Genome-wide identification and characterization of the bHLH gene family in tomato

BMC Genomics

Hong-Qing Ling¹  Hua-Jie Fan¹  Hua Sun¹ 

[1] State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, No. 1 West Beichen Road, Beijing 100101, Chaoyang District, China

关键词: fruit development;    transcription factor;    bHLH gene family;    Solanum lycopersicum;    Tomato;   

Others  :  1109907
DOI  :  10.1186/s12864-014-1209-2

 received in 2014-06-27, accepted in 2014-12-30,  发布年份 2015

【 摘 要 】

Background

The basic helix-loop-helix (bHLH) proteins are a large superfamily of transcription factors, and play a central role in a wide range of metabolic, physiological, and developmental processes in higher organisms. Tomato is an important vegetable crop, and its genome sequence has been published recently. However, the bHLH gene family of tomato has not been systematically identified and characterized yet.

Results

In this study, we identified 159 bHLH protein-encoding genes (SlbHLH) in tomato genome and analyzed their structures. Although bHLH domains were conserved among the bHLH proteins between tomato and Arabidopsis, the intron sequences and distribution of tomato bHLH genes were extremely different compared with Arabidopsis. The gene duplication analysis showed that 58.5% and 6.3% of SlbHLH genes belonged to low-stringency and high-stringency duplication, respectively, indicating that the SlbHLH genes are mainly generated via short low-stringency region duplication in tomato. Subsequently, we classified the SlbHLH genes into 21 subfamilies by phylogenetic tree analysis, and predicted their possible functions by comparison with their homologous genes of Arabidopsis. Moreover, the expression profile analysis of SlbHLH genes from 10 different tissues showed that 21 SlbHLH genes exhibited tissue-specific expression. Further, we identified that 11 SlbHLH genes were associated with fruit development and ripening (eight of them associated with young fruit development and three with fruit ripening). The evolutionary analysis revealed that 92% SlbHLH genes might be evolved from ancestor(s) originated from early land plant, and 8% from algae.

Conclusions

In this work, we systematically identified SlbHLHs by analyzing the tomato genome sequence using a set of bioinformatics approaches, and characterized their chromosomal distribution, gene structures, duplication, phylogenetic relationship and expression profiles, as well predicted their possible biological functions via comparative analysis with bHLHs of Arabidopsis. The results and information provide a good basis for further investigation of the biological functions and evolution of tomato bHLH genes.

【 授权许可】

   
2015 Sun et al.; licensee Biomed Central.

【 图 表 】

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【 参考文献 】

• [1]Ledent V, Vervoort M: The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res 2001, 11:754-70.
• [2]Toledo-Ortiz G, Huq E, Quail PH: The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 2003, 15:1749-70.
• [3]Sonnenfeld MJ, Delvecchio C, Sun X: Analysis of the transcriptional activation domain of the Drosophila tango bHLH-PAS transcription factor. Dev Genes Evol 2005, 215:221-9.
• [4]Murre C, McCaw PS, Baltimore D: A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 1989, 56:777-83.
• [5]Atchley WR, Terhalle W, Dress A: Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J Mol Evol 1999, 48:501-16.
• [6]Massari ME, Murre C: Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 2000, 20:429-40.
• [7]Ferre-D’Amare AR, Pognonec P, Roeder RG, Burley SK: Structure and function of the b/HLH/Z domain of USF. EMBO J 1994, 13:180-9.
• [8]Atchley WR, Fitch WM: A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A 1997, 94:5172-6.
• [9]Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, et al.: Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 2007, 7(33):1-18.
• [10]Henriksson M, Luscher B: Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 1996, 68:109-82.
• [11]Facchini LM, Penn LZ: The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J 1998, 12:633-51.
• [12]Goding CR: Mitf from neural crest to melanoma: signal transduction and transcription in the melanocyte lineage. Genes Dev 2000, 14:1712-28.
• [13]Sun XH, Copeland NG, Jenkins NA, Baltimore D: Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 1991, 11:5603-11.
• [14]Fisher A, Caudy M: The function of hairy-related bHLH repressor proteins in cell fate decisions. Bioessays 1998, 20:298-306.
• [15]Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, et al.: Characterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 2000, 66:195-203.
• [16]Crozatier M, Valle D, Dubois L, Ibnsouda S, Vincent A: Collier, a novel regulator of Drosophila head development, is expressed in a single mitotic domain. Curr Biol 1996, 6:707-18.
• [17]Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC: The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 2003, 20:735-47.
• [18]Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, et al.: Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 2006, 141:1167-84.
• [19]Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martinez-Garcia JF, Bilbao-Castro JR, Robertson DL: Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 2010, 153:1398-412.
• [20]Klee HJ, Giovannoni JJ: Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 2011, 45:41-59.
• [21]Consortium TTG: The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485:635-41.
• [22]Shimizu T, Toumoto A, Ihara K, Shimizu M, Kyogoku Y, Ogawa N, et al.: Crystal structure of PHO4 bHLH domain-DNA complex: flanking base recognition. EMBO J 1997, 16:4689-97.
• [23]Fujisawa M, Nakano T, Shima Y, Ito Y: A Large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 2013, 25:371-86.
• [24]Yamagata H, Yonesu K, Hirata A, Aizono Y: TGTCACA motif is a novel cis-regulatory enhancer element involved in fruit-specific expression of the cucumisin gene. J Biol Chem 2002, 277:11582-90.
• [25]Yuan YX, Zhang J, Wang DW, Ling HQ: AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 2005, 15:613-21.
• [26]Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, et al.: FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 2008, 18:385-97.
• [27]Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN: The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 2010, 22:2219-36.
• [28]Wang N, Cui Y, Liu Y, Fan H, Du J, Huang Z, et al.: Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 2013, 6:503-13.
• [29]Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M: The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci U S A 2002, 99:13938-43.
• [30]Pires ND, Dolan L: Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Lond B Biol Sci 2012, 367:508-18.
• [31]Pires N, Dolan L: Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 2010, 27:862-74.
• [32]Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Loffelhardt W, et al.: Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 2005, 15:1325-30.
• [33]Steemans P, Herisse AL, Melvin J, Miller MA, Paris F, Verniers J, et al.: Origin and radiation of the earliest vascular land plants. Science 2009, 324:353.
• [34]Rizzon C, Ponger L, Gaut BS: Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2006, 2:989-1000.
• [35]Schat H, Vooijs R, Kuiper E: Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 1996, 50:1888-95.