM was performed to observe the anther surface of ghgpat12/25, thus discovering the seemingly lacking cuticle on anther surface (Figures 5E,F). This defect is consistent with the observations in osgpat3 (Men et al, 2017) and zmms33 (Zhang et al, 2018;Zhu et al, 2019) mutants. Moreover, this defect may be explained by the biochemical evidence establishing that the synthesis of wax monomers, such as alkanes and fatty acids, as well as several other metabolites (tocopherols, campesterols, and diterpenoids), was largely reduced in ghgpat12/25 anthers (Figure 9).…”

Section: Ghgpat12/25 Are Required For the Anther Cuticle Formation And Pollen Exine Assemblysupporting

confidence: 92%

GhGPAT12/25 Are Essential for the Formation of Anther Cuticle and Pollen Exine in Cotton (Gossypium hirsutum L.)

et al. 2021

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Glycerol-3-phosphate acyltransferases (GPATs), critical for multiple biological processes like male fertility, have been extensively characterized. However, their precise functions and underlying regulatory mechanism in cotton anther development are unclear. This research demonstrated the importance of GhGPAT12/25 (a paralogs pair on A12/D12 sub-chromosome of cotton) to regulate the degradation of tapetum, anther cuticle formation, and pollen exine development. GhGPAT12 and GhGPAT25 exhibited specifically detected transcripts in tapetum and pollen exine during the early anther developmental stages. GhGPAT12/25 are sn-2 glycerol-3-phosphate acyltransferases and can transfer the acyl group of palmitoyl-CoA to glycerol-3-phosphate (G3P). CRISPR/Cas9-mediated knockout identified the functional redundancy of GhGPAT12 and GhGPAT25. Knockout of both genes caused completely male sterility associated with abnormal anther cuticle, swollen tapetum, and inviable microspores with defective exine and irregular unrestricted shape. RNA-seq analysis showed that the loss of function of GhGPAT12/25 affects the processes of wax metabolic, glycerol monomer biosynthesis, and transport. Consistently, cuticular waxes were dramatically reduced in mutant anthers. Yeast one-hybrid system (Y1H), virus-induced gene silencing (VIGS), and dual-luciferase (LUC) assays illustrated that GhMYB80s are likely to directly activate the expression of GhGPAT12/25. This study provides important insights for revealing the regulatory mechanism underlying anther development in cotton.

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Section: Ghgpat12/25 Are Required For the Anther Cuticle Formation And Pollen Exine Assemblysupporting

confidence: 92%

GhGPAT12/25 Are Essential for the Formation of Anther Cuticle and Pollen Exine in Cotton (Gossypium hirsutum L.)

et al. 2021

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“…Sequence analysis of ms305 genomic DNA revealed a 6-bp deletion in Ms33 (unpublished data). However, the abortion characteristics of Ms33, which showed no difference in anatomical structure or meiotic events in the fertile and sterile plants before the tetrad stage, as well as the severe degradation of the tapetum in sterile plants at the early uninucleate stage [39], were completely opposite to those of ms305, which delay the degradation of tapetum at this stage. Further cloning of ms305 is necessary to confirm whether ms305 is a novel male sterile mutant or an allele of Ms33 in maize.…”

Section: Discussionmentioning

confidence: 81%

“…Among the DEGs that were identified in 'cutin, suberine, and wax biosynthesis' and 'lipid metabolism' pathway, a KAS II (GRMZM2G124335) gene was found to be located in this region ( Figure 4C, Table S3); interestingly, this gene was the hub gene of highest degree value in the PPI network analysis; thus, further map-based cloning of KAS II will be helpful. Notably, the male sterile gene Ms33 was located in this region, which encodes a glycerol-3-phosphate acyltransferase protein that mediates anther cuticle formation and microspore development [17,39]. Sequence analysis of ms305 genomic DNA revealed a 6-bp deletion in Ms33 (unpublished data).…”

Section: Discussionmentioning

confidence: 99%

“…For example, anther cuticle, including cutin and wax, can protect plant anthers from hydration [26]. In maize, MS45, MS26, MS30, MS33, IPE1, and APV1 are reported to participate in the aliphatic metabolic pathways, which are required for anther cuticle development [19,26,29,39,43]. The abortion characteristics of MS30, MS33, IPE1, and APV1 in maize were described, such as the swollen microspore and the decreased vacuole of APV1 at the vacuolated stage [19], severe degradation of the tapetum in IPE1 [20] and an obvious abortion of MS30 first appeared after the vacuolated stage [15], these were, however, different from ms305.…”

Section: Discussionmentioning

confidence: 99%

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Male sterile 305 Mutation Leads the Misregulation of Anther Cuticle Formation by Disrupting Lipid Metabolism in Maize

Haichun

et al. 2020

IJMS

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The anther cuticle, which is mainly composed of lipid polymers, functions as physical barriers to protect genetic material intact; however, the mechanism of lipid biosynthesis in maize (Zea mays. L.) anther remains unclear. Herein, we report a male sterile mutant, male sterile 305 (ms305), in maize. It was shown that the mutant displayed a defective anther tapetum development and premature microspore degradation. Three pathways that are associated with the development of male sterile, including phenylpropanoid biosynthesis, biosynthesis of secondary metabolites, as well as cutin, suberine, and wax biosynthesis, were identified by transcriptome analysis. Gas chromatography-mass spectrometry disclosed that the content of cutin in ms305 anther was significantly lower than that of fertile siblings during the abortion stage, so did the total fatty acids, which indicated that ms305 mutation might lead to blocked synthesis of cutin and fatty acids in anther. Lipidome analysis uncovered that the content of phosphatidylcholine, phosphatidylserine, diacylglycerol, monogalactosyldiacylglycerol, and digalactosyldiacylglycerol in ms305 anther was significantly lower when compared with its fertile siblings, which suggested that ms305 mutation disrupted lipid synthesis. In conclusion, our findings indicated that ms305 might affect anther cuticle and microspore development by regulating the temporal progression of the lipidome in maize.

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“…If different ms mutants come from the mutation of the same GMS gene, the GMS gene function in male-sterility will be confirmed. For instance, the function of maize ZmMs33 has been confirmed by allelism test and sequencing of several ms33 allelic mutants, such as ms33-6019, ms33-6029, ms33-6024, ms33-6038, and ms33-6052 [20,97]. Most of the cloned GMS genes have allelic mutants and are confirmed by allelic mutant sequencing ( Table 1), so it is a usefully functional confirmation strategy besides the genetic complementation and targeted mutagenesis.…”

Section: Allelism Test and Allelic Mutant Sequencingmentioning

confidence: 99%

Molecular Cloning of Genic Male-Sterility Genes and Their Applications for Plant Heterosis via Biotechnology-based Male-sterility Systems

Wan¹,

Shu²

2020

Synthetic Biology - New Interdisciplinary Science

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In this chapter, we summarize the strategies about molecular cloning and functional confirmation of plant genic male-sterility (GMS) genes and their applications for hybrid breeding and seed production via biotechnology-based male-sterility (BMS) systems in crop plants. The main content includes four sections: (1) GMS gene cloning strategies, including forward genetic approaches (e.g., map-based cloning, T-DNA or transposon tagging, and MutMap method) and reverse genetic approaches (e.g., homology-based cloning, anther-specific expression gene screening, and other reverse genetic methods); (2) functional confirmation methods of GMS genes, including transgenic complementation, targeted mutagenesis, allelic mutant test and sequencing, anther spatiotemporal expression analysis, and cytological observation;(3) application value assessment of GMS genes and mutants, such as genetic stability analysis of male sterility controlled by GMS genes under different genetic backgrounds and multiple environments, and genetic effects driven by GMS genes on plant heterosis and analysis of potential linkage with bad traits; (4) development and application of BMS systems based on GMS genes and/or their mutants, including transgenic construct-driven non-transgenic seed systems (e.g., seed production technology (SPT) and multi-control sterility (MCS)), and transgenic male-sterility systems (e.g., roundup hybridization systems (RHS1 and RHS2) and Barnase/Barstar system). Finally, we summarize and provide our perspectives on the studies of GMS genes and development of cost-effective and environment-friendly BMS systems in crop plants.

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Maize male sterile 33 encodes a putative glycerol-3-phosphate acyltransferase that mediates anther cuticle formation and microspore development

Cited by 14 publications

References 73 publications

GhGPAT12/25 Are Essential for the Formation of Anther Cuticle and Pollen Exine in Cotton (Gossypium hirsutum L.)

GhGPAT12/25 Are Essential for the Formation of Anther Cuticle and Pollen Exine in Cotton (Gossypium hirsutum L.)

Male sterile 305 Mutation Leads the Misregulation of Anther Cuticle Formation by Disrupting Lipid Metabolism in Maize

Molecular Cloning of Genic Male-Sterility Genes and Their Applications for Plant Heterosis via Biotechnology-based Male-sterility Systems

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