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定位于质体的ZmENR1/ZmHAD1复合物通过调节脂质和活性氧代谢确保玉米花粉和花药发育。

Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism.

作者信息

Zhang Shaowei, An Xueli, Jiang Yilin, Hou Quancan, Ma Bin, Jiang Qingping, Zhang Kai, Zhao Lina, Wan Xiangyuan

机构信息

Research Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing, 100083, China.

Zhongzhi International Institute of Agricultural Biosciences, Beijing, 100083, China.

出版信息

Nat Commun. 2024 Dec 30;15(1):10857. doi: 10.1038/s41467-024-55208-8.

DOI:10.1038/s41467-024-55208-8
PMID:39738019
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11686123/
Abstract

Lipid metabolism is critical for male reproduction in plants. Many lipid-metabolic genic male-sterility (GMS) genes function in the anther tapetal endoplasmic reticulum, while little is known about GMS genes involved in de novo fatty acid biosynthesis in the anther tapetal plastid. In this study, we identify a maize male-sterile mutant, enr1, with early tapetal degradation, defective anther cuticle, and pollen exine. Using genetic mapping, we clone a key GMS gene, ZmENR1, which encodes a plastid-localized enoyl-acyl carrier protein (ACP) reductase. ZmENR1 interacts with β-hydroxyacyl-ACP dehydratase (ZmHAD1) to enhance the efficiency of de novo fatty acid biosynthesis. Furthermore, the ZmENR1/ZmHAD1 complex is regulated by a Maize Male Sterility 1 (ZmMS1)-mediated feedback repression loop to ensure anther cuticle and pollen exine formation by affecting the expression of cutin/wax- and sporopollenin-related genes. Intriguingly, homologous genes of ENR1 from rice and Arabidopsis also regulate male fertility, suggesting that the ENR1-mediated pathway likely represents a conserved regulatory mechanism underlying male reproduction in flowering plants.

摘要

脂质代谢对植物雄性生殖至关重要。许多脂质代谢基因雄性不育(GMS)基因在花药绒毡层内质网中发挥作用,而对于参与花药绒毡层质体中从头脂肪酸生物合成的GMS基因却知之甚少。在本研究中,我们鉴定出一个玉米雄性不育突变体enr1,其具有早期绒毡层降解、有缺陷的花药表皮和花粉外壁。通过遗传定位,我们克隆了一个关键的GMS基因ZmENR1,它编码一种定位于质体的烯酰-酰基载体蛋白(ACP)还原酶。ZmENR1与β-羟酰基-ACP脱水酶(ZmHAD1)相互作用,以提高从头脂肪酸生物合成的效率。此外,ZmENR1/ZmHAD1复合物受玉米雄性不育1(ZmMS1)介导的反馈抑制环调控,通过影响角质/蜡质和孢粉素相关基因的表达来确保花药表皮和花粉外壁的形成。有趣的是,水稻和拟南芥中ENR1的同源基因也调控雄性育性,这表明ENR1介导的途径可能代表了开花植物雄性生殖背后一种保守的调控机制。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/4873c0390a70/41467_2024_55208_Fig8_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/5b78ff754256/41467_2024_55208_Fig1_HTML.jpg
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https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/1b84517b2892/41467_2024_55208_Fig5_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/24cf05a5f78f/41467_2024_55208_Fig6_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/e442c9199f63/41467_2024_55208_Fig7_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/4873c0390a70/41467_2024_55208_Fig8_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/5b78ff754256/41467_2024_55208_Fig1_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/d3108f063429/41467_2024_55208_Fig2_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/b318819b81a8/41467_2024_55208_Fig3_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/e883743acdbc/41467_2024_55208_Fig4_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/1b84517b2892/41467_2024_55208_Fig5_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/24cf05a5f78f/41467_2024_55208_Fig6_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/e442c9199f63/41467_2024_55208_Fig7_HTML.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/09c7/11686123/4873c0390a70/41467_2024_55208_Fig8_HTML.jpg

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本文引用的文献

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Fatty acid de novo biosynthesis in plastids: Key enzymes and their critical roles for male reproduction and other processes in plants.质体中脂肪酸从头生物合成:关键酶及其在植物雄性生殖和其他过程中的关键作用。
Plant Physiol Biochem. 2024 May;210:108654. doi: 10.1016/j.plaphy.2024.108654. Epub 2024 Apr 22.
2
CRISPR/Cas9-based genome editing of 14 lipid metabolic genes reveals a sporopollenin metabolon ZmPKSB-ZmTKPR1-1/-2 required for pollen exine formation in maize.基于 CRISPR/Cas9 的 14 个脂质代谢基因的基因组编辑揭示了一个花粉外壁形成所必需的脂多糖代谢物 ZmPKSB-ZmTKPR1-1/-2 在玉米中的作用。
Plant Biotechnol J. 2024 Jan;22(1):216-232. doi: 10.1111/pbi.14181. Epub 2023 Oct 4.
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ZmMS1/ZmLBD30-orchestrated transcriptional regulatory networks precisely control pollen exine development.
ZmMS1/ZmLBD30 调控的转录调控网络精确控制花粉外壁的发育。
Mol Plant. 2023 Aug 7;16(8):1321-1338. doi: 10.1016/j.molp.2023.07.010. Epub 2023 Jul 26.
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Biosynthesis and transport of pollen coat precursors in angiosperms.被子植物花粉外壁前体物的生物合成与转运。
Nat Plants. 2023 Jun;9(6):864-876. doi: 10.1038/s41477-023-01413-0. Epub 2023 May 25.
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UDP-glucose epimerase 1, moonlighting as a transcriptional activator, is essential for tapetum degradation and male fertility in rice.UDP-葡萄糖差向异构酶 1 作为一种转录激活因子,对于水稻绒毡层降解和雄性育性是必需的。
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Ascorbic acid-mediated reactive oxygen species homeostasis modulates the switch from tapetal cell division to cell differentiation in Arabidopsis.抗坏血酸介导的活性氧稳态调节拟南芥绒毡层细胞分裂到细胞分化的转变。
Plant Cell. 2023 Apr 20;35(5):1474-1495. doi: 10.1093/plcell/koad037.
7
Triphasic regulation of ZmMs13 encoding an ABCG transporter is sequentially required for callose dissolution, pollen exine and anther cuticle formation in maize.ZmMs13 编码的 ABCG 转运蛋白的三相调节顺序需要用于玉米中的胼胝质溶解、花粉外壁和花药表皮形成。
J Adv Res. 2023 Jul;49:15-30. doi: 10.1016/j.jare.2022.09.006. Epub 2022 Sep 18.
8
Mitochondrial functions in plant immunity.线粒体在植物免疫中的作用。
Trends Plant Sci. 2022 Oct;27(10):1063-1076. doi: 10.1016/j.tplants.2022.04.007. Epub 2022 Jun 2.
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A natural allele of OsMS1 responds to temperature changes and confers thermosensitive genic male sterility.水稻雄性不育基因OsMS1的一个自然等位基因对温度变化作出响应,并赋予温敏型核雄性不育特性。
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A mitochondrial RNA processing protein mediates plant immunity to a broad spectrum of pathogens by modulating the mitochondrial oxidative burst.一种线粒体 RNA 加工蛋白通过调节线粒体氧化爆发介导植物对广谱病原体的免疫。
Plant Cell. 2022 May 24;34(6):2343-2363. doi: 10.1093/plcell/koac082.