Abstract
BTB (broad-complex, tramtrack, and bric-a-brac) family proteins are characterized by the presence of a protein–protein interaction BTB domain. BTB proteins have diverse functions, including transcriptional regulation, protein degradation, chromatin remodeling, and cytoskeletal regulation. However, little is known about this gene family in tomato (Solanum lycopersicum), the most important model plant for crop species. In this study, 38 BTB genes were identified based on tomato whole-genome sequence. Phylogenetic analysis of BTB proteins in tomato revealed that SlBTB proteins could be divided into at least 4 subfamilies. The SlBTB proteins contains 1–3 BTB domains, and several other types of functional domains, including KCTD (Potassium channel tetramerization domain-containing), the MATH (meprin and TRAF homology), ANK (Ankyrin repeats), NPR1 (nonexpressor of pathogenesis-related proteins1), NPH3 (Nonphototropic Hypocotyl 3), TAZ zinc finger, C-terminal Kelch, Skp1 and Arm (Armadillo/beta-catenin-like repeat) domains are also found in some tomato BTB proteins. Moreover, their expression patterns in tissues/stages, in response to different abiotic stress treatments and hormones were also investigated. This study provides the first comprehensive analysis of BTB gene family in the tomato genome. The data will undoubtedly be useful for better understanding the potential functions of BTB genes, and their possible roles in mediating hormone cross-talk and abiotic stress in tomato as well as in some other relative species.
Similar content being viewed by others
References
Ahmad KF, Melnick A, Lax S, Bouchard D, Liu J, Kiang CL, Mayer S, Takahashi S, Licht JD, Prive GG (2003) Mechanism of SMRT corepressor recruitment by the BCL6 BTB domain. Mol Cell 12:1551–1564
Araus V, Vidal EA, Puelma T, Alamos S, Mieulet D, Guiderdoni E, Gutierrez RA (2016) Members of BTB gene family of scaffold proteins suppress nitrate uptake and nitrogen use efficiency. Plant Physiol 171:1523–1532
Bardwell VJ, Treisman R (1994) The POZ domain: a conserved protein–protein interaction motif. Genes Dev 8:1664–1677
Bolger A, Scossa F, Bolger ME, Lanz C, Maumus F, Tohge T, Quesneville H, Alseekh S, Sørensen I, Lichtenstein G (2014) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat Genet 46:1034–1038
Bonchuk A, Denisov S, Georgiev P, Maksimenko O (2011) Drosophila BTB/POZ domains of “ttk group” can form multimers and selectively interact with each other. J Mol Biol 412:423–436
Bostan H, Chiusano ML (2015) NexGenEx-Tom: a gene expression platform to investigate the functionalities of the tomato genome. BMC Plant Biol 15:48
Boyle P, Le Su E, Rochon A, Shearer HL, Murmu J, Chu JY, Fobert PR, Despres C (2009) The BTB/POZ domain of the Arabidopsis disease resistance protein NPR1 interacts with the repression domain of TGA2 to negate its function. Plant Cell 21:3700–3713
Caldwell KS, Michelmore RW (2009) Arabidopsis thaliana genes encoding defense signaling and recognition proteins exhibit contrasting evolutionary dynamics. Genetics 181:671–684
Canning P, Cooper CD, Krojer T, Murray JW, Pike AC, Chaikuad A, Keates T, Thangaratnarajah C, Hojzan V, Marsden BD (2013) Structural basis for Cul3 protein assembly with the BTB-Kelch family of E3 ubiquitin ligases. J Biol Chem 288:7803–7814
Chaharbakhshi E, Jemc JC (2016) Broad-complex, tramtrack, and bric-a-brac (BTB) proteins: critical regulators of development. Genesis 10:505–518
Cheng D, Qian W, Meng M, Wang Y, Peng J, Xia Q (2014) Identification and expression profiling of the BTB domain-containing protein gene family in the silkworm, bombyx mori. Int J Genom 2014:865065
Chevrier S, Emslie D, Shi W, Kratina T, Wellard C, Karnowski A, Erikci E, Smyth GK, Chowdhury K, Tarlinton D, Corcoran LM (2014) The BTB-ZF transcription factor Zbtb20 is driven by Irf4 to promote plasma cell differentiation and longevity. J Exp Med 211:827–840
Cho JH, Kim MJ, Kim KJ, Kim JR (2012) POZ/BTB and AT-hook-containing zinc finger protein 1 (PATZ1) inhibits endothelial cell senescence through a p53 dependent pathway. Cell Death Differ 19:703–712
Coates JC (2003) Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol 13:463–471
Consortium TG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Friedman JS, Ray JW, Waseem N, Johnson K, Brooks MJ, Hugosson T, Breuer D, Branham KE, Krauth DS, Bowne SJ (2009) Mutations in a BTB-Kelch protein, KLHL7, cause autosomal-dominant retinitis pigmentosa. Am J Hum Genet 84:792–800
Furukawa M, He YJ, Borchers C, Xiong Y (2003) Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat Cell Biol 5:1001–1007
Geyer R, Wee S, Anderson S, Yates J, Wolf DA (2003) BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol Cell 12:783–790
Gong P, Zhang J, Li H, Yang C, Zhang C, Zhang X, Khurram Z, Zhang Y, Wang T, Fei Z, Ye Z (2010) Transcriptional profiles of drought-responsive genes in modulating transcription signal transduction, and biochemical pathways in tomato. J Exp Bot 61:3563–3575
Guo A, Zhu Q, Chen X, Luo J (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026
Hatzfeld M (1999) The armadillo family of structural proteins. Int Rev Cytol 186:179–224
Hou X, Xie K, Yao J, Qi Z, Xiong L (2009) A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA 106:6410–6415
Ito H, Sato K, Yamamoto D (2013) Sex-switching of the Drosophila brain by two antagonistic chromatin factors. Fly (Austin) 7:87–91
Juranic M, Srilunchang KO, Krohn NG, Leljak-Levanic D, Sprunck S, Dresselhaus T (2012) Germline-specific MATH-BTB substrate adaptor MAB1 regulates spindle length and nuclei identity in maize. Plant Cell 24:4974–4991
Kim SY, Choi H-i (2006) Nucleic acid molecule encoding an armadillo repeat protein, aria and a method utilizing aria to generate salt tolerant plants. US Patent No. 7049482
Kim H, Kim SH, Seo DH, Chung S, Kim SW, Lee JS, Kim WT, Lee JH (2016) Aba-hypersensitive BTB/POZ protein 1 functions as a negative regulator in ABA-mediated inhibition of germination in Arabidopsis. Plant Mol Biol 90:303–315
Ko JH, Son W, Bae GY, Kang JH, Oh W, Yoo OJ (2006) A new hepatocytic isoform of PLZF lacking the BTB domain interacts with ATP7B, the Wilson disease protein, and positively regulates ERK signal transduction. J Cell Biochem 99:719–734
Korutla L, Wang PJ, Mackler SA (2005) The POZ/BTB protein NAC1 interacts with two different histone deacetylases in neuronal-like cultures. J Neurochem 94:786–793
Krylov DM, Wolf YI, Rogozin IB, Koonin EV (2003) Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res 13:2229–2235
Kushwaha HR, Joshi R, Pareek A, Singla-Pareek SL (2016) MATH-domain family shows response toward abiotic stress in Arabidopsis and rice. Front Plant Sci 7:923
Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21:1116–1128
Lim JH (2014) Zinc finger and BTB domain-containing protein 3 is essential for the growth of cancer cells. BMB Rep 47:405–410
Liu Q, Yao F, Wang M, Zhou B, Cheng H, Wang W, Jin L, Lin Q, Wang JC (2011) Novel human BTB/POZ domain-containing zinc finger protein ZBTB1 inhibits transcriptional activities of CRE. Mol Cell Biochem 357:405–414
Liu Z, Xiang Y, Sun G (2013) The KCTD family of proteins: structure, function, disease relevance. Cell Biosci 3:45
Mandadi KK, Misra A, Ren S, McKnight TD (2009) BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis. Plant Physiol 150:1930–1939
Masuda HP, Cabral LM, De Veylder L, Tanurdzic M, de Almeida Engler J, Geelen D, Inzé D, Martienssen RA, Ferreira PC, Hemerly AS (2008) ABAP1 is a novel plant Armadillo BTB protein involved in DNA replication and transcription. EMBO J 27:2746–2756
Melnick A, Ahmad KF, Arai S, Polinger A, Ball H, Borden KL, Carlile GW, Prive GG, Licht JD (2000) In-depth mutational analysis of the promyelocytic leukemia zinc finger BTB/POZ domain reveals motifs and residues required for biological and transcriptional functions. Mol Cell Biol 20:6550–6567
Michaely P, Bennett V (1992) The ANK repeat: a ubiquitous motif involved in macromolecular recognition. Trends Cell Biol 2:127–129
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19
Mosavi LK, Minor DL Jr, Peng ZY (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA 99:16029–16034
Motchoulski A, Liscum E (1999) Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286:961–964
Mukhtar MS, Nishimura MT, Dangl J (2009) NPR1 in plant defense: it’s not over’til it’s turned over. Cell 137:804–806
Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789–791
Perez-Torrado R, Yamada D, Defossez PA (2006) Born to bind: the BTB protein–protein interaction domain. Bioessays 28:1194–1202
Pintard L, Willis JH, Willems A, Johnson JL, Srayko M, Kurz T, Glaser S, Mains PE, Tyers M, Bowerman B, Peter M (2003) The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425:311–316
Qi J, Zhang X, Zhang HK, Yang HM, Zhou YB, Han ZG (2006) ZBTB34, a novel human BTB/POZ zinc finger protein, is a potential transcriptional repressor. Mol Cell Biochem 290:159–167
Riggleman B, Wieschaus E, Schedl P (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3:96–113
Robert HS, Quint A, Brand D, Vivian-Smith A, Offringa R (2009) BTB and TAZ domain scaffold proteins perform a crucial function in Arabidopsis development. Plant J 58:109–121
Roberts D, Pedmale UV, Morrow J, Sachdev S, Lechner E, Tang X, Zheng N, Hannink M, Genschik P, Liscum E (2011) Modulation of phototropic responsiveness in Arabidopsis through ubiquitination of phototropin 1 by the CUL3-ring E3 ubiquitin ligase CRL3NPH3. The Plant Cell 23:3627–3640
Robinson DN, Cooley L (1997) Drosophila kelch is an oligomeric ring canal actin organizer. J Cell Biol 138:799–810
Siggs OM, Li X, Xia Y, Beutler B (2012) ZBTB1 is a determinant of lymphoid development. J Exp Med 209:19–27
Skoblov M, Marakhonov A, Marakasova E, Guskova A, Chandhoke V, Birerdinc A, Baranova A (2013) Protein partners of KCTD proteins provide insights about their functional roles in cell differentiation and vertebrate development. Bioessays 35:586–596
Smaldone G, Pirone L, Pedone E, Marlovits T, Vitagliano L, Ciccarelli L (2016) The BTB domains of the potassium channel tetramerization domain proteins prevalently assume pentameric states. FEBS Lett 590:1663–1671
Stebbins CE, Kaelin WG Jr, Pavletich NP (1999) Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function. Science 284:455–461
Stogios PJ, Prive GG (2004) The back domain in BTB-kelch proteins. Trends Biochem Sci 29:634–637
Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Prive GG (2005) Sequence and structural analysis of BTB domain proteins. Genome Biol 6:R82
Sunnerhagen M, Pursglove S, Fladvad M (2002) The new MATH: homology suggests shared binding surfaces in meprin tetramers and TRAF trimers. FEBS Lett 530:1–3
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
Tomato Genome C (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Weber H, Hellmann H (2009) Arabidopsis thaliana BTB/POZ-MATH proteins interact with members of the ERF/AP2 transcription factor family. FEBS J 276:6624–6635
Weber H, Bernhardt A, Dieterle M, Hano P, Mutlu A, Estelle M, Genschik P, Hellmann H (2005) Arabidopsis AtCUL3a and AtCUL3b form complexes with members of the BTB/POZ-MATH protein family. Plant Physiol 137:83–93
Weyers JJ, Milutinovich AB, Takeda Y, Jemc JC, Van Doren M (2011) A genetic screen for mutations affecting gonad formation in Drosophila reveals a role for the slit/robo pathway. Dev Biol 353:217–228
Wilkins A, Ping Q, Carpenter CL (2004) RhoBTB2 is a substrate of the mammalian Cul3 ubiquitin ligase complex. Genes Dev 18:856–861
Withers J, Dong X (2016) Posttranslational modifications of NPR1: A single protein playing multiple roles in plant immunity and physiology. PLoS Pathog 12:e1005707
Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M, Elledge SJ, Harper JW (2003) BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316–321
Xu C, Park SJ, Van Eck J, Lippman ZB (2016) Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes Dev 30:2048–2061
Yuan X, Zhang S, Qing X, Sun M, Liu S, Su H, Shu H, Li X (2013) Superfamily of ankyrin repeat proteins in tomato. Gene 523:126–136
Zhuang M, Calabrese MF, Liu J, Waddell MB, Nourse A, Hammel M, Miller DJ, Walden H, Duda DM, Seyedin SN (2009) Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases. Mol Cell 36:39–50
Zollman S, Godt D, Prive GG, Couderc JL, Laski FA (1994) The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci USA 91:10717–10721
Acknowledgements
This work was supported by grants from the Basic and Frontier Research Project of Chongqing (No. cstc2015jcyjA80030), The National Natural Science Foundation of China (Nos. 31301779 and 31401884), Natural Science Foundation of Youth in Jiangsu Province (No. BK20140739).
Author information
Authors and Affiliations
Contributions
The work presented here was carried out in collaboration between all authors. JL and XZ conceived the study; XS and WY performed the experiments, JL collected and analyzed the data; CS, YP and YW provided reagents and tools; JL written the manuscript; all authors read and approved of the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest. Jinhua Li declares that he has no conflict of interest. Xiaoxing Su declares that she has no conflict of interest. Yinlei Wang declares that he has no conflict of interest. Wei Yang declares that he has no conflict of interest. Yu Pan declares that she has no conflict of interest. Chenggang Su declares that he has no conflict of interest. Xingguo Zhang declares that he has no conflict of interest.
Research involving human and animal participants
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
13258_2017_604_MOESM3_ESM.xlsx
Table S2 The differences about the cis-elements in the promoter sequence of BTB genes between S. pennellii and M82 (XLSX 194 KB)
Rights and permissions
About this article
Cite this article
Li, J., Su, X., Wang, Y. et al. Genome-wide identification and expression analysis of the BTB domain-containing protein gene family in tomato. Genes Genom 40, 1–15 (2018). https://doi.org/10.1007/s13258-017-0604-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-017-0604-x