Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control

Strigolactones (SLs) are a class of important plant hormones mainly regulating plant architecture such as branching, which is crucial for crop yield. It is valuable to study SL signaling pathway and its physiological function in sugarcane, the most important sugar crop, for further molecular breedin...

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Main Authors: Anqi Hu, Qiaoqiao Zhao, Li Chen, Jinping Zhao, Yuehua Wang, Kuiliang Feng, Ling Wu, Miao Xie, Xuemei Zhou, Langtao Xiao, Zhenhua Ming, Meng Zhang, Ruifeng Yao
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.747160/full
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author Anqi Hu
Qiaoqiao Zhao
Li Chen
Jinping Zhao
Jinping Zhao
Yuehua Wang
Kuiliang Feng
Ling Wu
Miao Xie
Xuemei Zhou
Langtao Xiao
Zhenhua Ming
Meng Zhang
Ruifeng Yao
author_facet Anqi Hu
Qiaoqiao Zhao
Li Chen
Jinping Zhao
Jinping Zhao
Yuehua Wang
Kuiliang Feng
Ling Wu
Miao Xie
Xuemei Zhou
Langtao Xiao
Zhenhua Ming
Meng Zhang
Ruifeng Yao
author_sort Anqi Hu
collection DOAJ
description Strigolactones (SLs) are a class of important plant hormones mainly regulating plant architecture such as branching, which is crucial for crop yield. It is valuable to study SL signaling pathway and its physiological function in sugarcane, the most important sugar crop, for further molecular breeding. Here, two putative SL receptors SsD14a/b and the interacting F-box protein SsMAX2 were identified in Saccharum spontaneum. SL induced both SsD14a and SsD14b to interact with SsMAX2 in yeast. SsD14a, but not SsD14b, could bind with AtMAX2 and AtSMXL7/SsSMXL7. Overexpression of SsD14a or SsMAX2 rescued the increased branching phenotypes of Arabidopsis thaliana d14-1 or max2-3 mutants, respectively. Moreover, the crystal structure of N-terminal truncated SsD14a was solved, with an overall structure identical to AtD14 and OsD14 in the open state, consistent with its conserved branching suppression capacity in Arabidopsis. In line with the biochemical observations, SsD14b could not completely complement in d14-1 although these two SsD14 proteins have almost identical primary sequences except for very few residues. Complement with the combination of SsD14b and SsMAX2 still failed to rescue the d14-1 max2-3 double mutant multi-branching phenotype, indicating SsD14b–AtSMXL7 complex formation is required for regulating branching. Mutagenesis analyses revealed that residue R310 at α10 helix of SsD14a was crucial for the binding with SsSMXL7/AtSMXL7 but not SsMAX2. The site-equivalent single-residue P304R substitution enabled SsD14b to bind with AtMAX2 and AtSMXL7/SsSMXL7 and to rescue the phenotype of d14-1 max2-3 together with SsMAX2. Moreover, this conserved Arg residue across species including rice and Arabidopsis determined the activity of SL receptors through maintaining their interaction with SMXL repressors. Taken together, our work identified conserved and divergent strigolactone receptors in sugarcane core SL signaling pathway and revealed a key residue crucial for plant branching control.
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spelling doaj.art-5ac1d94f8d45479084e27e55531d45b42022-12-21T17:16:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-11-011210.3389/fpls.2021.747160747160Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching ControlAnqi Hu0Qiaoqiao Zhao1Li Chen2Jinping Zhao3Jinping Zhao4Yuehua Wang5Kuiliang Feng6Ling Wu7Miao Xie8Xuemei Zhou9Langtao Xiao10Zhenhua Ming11Meng Zhang12Ruifeng Yao13State Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bio Resources, Guangxi Key Laboratory for Sugarcane Biology, College of Life Science and Technology, Guangxi University, Nanning, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaHunan Province Key Laboratory of Phytohormones and Growth Development, Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan Agricultural University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaHunan Province Key Laboratory of Phytohormones and Growth Development, Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan Agricultural University, Changsha, ChinaState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bio Resources, Guangxi Key Laboratory for Sugarcane Biology, College of Life Science and Technology, Guangxi University, Nanning, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Chemo/Biosensing and Chemometrics, Hunan Provincial Key Laboratory of Plant Functional Genomics and Developmental Regulation, College of Biology, Hunan University, Changsha, ChinaStrigolactones (SLs) are a class of important plant hormones mainly regulating plant architecture such as branching, which is crucial for crop yield. It is valuable to study SL signaling pathway and its physiological function in sugarcane, the most important sugar crop, for further molecular breeding. Here, two putative SL receptors SsD14a/b and the interacting F-box protein SsMAX2 were identified in Saccharum spontaneum. SL induced both SsD14a and SsD14b to interact with SsMAX2 in yeast. SsD14a, but not SsD14b, could bind with AtMAX2 and AtSMXL7/SsSMXL7. Overexpression of SsD14a or SsMAX2 rescued the increased branching phenotypes of Arabidopsis thaliana d14-1 or max2-3 mutants, respectively. Moreover, the crystal structure of N-terminal truncated SsD14a was solved, with an overall structure identical to AtD14 and OsD14 in the open state, consistent with its conserved branching suppression capacity in Arabidopsis. In line with the biochemical observations, SsD14b could not completely complement in d14-1 although these two SsD14 proteins have almost identical primary sequences except for very few residues. Complement with the combination of SsD14b and SsMAX2 still failed to rescue the d14-1 max2-3 double mutant multi-branching phenotype, indicating SsD14b–AtSMXL7 complex formation is required for regulating branching. Mutagenesis analyses revealed that residue R310 at α10 helix of SsD14a was crucial for the binding with SsSMXL7/AtSMXL7 but not SsMAX2. The site-equivalent single-residue P304R substitution enabled SsD14b to bind with AtMAX2 and AtSMXL7/SsSMXL7 and to rescue the phenotype of d14-1 max2-3 together with SsMAX2. Moreover, this conserved Arg residue across species including rice and Arabidopsis determined the activity of SL receptors through maintaining their interaction with SMXL repressors. Taken together, our work identified conserved and divergent strigolactone receptors in sugarcane core SL signaling pathway and revealed a key residue crucial for plant branching control.https://www.frontiersin.org/articles/10.3389/fpls.2021.747160/fullsugarcanestrigolactonereceptorD14MAX2SMXL
spellingShingle Anqi Hu
Qiaoqiao Zhao
Li Chen
Jinping Zhao
Jinping Zhao
Yuehua Wang
Kuiliang Feng
Ling Wu
Miao Xie
Xuemei Zhou
Langtao Xiao
Zhenhua Ming
Meng Zhang
Ruifeng Yao
Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
Frontiers in Plant Science
sugarcane
strigolactone
receptor
D14
MAX2
SMXL
title Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
title_full Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
title_fullStr Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
title_full_unstemmed Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
title_short Identification of Conserved and Divergent Strigolactone Receptors in Sugarcane Reveals a Key Residue Crucial for Plant Branching Control
title_sort identification of conserved and divergent strigolactone receptors in sugarcane reveals a key residue crucial for plant branching control
topic sugarcane
strigolactone
receptor
D14
MAX2
SMXL
url https://www.frontiersin.org/articles/10.3389/fpls.2021.747160/full
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