Abstract
The B-box proteins (BBXs) are a family of zinc finger proteins containing one/two B-box domain(s). Compared with intensive studies of animal BBXs, investigations of the plant BBX family are limited, though some specific plant BBXs have been demonstrated to act as transcription factors in the regulation of flowering and photomorphogenesis. In this study, using a global search of the apple (Malus domestica Borkh.) genome, a total of 64 members of BBX (MdBBX) were identified. All the MdBBXs were divided into five groups based on the phylogenetic relationship, numbers of B-boxes contained and whether there was with an additional CCT domain. According to the characteristics of organ-specific expression, MdBBXs were divided into three groups based on the microarray information. An analysis of cis-acting elements showed that elements related to the stress response were prevalent in the promoter sequences of most MdBBXs. Twelve MdBBX members from different groups were randomly selected and exposed to abiotic stresses. Their expressions were up-regulated to some extent in the roots and leaves. Six among 12 MdBBXs were sensitive to osmotic pressure, salt, cold stress and exogenous abscisic acid treatment, with their expressions enhanced more than 20-fold. Our results suggested that MdBBXs may take part in response to abiotic stress.
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Bai S, Saito T, Honda C, Hatsuyama Y, Ito A, Moriguchi T (2014) An apple B-box protein, MdCOL11, is involved in UV-B- and temperature-induced anthocyanin biosynthesis. Planta 240:1051–1062
Beenders B, Jones PL, Bellini M (2007) The tripartite motif of nuclear factor 7 is required for its association with transcriptional units. Mol Cell Biol 27:2615–2624
Borden KL (1998) RING fingers and B-boxes: zinc-binding protein–protein interaction domains. Biochem Cell Biol 76:351–358
Chaurasia AK, Patil HB, Azeez A, Subramaniam VR, Krishna B, Sane AP, Sane PV (2016) Molecular characterization of CONSTANS-Like (COL) genes in banana (Musa acuminata L. AAA Group, cv. Grand Nain). Physiol Mol Biol Plants 22:1–15
Cheng XF, Wang ZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43:758–768
Chia TY, Muller A, Jung C, Mutasa-Gottgens ES (2008) Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus. J Exp Bot 59:2735–2748
Chu Z, Wang X, Li Y, Yu H, Li J, Lu Y, Li H, Ouyang B (2016) Genomic organization, phylogenetic and expression analysis of the B-BOX gene family in tomato. Front Plant Sci 7:1552
Crocco CD, Botto JF (2013) BBX proteins in green plants: insights into their evolution, structure, feature and functional diversification. Gene 531:44–52
Cui HR, Zhang ZR, Lv W, Xu JN, Wang XY (2015) Genome-wide characterization and analysis of F-box protein-encoding genes in the Malus domestica genome. Mol Genet Genomics 290:1435–1446
Datta S, Hettiarachchi GH, Deng XW, Holm M (2006) Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth. Plant Cell 18:70–84
Datta S, Hettiarachchi C, Johansson H, Holm M (2007) SALT TOLERANCE HOMOLOG2, a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development. Plant Cell 19:3242–3255
Datta S, Johansson H, Hettiarachchi C, Irigoyen ML, 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
Du D, Zhang Q, Cheng T, Pan H, Yang W, Sun L (2013) Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume. Mol Biol Rep 40:1937–1946
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763
Fan XY, Sun Y, Cao DM, Bai MY, Luo XM, Yang HJ, Wei CQ, Zhu SW, Sun Y, Chong K, Wang ZY (2012) BZS1, a B-box protein, promotes photomorphogenesis downstream of both brassinosteroid and light signaling pathways. Mol Plant 5:591–600
Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19:460–470
Gasic K, Hernandez A, Korban SS (2004) RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Biol Rep 22:437–438
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
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
Jeong D-H, Sung S-K, An G (1999) Molecular cloning and characterization of CONSTANS-Like cDNA clones of the fuji apple. J Plant Biol 42:23–31
Jia F, Wu B, Li H, Huang J, Zheng C (2013) Genome-wide identification and characterisation of F-box family in maize. Mol Genet Genom 288:559–577
Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040-D1045
Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, Wu SH (2009) The Arabidopsis B-box zinc finger family. Plant Cell 21:3416–3420
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, S. R (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li Y, Wu B, Yu Y, Yang G, Wu C, Zheng C (2011) Genome-wide analysis of the RING finger gene family in apple. Mol Genet Genom 286:81–94
Liu RH, Meng JL (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Yi Chuan 25:317–321
Massiah MA, Simmons BN, Short KM, Cox TC (2006) Solution structure of the RBCC/TRIM B-box1 domain of human MID1: B-box with a RING. J Mol Biol 358:532–545
Massiah MA, Matts JA, Short KM, Simmons BN, Singireddy S, Yi Z, Cox TC (2007) Solution structure of the MID1 B-box2 CHC(D/C)C(2)H(2) zinc-binding domain: insights into an evolutionarily conserved RING fold. J Mol Biol 369:1–10
Meroni G, Diez-Roux G (2005) TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases. Bioessays 27:1147–1157
Min JH, Chung JS, Lee KH, Kim CS (2015) The CONSTANS-like 4 transcription factor, AtCOL4, positively regulates abiotic stress tolerance through an abscisic acid-dependent manner in Arabidopsis. J Integr Plant Biol 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. J Exp Bot 54:2231–2237
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
Robson F, Costa MM, Hepworth SR, Vizir I, Pineiro M, Reeves PH, 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 J 28:619–631
Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289:768–771
Su H, Zhang S, Yuan X, Chen C, Wang X-F, Hao Y-J (2013) Genome-wide analysis and identification of stress-responsive genes of the NAM-ATAF1,2-CUC2 transcription factor family in apple. Plant Physiol Biochem 71:11–21
Suarez-Lopez 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
Talar U, Kielbowicz-Matuk A, Czarnecka J, Rorat T (2017) Genome-wide survey of B-box proteins in potato (Solanum tuberosum)—identification, characterization and expression patterns during diurnal cycle, etiolation and de-etiolation. PLoS One 12:e0177471
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Torok M, Etkin LD (2001) Two B or not two B? Overview of the rapidly expanding B-box family of proteins. Differentiation 67:63–71
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42:833–839
Wang H, Zhang Z, Li H, Zhao X, Liu X, Ortiz M, Lin C, Liu B (2013) CONSTANS-LIKE 7 regulates branching and shade avoidance response in Arabidopsis. J Exp Bot 64:1017–1024
Wang XL, Zhong Y, Cheng ZM, Xiong JS (2015) Divergence of the bZIP gene family in strawberry, peach, and apple suggests multiple modes of gene evolution after duplication. Int J Genom 2015:536943
Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18:2971–2984
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552
Xu JN, Xing SS, Zhang ZR, Chen XS, Wang XY (2016) Genome-wide identification and expression analysis of the tubby-like protein family in the Malus domestica genome. Front Plant Sci 7:1693
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483
Yuan H, Zhao K, Lei H, Shen X, Liu Y, Liao X, Li T (2013) Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genom 14:297
Zhao T, Liang D, Wang P, Liu J, Ma F (2012) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genomics 287:423–436
Zhao J, Guo R, Guo C, Hou H, Wang X, Gao H (2016) Evolutionary and expression analyses of the apple basic leucine zipper transcription factor family. Front Plant Sci 7:376
Zou Z, Wang R, Wang R, Yang S, Yang Y (2017) Genome-wide identification, phylogenetic analysis, and expression profiling of the BBX family genes in pear. J Hortic Sci Biotechnol. doi:10.1080/14620316.2017.1338927
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This work was supported by Special Research Fund of Public Welfare of China Agricultural Ministry (201303093).
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Designed the experiments: XYW and XL. Performed the experiments: XL, RL and YQD. Analyzed the data: XL, RL,YQD and XSC. Wrote the paper: XYW and XL. All authors read and approved the manuscript.
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438_2017_1386_MOESM6_ESM.png
Distribution of the B-box genes in apple chromosomes. Tandem duplication genes are indicated by light green and homologous regions are marked in gray shade (PNG 296 KB)
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Liu, X., Li, R., Dai, Y. et al. Genome-wide identification and expression analysis of the B-box gene family in the Apple (Malus domestica Borkh.) genome. Mol Genet Genomics 293, 303–315 (2018). https://doi.org/10.1007/s00438-017-1386-1
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DOI: https://doi.org/10.1007/s00438-017-1386-1