玉米B-box锌指蛋白家族基因的鉴定、进化、表达及蛋白互作分析

doi:10.1016/j.jia.2022.08.091

摘要/Abstract

摘要：

B-box（BBX）基因家族编码的蛋白是由包含锌指结构的转录因子组成，其N端有一个或两个高度保守的B-box基序。BBX蛋白在植物生长发育的各个方面起着至关重要的作用，包括幼苗的光形态发生、避荫、开花时间以及生物和非生物胁迫响应。目前,各国的研究者已经从几种植物中鉴定了BBX的家族成员，然而玉米中的BBX家族成员还知之甚少。通过对玉米BBX家族基因的全基因组鉴定、表达和互作的综合分析，可为了解其功能提供有用信息。本研究共鉴定出36个玉米BBX家族成员，进化分析显示其分布于三个主要分支。在每个主分支中ZmBBXs都具有相似的结构域、基序和基因组结构。基因重复分析表明，玉米BBX蛋白家族的扩张主要是通过片段重复来完成的。利用实时荧光定量PCR技术，本研究分析了ZmBBXs在不同器官组织和不同非生物胁迫条件下的表达。利用生物信息学工具，本研究建立了ZmBBXs蛋白的相互作用网络，并通过双分子荧光互补（BiFC）试验进行了验证。本研究的发现有助于理解ZmBBX家族的复杂性，并为揭示ZmBBX蛋白的生物学功能提供新的线索。

Abstract:

The B-box (BBX) family of proteins consists of zinc-finger transcription factors with one or two highly conserved B-box motifs at their N-termini. BBX proteins play crucial roles in various aspects of plant growth and development, including seedling photomorphogenesis, shade avoidance, flowering time, and biotic and abiotic stress responses. Previous studies have identified many different BBXs from several plant species, although the BBX family members in maize are largely unknown. Genome-wide identification and comprehensive analysis of maize BBX (ZmBBX) expression and interaction networks would therefore provide valuable information for understanding their functions. In this study, 36 maize BBXs in three major clades were identified. The ZmBBXs within a given clade were found to share similar domains, motifs, and genomic structures. Gene duplication analyses revealed that the expansion of BBX proteins in maize has mainly occurred by segmental duplication. The expression levels of ZmBBXs were analyzed in various organs and tissues, and under different abiotic stress conditions. Protein–protein interaction networks of ZmBBXs were established using bioinformatic tools and verified by bimolecular fluorescence complementation (BiFC) assays. Our findings can facilitate a greater understanding of the complexity of the ZmBBX family and provide novel clues for unravelling ZmBBX protein functions

Key words: maize , B-box family protein , , evolution , , expression , , protein interaction

. 玉米B-box锌指蛋白家族基因的鉴定、进化、表达及蛋白互作分析 [J]. Journal of Integrative Agriculture, 2023, 22(2): 371-388.

XU Xiao-hui, LI Wen-lan, YANG Shu-ke, ZHU Xiang-zhen, SUN Hong-wei, LI Fan, LU Xing-bo, CUI Jin-jie. Identification, evolution, expression and protein interaction analysis of genes encoding B-box zinc-finger proteins in maize[J]. Journal of Integrative Agriculture, 2023, 22(2): 371-388.

参考文献

Borden K L. 1998. RING fingers and B-boxes: zinc-binding protein–protein interaction domains. Biochemistry and Cell Biology, 76, 351–358.
Chang C S J, Li Y H, Chen L T, Hsieh W P, Shin J, Jane W N, Chou S J, Choi G, Hu J M, Somerville S, Wu S H. 2008. LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant Journal, 54, 205–219.
Cheng X F, Wang Z Y. 2005. Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant Journal, 43, 758–768.
Crocco C D, Botto J F. 2013. BBX proteins in green plants: insights into their evolution, structure feather and function diversification. Gene, 15, 44–52.
Datta S, Hettiarachchi C, Johansson H, Holm M. 2007. SALT TOLERANCE HOMOLOG 2, a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development. Plant Cell, 19, 3242–3255.
Datta S, Hettiarachchi G H C M, Deng X W, Holm M. 2006. Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. Plant Cell, 18, 70–84.
Datta S, Johansson H, Hettiarachchi C, Irigoyen M L, Desai M, Rubio V, Holm M. 2008. LZF1/SALT TOLERANCE HOMOLOG3, an Arabidopsis B-box protein involved in light dependent development and gene expression, undergoes COP1-mediated ubiquitination. Plant Cell, 20, 2324–2338.
Fan X Y, Sun Y, Cao D M, Bai M Y, Luo X M, Yang H J, Wei C Q, Zhu S W, Sun Y, Chong K, Wang Z Y. 2012. BZS1, a B-box protein, promotes photomorphogenesis downstream of both brassinosteroid and light signaling pathways. Molecular Plant, 5, 591–600.
Gangappa S N, Crocco C D, Johansson H, Datta S, Hettiarachchi C, Holm M, Botto J F. 2013. The Arabidopsis B-box protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell, 25, 1243–1257.
Gu Z, Cavalcanti A, Chen F C, Bouman P, Li W H. 2002. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Molecular Biology and Evolution, 19, 256–262.
Hassidim M, Harir Y, Yakir E, Kron I, Green R M. 2009. Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta, 230, 481–491.
Holm M, Hardtke C S, Gaudet R, Deng X W. 2001. Identification of a structural motif that confers specific interaction with the WD40 repeat domain of Arabidopsis COP1. EMBO Journal, 20, 118–127.
Huang J, Zhao X, Weng X, Wang L, Xie W. 2012. The rice B-box zinc finger gene family: genomic identification, characterization, expression profiling and diurnal analysis. PLoS ONE, 7, e48242.
Jang S, Marchal V, Panigrahi K C S, Wenkel S, Soppe W, Deng X W, Valverde F, Coupland G. 2008. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO Journal, 27, 1277–1288.
Kenrick P, Crane P R. 1997. The origin and early evolution of plants on land. Nature, 389, 33–39.
Khanna R, Kronmiller B, Maszle D R, Coupland G, Holm M, Mizuno T, Wu S H. 2009. The Arabidopsis B-box zinc finger family. Plant Cell, 21, 3416–3420.
Klug A, Schwabe J W. 1995. Protein motifs 5. Zinc fingers. FASEB Journal, 9, 597–604.
Lau K, Podolec R, Chappuis R, Ulm R, Hothorn M. 2019. Plant photoreceptors and their signaling components compete for binding to the ubiquitin ligase COP1 using their VP-peptide motifs. EMBO Journal, 38, e102140.
Laubinger S, Marchal V, Le Gourrierec J, Wenkel S, Adrian J, Jang S, Kulajta C, Braun H, Coupland G, Hoecker U. 2006. Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development, 133, 3213–3222.
Li W, Wang J, Sun Q, Li W, Yu Y, Zhao M, Meng Z. 2017. Expression analysis of genes encoding double B-box zinc finger proteins in maize. Functional & Integrative Genomics, 17, 653–666.
Liu J, Shen J, Xu Y, Li X, Xiao J, Xiong L. 2016. Ghd2, a CONSTANS-like gene, confers drought sensitivity through regulation of senescence in rice. Journal of Experimental Botany, 67, 5785–5798.
Liu H, Dong S, Sun D, Liu W, Gu F, Liu Y, Guo T, Wang J F, Chen Z Q. 2016. CONSTANS-Like 9 (OsCOL9) interacts with receptor for activated C-Kinase 1 (OsRACK1) to regulate blast resistance through salicylic acid and ethylene signaling pathways. PLoS ONE, 11, e166249.
Liu X, Li R, Dai Y, Chen X, Wang X. 2018. Genome-wide identification and expression analysis of the B-box gene family in the apple (Malus domestica Borkh.) genome. Molecular Genetics and Genomics, 293, 303–315.
Liu X, Li R, Dai Y, Yuan L, Sun Q, Zhang S, Wang X Y. 2019. A B-box zinc finger protein, MdBBX10, enhanced salt and drought stresses tolerance in Arabidopsis. Plant Molecular Biology, 99, 437–447.
Min J H, Chung J S, Lee K H, Kim C S. 2015. The CONSTANS-like 4 transcription factor, AtCOL4, positively regulates abiotic stress tolerance through an abscisic acid-dependent manner in Arabidopsis. Journal of Integrative Plant Biology, 57, 313–324.
Nagaoka S, Takano T. 2003. Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis. Journal of Experimental Botany, 54, 2231–2237.
Narusaka M, Kawai K, Izawa N, Seki M, Shinozaki K, Seo S, Kobayashi M, Shiraishi T, Narusaka Y. 2008. Gene coding for SigA-binding protein from Arabidopsis appears to be transcriptionally up-regulated by salicylic acid and NPR1-dependent mechanisms. Journal of General Plant Pathology, 74, 345–354.
Park H Y, Lee S Y, Seok H Y, Kim S H, Sung Z R, Moon Y H. 2011. EMF1 interacts with EIP1, EIP6 or EIP9 involved in the regulation of flowering time in Arabidopsis. Plant and Cell Physiology, 52, 1376–1388.
Peers G, Niyogi K K. 2008. Pond scum genomics: the genomes of Chlamydomonas and Ostreococcus. Plant Cell, 20, 502–507.
Putterill J, Robson F, Lee K, Simon R, Coupland G. 1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell, 80, 847–857.
Qi Q, Gibson A, Fu X, Zheng M Y, Kuehn R, Wang Y, Navarro S, Morrell J A, Jiang D M, Simmons G, Bell E, Ivleva N B, McClerren A L, Loida P, Ruff T G, Petracek M, Preuss S. 2012. Involvement of the N-terminal B-box domain of Arabidopsis BBX32 protein in interaction with soybean BBX62 protein. Journal of Biological Chemistry, 287, 31482–31493.
Qin W, Yu Y, Jin Y, Wang X, Liu J, Xi J, Li Z, Li H, Zhao G, Hu W, Chen C, Li F, Yang Z. 2018. Genome-wide analysis elucidateds the role of CONSTANS-like genes in stress responses of cotton. International Journal of Molecular Sciences, 19, 2658.
Robson F, Costa M M, Hepworth S R, Vizir I, Piñeiro M, Reeves P H, Putterill J, Coupland G. 2001. Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant Journal, 28, 619–631.
Steinbach Y. 2019. The Arabidopsis thaliana CONSTANS-LIKE 4 (COL4) - A modulator of flowering time. Frontiers in Plant Science, 10, 651.
Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature, 410, 1116–1120.
Sun Y, Fan X Y, Cao D M, Tang W, He K, Zhu J Y, He J X, Bai M Y, Zhu S W, Oh E, Patil S, Kim T W, Ji H K, Wong W H, Rhee S Y, Wang Z Y. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell, 19, 765–777.
Tiwari S B, Shen Y, Chang H C, Hou Y, Harris A, Ma S F, McPartland M, Hymus G J, Adam L, Marion C, Belachew A, Repetti P P, Reuber T L, Ratcliffe O J. 2010. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytologist, 187, 57–66.
Torok M, Etkin D L. 2000. Two B or not two B? Overview of the rapidly expanding B-box family of proteins. Differentiation, 67, 63–71.
Tripathi P, Carvallo M, Hamilton E E, Preuss S, Kay S A. 2017. Arabidopsis B-BOX32 interacts with CONSTANS-LIKE3 to regulate flowering. Proceedings of the National Academy of Sciences of the United States of America, 114, 172–177.
Walley J W, Sartor R C, Shen Z, Schmitz R J, Wu K J, Urich M A, Nery J R, Smith L G, Schnable J C, Ecker J R, Briggs S P. 2016. Integration of omic networks in a developmental atlas of maize. Science, 353, 814–818.
Wang C Q, Guthrie C, Sarmast M K, Dehesh K. 2014. BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T
transcription, defining a flowering time checkpoint in Arabidopsis. Plant Cell, 26, 3589–3602.
Wang C Q, Sarmast M K, Jiang J, Dehesh K. 2015. The transcriptional regulator BBX19 promotes hypocotyl growth by facilitating COP1-mediated EARLY FLOWERING3 degradation in Arabidbopsis. Plant Cell, 27, 1128–1139.
Wang Q, Tu X, Zhang J, Chen X, Rao L. 2013. Heat stress-induced BBX18 negatively regulates the thermotolerance in Arabidopsis. Molecular Biology Reports, 40, 2679–2688.
Wang Q, Zeng J, Deng K, Tu X, Zhao X, Tang D, Liu X. 2011. DBB1a, involved in gibberellin homeostasis, functions as a negative regulator of blue light-mediated hypocotyl elongation in Arabidopsis. Planta, 233, 13–23.
Xu D, Jiang Y, Li J, Lin F, Holm M, Deng X W. 2016. BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation. Proceedings of the National Academy of Sciences of the United States of America, 113, 7655–7660.
Xu X H, Chen H, Sang Y L, Wang F, Ma J P, Gao, X Q, Zhang X S. 2012. Identification of genes specifically or preferentially expressed in maize silk reveals similarity and diversity in transcript abundance of different dry stigmas. BMC Genomics, 13, 294.
Yamawaki S, Yamashino T, Nakamichi N, Nakanishi H, Mizuno T. 2011. Light-responsive double B-box containing transcription factors are conserved in Physcomitrella pattens. Bioscience Biotechnology and Biochemistry, 75, 2037–2041.
Yang S, Zhang X, Yue J X, Tian D, Chen J Q. 2008. Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics, 280, 187–198.
Zhang Z, Ji R, Li H, Zhao T, Liu J, Lin C, Liu B. 2014. CONSTANS-LIKE 7 (COL7) is involved in phytochrome B (phyB)-mediated light-quality regulation of auxin homeostasis. Molecular Plant, 7, 1429–1440.
Zobell O, Coupland G, Reiss B. 2005. The family of CONSTANS-like genes in Physcomitrella patens. Plant Biology, 7, 266–275.