EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton

EPSPS is a key gene in the shikimic acid synthesis pathway that has been widely used in breeding crops with herbicide resistance. However, its role in regulating cell elongation is poorly understood. Through the overexpression of EPSPS genes, we generated lines resistant to glyphosate that exhibit a...

Full description

Saved in:
Bibliographic Details
Main Authors: Qingdi Yan, Wei Hu, Chenxu Gao, Lan Yang, Jiaxian Yang, Renju Liu, Masum Billah, Yongjun Lin, Ji Liu, Pengfei Miao, Zhaoen Yang, Fuguang Li, Wenqiang Qin
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-10-01
Series:Journal of Integrative Agriculture
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2095311923003854
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849253505529806848
author Qingdi Yan
Wei Hu
Chenxu Gao
Lan Yang
Jiaxian Yang
Renju Liu
Masum Billah
Yongjun Lin
Ji Liu
Pengfei Miao
Zhaoen Yang
Fuguang Li
Wenqiang Qin
author_facet Qingdi Yan
Wei Hu
Chenxu Gao
Lan Yang
Jiaxian Yang
Renju Liu
Masum Billah
Yongjun Lin
Ji Liu
Pengfei Miao
Zhaoen Yang
Fuguang Li
Wenqiang Qin
author_sort Qingdi Yan
collection DOAJ
description EPSPS is a key gene in the shikimic acid synthesis pathway that has been widely used in breeding crops with herbicide resistance. However, its role in regulating cell elongation is poorly understood. Through the overexpression of EPSPS genes, we generated lines resistant to glyphosate that exhibit an unexpected dwarf phenotype. A representative line, DHR1, exhibits a stable dwarf phenotype throughout its entire growth period. Except for plant height, the other agronomic traits of DHR1 are similar to its transgenic explants ZM24. Paraffin section observations showed that DHR1 internodes are shortened due to reduced elongation and division of the internode cells. Exogenous hormones confirmed that DHR1 is not a classical brassinolide (BR)- or gibberellin (GA)-related dwarfing mutant. Hybridization analysis and fine mapping confirmed that the EPSPS gene is the causal gene for dwarfism, and the phenotype can be inherited in different genotypes. Transcriptome and metabolome analyses showed that genes associated with the phenylpropanoid synthesis pathway are enriched in DHR1 compared with ZM24. Flavonoid metabolites are enriched in DHR1, whereas lignin metabolites are reduced. The enhancement of flavonoids likely results in differential expression of auxin signal pathway genes and alters the auxin response, subsequently affecting cell elongation. This study provides a new strategy for generating dwarfs and will accelerate advancements in light simplification in the cultivation and mechanized harvesting of cotton.
format Article
id doaj-art-6e94ce12060e4172ae013c516a2f4021
institution Kabale University
issn 2095-3119
language English
publishDate 2024-10-01
publisher KeAi Communications Co., Ltd.
record_format Article
series Journal of Integrative Agriculture
spelling doaj-art-6e94ce12060e4172ae013c516a2f40212025-08-20T03:56:18ZengKeAi Communications Co., Ltd.Journal of Integrative Agriculture2095-31192024-10-0123103437345610.1016/j.jia.2023.11.002EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cottonQingdi Yan0Wei Hu1Chenxu Gao2Lan Yang3Jiaxian Yang4Renju Liu5Masum Billah6Yongjun Lin7Ji Liu8Pengfei Miao9Zhaoen Yang10Fuguang Li11Wenqiang Qin12State Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research, Huazhong Agricultural University, Wuhan 430070, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaNational Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research, Huazhong Agricultural University, Wuhan 430070, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572025, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572025, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; State Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, China; Correspondence Zhaoen YangState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; State Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Zhengzhou University, Zhengzhou 450066, China; Correspondence Fuguang LiState Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572025, China; Correspondence Wenqiang QinEPSPS is a key gene in the shikimic acid synthesis pathway that has been widely used in breeding crops with herbicide resistance. However, its role in regulating cell elongation is poorly understood. Through the overexpression of EPSPS genes, we generated lines resistant to glyphosate that exhibit an unexpected dwarf phenotype. A representative line, DHR1, exhibits a stable dwarf phenotype throughout its entire growth period. Except for plant height, the other agronomic traits of DHR1 are similar to its transgenic explants ZM24. Paraffin section observations showed that DHR1 internodes are shortened due to reduced elongation and division of the internode cells. Exogenous hormones confirmed that DHR1 is not a classical brassinolide (BR)- or gibberellin (GA)-related dwarfing mutant. Hybridization analysis and fine mapping confirmed that the EPSPS gene is the causal gene for dwarfism, and the phenotype can be inherited in different genotypes. Transcriptome and metabolome analyses showed that genes associated with the phenylpropanoid synthesis pathway are enriched in DHR1 compared with ZM24. Flavonoid metabolites are enriched in DHR1, whereas lignin metabolites are reduced. The enhancement of flavonoids likely results in differential expression of auxin signal pathway genes and alters the auxin response, subsequently affecting cell elongation. This study provides a new strategy for generating dwarfs and will accelerate advancements in light simplification in the cultivation and mechanized harvesting of cotton.http://www.sciencedirect.com/science/article/pii/S2095311923003854EPSPScottonT-DNAdwarfismherbicide resistance
spellingShingle Qingdi Yan
Wei Hu
Chenxu Gao
Lan Yang
Jiaxian Yang
Renju Liu
Masum Billah
Yongjun Lin
Ji Liu
Pengfei Miao
Zhaoen Yang
Fuguang Li
Wenqiang Qin
EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
Journal of Integrative Agriculture
EPSPS
cotton
T-DNA
dwarfism
herbicide resistance
title EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
title_full EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
title_fullStr EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
title_full_unstemmed EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
title_short EPSPS regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
title_sort epsps regulates cell elongation by disrupting the balance of lignin and flavonoid biosynthesis in cotton
topic EPSPS
cotton
T-DNA
dwarfism
herbicide resistance
url http://www.sciencedirect.com/science/article/pii/S2095311923003854
work_keys_str_mv AT qingdiyan epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT weihu epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT chenxugao epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT lanyang epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT jiaxianyang epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT renjuliu epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT masumbillah epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT yongjunlin epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT jiliu epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT pengfeimiao epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT zhaoenyang epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT fuguangli epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton
AT wenqiangqin epspsregulatescellelongationbydisruptingthebalanceofligninandflavonoidbiosynthesisincotton