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

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...

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Main Authors: Shaowei Zhang, Xueli An, Yilin Jiang, Quancan Hou, Bin Ma, Qingping Jiang, Kai Zhang, Lina Zhao, Xiangyuan Wan
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55208-8
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author Shaowei Zhang
Xueli An
Yilin Jiang
Quancan Hou
Bin Ma
Qingping Jiang
Kai Zhang
Lina Zhao
Xiangyuan Wan
author_facet Shaowei Zhang
Xueli An
Yilin Jiang
Quancan Hou
Bin Ma
Qingping Jiang
Kai Zhang
Lina Zhao
Xiangyuan Wan
author_sort Shaowei Zhang
collection DOAJ
description 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.
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issn 2041-1723
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spelling doaj-art-7a178d24eb4b4cf8af5b6041065e82ac2025-01-05T12:34:35ZengNature PortfolioNature Communications2041-17232024-12-0115111910.1038/s41467-024-55208-8Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolismShaowei Zhang0Xueli An1Yilin Jiang2Quancan Hou3Bin Ma4Qingping Jiang5Kai Zhang6Lina Zhao7Xiangyuan Wan8Research Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingResearch Institute of Biology and Agriculture, School of Chemistry and Biological Engineering, University of Science and Technology BeijingAbstract 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.https://doi.org/10.1038/s41467-024-55208-8
spellingShingle Shaowei Zhang
Xueli An
Yilin Jiang
Quancan Hou
Bin Ma
Qingping Jiang
Kai Zhang
Lina Zhao
Xiangyuan Wan
Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
Nature Communications
title Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
title_full Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
title_fullStr Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
title_full_unstemmed Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
title_short Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism
title_sort plastid localized zmenr1 zmhad1 complex ensures maize pollen and anther development through regulating lipid and ros metabolism
url https://doi.org/10.1038/s41467-024-55208-8
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