OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice

The formation of the anther wall and the development of pollen processes, central to rice fertility and yield, are highly dependent on the synthesis and accumulation of lipid polymers. Although several regulatory factors related to lipid biosynthesis during pollen wall development have been identifi...

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Main Authors: Dai-bo Chen, Ran Zhou, Hui-min Wang, Pei-pei Zhang, Zheng-fu Yang, Dan-dan Xuan, Ying-xin Zhang, Xiao-deng Zhan, Li-yong Cao, Shi-hua Cheng, Lian-ping Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1508828/full
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author Dai-bo Chen
Ran Zhou
Ran Zhou
Hui-min Wang
Pei-pei Zhang
Zheng-fu Yang
Zheng-fu Yang
Dan-dan Xuan
Ying-xin Zhang
Xiao-deng Zhan
Li-yong Cao
Li-yong Cao
Shi-hua Cheng
Lian-ping Sun
Lian-ping Sun
author_facet Dai-bo Chen
Ran Zhou
Ran Zhou
Hui-min Wang
Pei-pei Zhang
Zheng-fu Yang
Zheng-fu Yang
Dan-dan Xuan
Ying-xin Zhang
Xiao-deng Zhan
Li-yong Cao
Li-yong Cao
Shi-hua Cheng
Lian-ping Sun
Lian-ping Sun
author_sort Dai-bo Chen
collection DOAJ
description The formation of the anther wall and the development of pollen processes, central to rice fertility and yield, are highly dependent on the synthesis and accumulation of lipid polymers. Although several regulatory factors related to lipid biosynthesis during pollen wall development have been identified, the molecular mechanisms controlling these processes remain poorly understood. In this study, a male-sterile rice mutant, lap3, was identified, characterized by normal vegetative growth but complete male sterility due to delayed programmed cell death (PCD) in tapetal cells and defects in anther cuticle and pollen exine formation. Map-based cloning revealed that OsLAP3 is a new allele of the strictosidine synthase-like gene, OsSTRL2. Functional analysis, including complementation and CRISPR/Cas9-based gene editing, confirmed that the 2-nucleotide deletion in the OsLAP3 is responsible for the male sterility phenotype. OsLAP3 is homologous to the maize ZmMS45, the core recessive nuclear sterile gene of maize Seed Production Technology (SPT), and localizes to the endoplasmic reticulum and plays a conserved role in anther development and pollenformation. Gene expression analysis revealed a significant downregulation of key genes involved in anther development and sporopollenin biosynthesis in lap3 anthers. Furthermore, lipid profiling demonstrated a marked reduction in both wax and cutin content. These findings establish OsLAP3 as a critical regulator of fatty acid synthesis and highlight its role in anther cuticle formation and pollen exine development. The findings of this study provide valuable insights into the molecular regulation of lipid biosynthesis during rice male reproductive development and offer potential applications for hybrid rice breeding.
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spelling doaj-art-a133d432da814cbe9f370a4ebb49aa1e2025-01-20T17:36:30ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.15088281508828OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in riceDai-bo Chen0Ran Zhou1Ran Zhou2Hui-min Wang3Pei-pei Zhang4Zheng-fu Yang5Zheng-fu Yang6Dan-dan Xuan7Ying-xin Zhang8Xiao-deng Zhan9Li-yong Cao10Li-yong Cao11Shi-hua Cheng12Lian-ping Sun13Lian-ping Sun14State Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaNational Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya, ChinaJiangxi Academy of Agricultural Sciences, Nanchang, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, Zhejiang, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaNational Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaState Key Laboratory of Rice Biology and Breeding, National Center of Rice Improvement, China National Rice Research Institute, Hangzhou, ChinaNational Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya, ChinaThe formation of the anther wall and the development of pollen processes, central to rice fertility and yield, are highly dependent on the synthesis and accumulation of lipid polymers. Although several regulatory factors related to lipid biosynthesis during pollen wall development have been identified, the molecular mechanisms controlling these processes remain poorly understood. In this study, a male-sterile rice mutant, lap3, was identified, characterized by normal vegetative growth but complete male sterility due to delayed programmed cell death (PCD) in tapetal cells and defects in anther cuticle and pollen exine formation. Map-based cloning revealed that OsLAP3 is a new allele of the strictosidine synthase-like gene, OsSTRL2. Functional analysis, including complementation and CRISPR/Cas9-based gene editing, confirmed that the 2-nucleotide deletion in the OsLAP3 is responsible for the male sterility phenotype. OsLAP3 is homologous to the maize ZmMS45, the core recessive nuclear sterile gene of maize Seed Production Technology (SPT), and localizes to the endoplasmic reticulum and plays a conserved role in anther development and pollenformation. Gene expression analysis revealed a significant downregulation of key genes involved in anther development and sporopollenin biosynthesis in lap3 anthers. Furthermore, lipid profiling demonstrated a marked reduction in both wax and cutin content. These findings establish OsLAP3 as a critical regulator of fatty acid synthesis and highlight its role in anther cuticle formation and pollen exine development. The findings of this study provide valuable insights into the molecular regulation of lipid biosynthesis during rice male reproductive development and offer potential applications for hybrid rice breeding.https://www.frontiersin.org/articles/10.3389/fpls.2024.1508828/fullricemale sterilityOsLAP3pollen exineanther development
spellingShingle Dai-bo Chen
Ran Zhou
Ran Zhou
Hui-min Wang
Pei-pei Zhang
Zheng-fu Yang
Zheng-fu Yang
Dan-dan Xuan
Ying-xin Zhang
Xiao-deng Zhan
Li-yong Cao
Li-yong Cao
Shi-hua Cheng
Lian-ping Sun
Lian-ping Sun
OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
Frontiers in Plant Science
rice
male sterility
OsLAP3
pollen exine
anther development
title OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
title_full OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
title_fullStr OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
title_full_unstemmed OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
title_short OsLAP3/OsSTRL2, encoding a rice strictosidine synthase, is required for anther cuticle formation and pollen exine patterning in rice
title_sort oslap3 osstrl2 encoding a rice strictosidine synthase is required for anther cuticle formation and pollen exine patterning in rice
topic rice
male sterility
OsLAP3
pollen exine
anther development
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1508828/full
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