Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato

Perceiving incoming environmental information is critical for optimizing plant growth and development. Multiple B-box proteins (BBXs) play essential roles in light-dependent developmental processes in plants. However, whether BBXs function as a signal integrator between light and temperature in toma...

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Main Authors: Xin Bu, Xiujie Wang, Jiarong Yan, Ying Zhang, Shunyuan Zhou, Xin Sun, Youxin Yang, Golam Jalal Ahammed, Yufeng Liu, Mingfang Qi, Feng Wang, Tianlai Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.698525/full
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author Xin Bu
Xin Bu
Xin Bu
Xiujie Wang
Jiarong Yan
Ying Zhang
Shunyuan Zhou
Xin Sun
Youxin Yang
Golam Jalal Ahammed
Yufeng Liu
Yufeng Liu
Yufeng Liu
Mingfang Qi
Mingfang Qi
Mingfang Qi
Feng Wang
Feng Wang
Feng Wang
Tianlai Li
Tianlai Li
Tianlai Li
author_facet Xin Bu
Xin Bu
Xin Bu
Xiujie Wang
Jiarong Yan
Ying Zhang
Shunyuan Zhou
Xin Sun
Youxin Yang
Golam Jalal Ahammed
Yufeng Liu
Yufeng Liu
Yufeng Liu
Mingfang Qi
Mingfang Qi
Mingfang Qi
Feng Wang
Feng Wang
Feng Wang
Tianlai Li
Tianlai Li
Tianlai Li
author_sort Xin Bu
collection DOAJ
description Perceiving incoming environmental information is critical for optimizing plant growth and development. Multiple B-box proteins (BBXs) play essential roles in light-dependent developmental processes in plants. However, whether BBXs function as a signal integrator between light and temperature in tomato plants remains elusive. In this study, 31 SlBBX genes were identified from the newly released tomato (Solanum lycopersicum) genome sequences and were clustered into five subgroups. Gene structure and protein motif analyses showed relatively high conservation of closely clustered SlBBX genes within each subgroup; however, genome mapping analysis indicated the uneven distribution of the SlBBX genes on tomato chromosomes. Promoter cis-regulatory elements prediction and gene expression indicated that SlBBX genes were highly responsive to light, hormones, and stress conditions. Reverse genetic approaches revealed that disruption of SlBBX7, SlBBX9, and SlBBX20 largely suppressed the cold tolerance of tomato plants. Furthermore, the impairment of SlBBX7, SlBBX9, and SlBBX20 suppressed the photosynthetic response immediately after cold stress. Due to the impairment of non-photochemical quenching (NPQ), the excess photon energy and electron flow excited by low temperature were not consumed in SlBBX7-, SlBBX9-, and SlBBX20- silenced plants, leading to the over reduction of electron carriers and damage of the photosystem. Our study emphasized the positive roles of light signaling transcription factors SlBBXs in cold tolerance in tomato plants, which may improve the current understanding of how plants integrate light and temperature signals to adapt to adverse environments.
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spelling doaj.art-bf2c142d89b94f5680c9faef360740de2022-12-21T21:25:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-07-011210.3389/fpls.2021.698525698525Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in TomatoXin Bu0Xin Bu1Xin Bu2Xiujie Wang3Jiarong Yan4Ying Zhang5Shunyuan Zhou6Xin Sun7Youxin Yang8Golam Jalal Ahammed9Yufeng Liu10Yufeng Liu11Yufeng Liu12Mingfang Qi13Mingfang Qi14Mingfang Qi15Feng Wang16Feng Wang17Feng Wang18Tianlai Li19Tianlai Li20Tianlai Li21College of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture, Ministry of Education, Shenyang, ChinaNational & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaCollege of Land and Environment, Shenyang Agricultural University, Shenyang, ChinaCollege of Agronomy, Jiangxi Agricultural University, Nanchang, ChinaCollege of Forestry, Henan University of Science and Technology, Luoyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture, Ministry of Education, Shenyang, ChinaNational & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture, Ministry of Education, Shenyang, ChinaNational & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture, Ministry of Education, Shenyang, ChinaNational & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang, ChinaCollege of Horticulture, Shenyang Agricultural University, Shenyang, ChinaKey Laboratory of Protected Horticulture, Ministry of Education, Shenyang, ChinaNational & Local Joint Engineering Research Center of Northern Horticultural Facilities Design & Application Technology, Shenyang, ChinaPerceiving incoming environmental information is critical for optimizing plant growth and development. Multiple B-box proteins (BBXs) play essential roles in light-dependent developmental processes in plants. However, whether BBXs function as a signal integrator between light and temperature in tomato plants remains elusive. In this study, 31 SlBBX genes were identified from the newly released tomato (Solanum lycopersicum) genome sequences and were clustered into five subgroups. Gene structure and protein motif analyses showed relatively high conservation of closely clustered SlBBX genes within each subgroup; however, genome mapping analysis indicated the uneven distribution of the SlBBX genes on tomato chromosomes. Promoter cis-regulatory elements prediction and gene expression indicated that SlBBX genes were highly responsive to light, hormones, and stress conditions. Reverse genetic approaches revealed that disruption of SlBBX7, SlBBX9, and SlBBX20 largely suppressed the cold tolerance of tomato plants. Furthermore, the impairment of SlBBX7, SlBBX9, and SlBBX20 suppressed the photosynthetic response immediately after cold stress. Due to the impairment of non-photochemical quenching (NPQ), the excess photon energy and electron flow excited by low temperature were not consumed in SlBBX7-, SlBBX9-, and SlBBX20- silenced plants, leading to the over reduction of electron carriers and damage of the photosystem. Our study emphasized the positive roles of light signaling transcription factors SlBBXs in cold tolerance in tomato plants, which may improve the current understanding of how plants integrate light and temperature signals to adapt to adverse environments.https://www.frontiersin.org/articles/10.3389/fpls.2021.698525/fullBBXlightcold stressSolanum lycopersicumphotoinhibition
spellingShingle Xin Bu
Xin Bu
Xin Bu
Xiujie Wang
Jiarong Yan
Ying Zhang
Shunyuan Zhou
Xin Sun
Youxin Yang
Golam Jalal Ahammed
Yufeng Liu
Yufeng Liu
Yufeng Liu
Mingfang Qi
Mingfang Qi
Mingfang Qi
Feng Wang
Feng Wang
Feng Wang
Tianlai Li
Tianlai Li
Tianlai Li
Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
Frontiers in Plant Science
BBX
light
cold stress
Solanum lycopersicum
photoinhibition
title Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
title_full Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
title_fullStr Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
title_full_unstemmed Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
title_short Genome-Wide Characterization of B-Box Gene Family and Its Roles in Responses to Light Quality and Cold Stress in Tomato
title_sort genome wide characterization of b box gene family and its roles in responses to light quality and cold stress in tomato
topic BBX
light
cold stress
Solanum lycopersicum
photoinhibition
url https://www.frontiersin.org/articles/10.3389/fpls.2021.698525/full
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