Global evolution and expression analysis of BTB-containing ankyrin repeat genes in plants

Authors

  • Peiyan Guan State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Lixue Sun State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Rui Yang State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Huiyang Gao State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Pu Liu State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Chengchao Zheng State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018
  • Shizhong Zhang State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018

Keywords:

ANK, BTB, bioinformatics, expression pattern, abiotic stress, evolution

Abstract

The ankyrin (ANK) repeat domain and bric-a-brac, tram-track, broad complex (BTB) domains, which are the most common protein motifs in eukaryotic proteins, regulate diverse developmental and biological processes in plants. In this study, 230 BTB-containing ANK (ANK-BTB) homologs were identified and categorized into two groups (class I and class II) in plants. Phylogenetic and comparative analysis found that ANK-BTB genes originated in bryophytes and ferns and their number expanded by segment duplications. All of the selected ANK-BTB genes were expressed in two or more tested tissues, indicating that these genes are involved in various aspects of developmental processes in Arabidopsis. Furthermore, the ANK-BTB genes responded to abiotic stresses (NaCl, mannitol, heat and cold) and ABA treatments. To our knowledge, this study is the first report of a genome-wide analysis of ANK-BTB genes. This study also provides valuable information to understand the classification, evolution and putative functions of the gene family.

https://doi.org/10.2298/ABS170306042G

Received: March 6, 2017; Revised: June 14, 2017; Accepted: September 26, 2017; Published online: October 30, 2017

How to cite this article: Guan P, Sun L, Yang R, Gao H, Liu P, Zheng C, Zhang S. Global evolution and expression analysis of BTB-containing ankyrin repeat genes in plants. Arch Biol Sci. 2018;70(2):249-58.

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Author Biography

Shizhong Zhang, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong Province, 271018


References

Sedgwick SG, Smerdon SJ. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci. 1999;24(8):311-16.

Mosavi LK, Minor P DL Jr, Eng ZY. Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci U S A. 2002;99(25):16029-34.

Breeden L, Nasmyth K. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell. 1987;48(3):389-97.

Rohde K, Bork P. A fast, sensitive pattern-matching approach for protein sequences. Comput Appl Biosci. 1993;9(2):183-9.

Desrosiers DC, Peng ZY. A binding free energy hot spot in the ankyrin repeat protein GABPbeta mediated protein-protein interaction. J Mol Biol. 2005;354(2):375-84.

Li J, Mahajan A, Tsai MD. Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry. 2006;45(51):15168-78.

Zhang H, Scheirer DC, Fowle WH, Goodman HM. Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Arabidopsis. Plant Cell. 1992;4(12):1575-88.

Albert S, Despres B, Guilleminot J, Bechtold N, Pelletier G, Delseny M, Devic M. The EMB 506 gene encodes a novel ankyrin repeat containing protein that is essential for the normal development of Arabidopsis embryos. Plant J. 1999;17(2):169-79.

Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997;88(1):57-63.

Lu H, Rate DN, Song JT, Greenberg JT. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell. 2003;15(10):2408-20.

Sakamoto H, Matsuda O, Iba K. ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. Plant J. 2008;56(3):411-22.

Lyzenga WJ, Booth JK, Stone SL. The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. Plant J. 2012;71(1):23-34.

Zhang X, Li D, Zhang H, Wang X, Zheng Z, Song F. Molecular characterization of rice OsBIANK1, encoding a plasma membrane-anchored ankyrin repeat protein, and its inducible expression in defense responses. Mol Biol Rep. 2010;37(2):653-60.

Li X, Peng H, Schultz DC, Lopez-Guisa JM, Rauscher FJ 3rd, Marmorstein R. Structure-function studies of the BTB/POZ transcriptional repression domain from the promyelocytic leukemia zinc finger oncoprotein. Cancer Res. 1999;59(20):5275-82.

Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Prive GG. Sequence and structural analysis of BTB domain proteins. Genome Biol. 2005;6(10):R82.

Gingerich DJ, Hanada K, Shiu SH, Vierstra RD. Large-scale, lineage-specific expansion of a bric-a-brac/tramtrack/broad complex ubiquitin-ligase gene family in rice. Plant Cell. 2007;19(8):2329-48.

Bardwell VJ, Treisman R. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994;8(14):1664-77.

Alliel PM, Seddiqi N, Goudou D, Cifuentes-Diaz C, Romero N, Velasco E, Rieger F, Perin JP. Myoneurin, a novel member of the BTB/POZ-zinc finger family highly expressed in human muscle. Biochem Biophys Res Commun. 2000;273(1):385-91.

Collins T, Stone JR, Williams AJ. All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol Cell Biol. 2001;21(11):3609-15.

Prasad ME, Schofield A, Lyzenga W, Liu H, Stone SL. Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol. 2010;153(4):1587-96.

Weber H, Hellmann H. Arabidopsis thaliana BTB/ POZ-MATH proteins interact with members of the ERF/AP2 transcription factor family. FEBS J. 2009;276(22):6624-35.

Chevrier S, Corcoran LM. BTB-ZF transcription factors, a growing family of regulators of early and late B-cell development. Immunol Cell Biol. 2014;92(6):481-8.

Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD. The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 2009;57(2):332-45.

Mandadi KK, Misra A, Ren S, McKnight TD. BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis. Plant Physiol. 2009;150(4):1930-9.

Ha CM, Jun JH, Nam HG, Fletcher JC. BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol. 2004;45(10):1361-70.

Cai X, Zhang Y. Molecular evolution of the ankyrin gene family. Mol Biol Evol. 2006;23(3):550-8.

Huang J, Zhao X, Yu H, Ouyang Y, Wang L, Zhang Q. The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling. Plant Mol Biol. 2009;71(3):207-26.

Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:D1178-86.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-10.

Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. The Pfam protein families database. Nucleic Acids Res. 2012;40:D290-301.

Letunic I, Doerks T, Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 2012;40:D302-5.

Wu X, Song C, Wang B, Cheng J. Hidden Markov model used in protein sequence analysis. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi. 2002;19(3):455-8.

Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. Multiple sequence alignment with Clustal X. Trends Biochem Sci. 1998;23(10):403-5.

Poole RL. The TAIR database. Methods Mol Biol. 2007;406:179-212.

Guo AY, Zhu QH, Chen X, Luo JC. [GSDS: a gene structure display server]. Yi Chuan. 2007;29(8):1023-6. Chinese.

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792-7.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731-9.

Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11):1451-2.

Rozas J. DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol. 2009;537:337-50.

Liu Q, Yao F, Wang M, Zhou B, Cheng H, Wang W, Jin L, Lin Q, Wang JC. Novel human BTB/POZ domain-containing zinc finger protein ZBTB1 inhibits transcriptional activities of CRE. Mol Cell Biochem. 2011;357(1-2):405-14.

Cai Y, Li J, Yang S, Li P, Zhang X, Liu H. CIBZ, a novel BTB domain-containing protein, is involved in mouse spinal cord injury via mitochondrial pathway independent of p53 gene. PLoS One. 2012;7(3):e33156.

Nielsen JV, Nielsen FH, Ismail R, Noraberg J, Jensen NA. Hippocampus-like corticoneurogenesis induced by two isoforms of the BTB-zinc finger gene Zbtb20 in mice. Development. 2007;134(6):1133-40.

Warnatz HJ, Schmidt D, Manke T, Piccini I, Sultan M, Borodina T, Balzereit D, Wruck W, Soldatov A, Vingron M, Lehrach H, Yaspo ML. The BTB and CNC homology 1 (BACH1) target genes are involved in the oxidative stress response and in control of the cell cycle. J Biol Chem. 2011;286(26):23521-32.

Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol. 2004;24(19):8477-86.

Kun J, Szitter I, Kemény A, Perkecz A, Kereskai L, Pohóczky K, Vincze A, Gódi S, Szabó I, Szolcsányi J, Pintér E, Helyes Z. Upregulation of the transient receptor potential ankyrin 1 ion channel in the inflamed human and mouse colon and its protective roles. PLoS One. 2014;9(9):e108164.

Romero Z, Campo-Fernandez B, Wherley J, Kaufman ML, Urbinati F, Cooper AR, Hoban MD, Baldwin KM, Lumaquin D, Wang X, Senadheera S, Hollis RP, Kohn DB. The human ankyrin 1 promoter insulator sustains gene expression in a beta-globin lentiviral vector in hematopoietic stem cells. Mol Ther Methods Clin Dev. 2015;2:15012.

Yan J, Wang J, Zhang H: An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J. 2002;29(2):193-202.

Lu H, Liu Y, Greenberg JT. Structure-function analysis of the plasma membrane- localized Arabidopsis defense component ACD6. Plant J. 2005;44(5):798-809.

Hu H, Wang J, Shi C, Yuan C, Peng C, Yin J, Li W, He M, Ma B, Wang Y, Li S, Chen X. A receptor like kinase gene with expressional responsiveness on Xanthomonas oryzae pv. oryzae is essential for Xa21-mediated disease resistance. Rice (N Y). 2015;8(1):34.

Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li L, Benny U, Oard J, Ronald PC, Song WY. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell. 2006;18(12):3635-46.

Jiang Y, Chen X, Ding X, Wang Y, Chen Q, Song WY. The XA21 binding protein XB25 is required for maintaining XA21-mediated disease resistance. Plant J. 2013;73(5):814-23.

Seong ES, Choi D, Cho HS, Lim CK, Cho HJ, Wang MH. Characterization of a stress-responsive ankyrin repeat-containing zinc finger protein of Capsicum annuum (CaKR1). J Biochem Mol Biol. 2007;40(6):952-8.

Zhang H, Scheirer DC, Fowle WH, Goodman, HM. Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Arabidopsis. Plant Cell. 1992;4(12):1575-88.

Garcion C, Guilleminot J, Kroj T, Parcy F, Giraudat J, Devic M. AKRP and EMB506 are two ankyrin repeat proteins essential for plastid differentiation and plant development in Arabidopsis. Plant J. 2006;48(6):895-906.

Ha CM, Jun JH, Nam HG, Fletcher JC. BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol. 2004;45(10):1361-70.

Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development. 2003;130(1):161-72.

Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY. The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J. 2004; 40(6);996-1006.

Bae W, Lee YJ, Kim D, Lee J, Kim S, Sohn EJ, Hwang Inhwan. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol. 2008;10(2):220-7.

Sharma M, Pandey GK. Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci. 2015;6(e114):487-504.

Hirsch RE, Lewis BD, Spalding EP, Sussman MR. A role for the AKT1 potassium channel in plant nutrition. Science. 1998;280(5365):918-21.

Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD. Potassium uptake supporting plant growth in the absence of AKT1 channel activity: inhibition by ammonium and stimulation by sodium. J Gen Physiol. 1999;113(6):909-18.

Gierth M, Maser P, Schroeder JI. The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol. 2005;137(3):1105-14.

Rubio F, Nieves-Cordones M, Alemán F, Martínez V. Relative contribution of AtHAK5 and AtAKT1 to K+ uptake in the high-affinity range of concentrations. Physiol Plant. 2008;134(4):598-608.

Alemán F, Nieves-Cordones M, Martínez V, Rubio F. Root K+ acquisition in plants: the Arabidopsis thaliana model. Plant Cell Physiol. 2011;52(9):1603-12.

Nieves-Cordones M, Caballero F, Martínez V, Rubio F. Disruption of the Arabidopsis thaliana in ward-rectifier K+ channel AKT1 improves plant responses to water stress. Plant Cell Physiol. 2012;53(2):423-32.

Blanvillain R, Wei S, Wei P, Kim JH, Ow DW. Stress tolerance to stress escape in plants: role of the OXS2 zinc-finger transcription factor family. EMBO J. 2011;30(18):3812-22.

Roy A, Pahan K. Ankyrin repeat and BTB/POZ domain containing protein-2 inhibits the aggregation of alpha-synuclein: implications for Parkinson’s disease. FEBS Lett. 2013;587(21):3567-74.

Dai KS, Wei W, Liew CC. Molecular cloning and characterization of a novel human gene containing ankyrin repeat and double BTB/POZ domain. Biochem Biophys Res Commun. 2000;273(3):991-6.

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Published

2018-04-27

How to Cite

1.
Guan P, Sun L, Yang R, Gao H, Liu P, Zheng C, Zhang S. Global evolution and expression analysis of BTB-containing ankyrin repeat genes in plants. Arch Biol Sci [Internet]. 2018Apr.27 [cited 2024Apr.26];70(2):249-58. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/1532

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