Abstract
BES1/BZR1 transcription factors regulate the expression of brassinosteroid-responsive genes and play vital roles in plant growth and response to environmental stimuli. Their regulation mechanism has been well elucidated in genetic model plants. The complexity of the maize genome might lead to evolutional and functional diversification among the members of the ZmBES1/BZR1 gene family. In the present study, eleven members of the ZmBES1/BZR1 gene family were identified by genome-wide analysis, and ten of their open reading frames were successfully amplified. Bioinformatics analysis showed that these genes unevenly distributed on seven of the ten maize chromosomes, with three pairs of segmental duplication genes, and their encoding proteins shared similar motif composition and conserved domains. The expression of the ZmBES1/BZR1 genes displayed much differential in different organs and developmental stages, as well as in response to abscisic acid and light signal. Subcellular localization confirmed that most of them localized in nucleus. More attention should be paid to ZmBES1/BZR1-4 and -5, which were clustered into a distinguished phylogenetic clade, and ZmBES1/BZR1-2 and -7, which localized in chloroplast. The results indicated their similar but not identical functions in brassinosteroid-mediated signaling pathway and would be helpful in further functional study of the ZmBES1/BZR1s in maize.
Similar content being viewed by others
References
Anne P, Azzopardi M, Gissot L, Beaubiat S, Hematy K, Palauqui JC (2015) OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr Biol 25(19):2584–2590
Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104:13839–13844
Bai XF, Huang Y, Hu Y, Liu HY, Zhang B, Smaczniak C, Hu G, Han ZM, Xing YZ (2017) Duplication of an upstream silencer of FZP increases grain yield in rice. Nat Plants 3(11):885–893
Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signalling. New Phytol 206:522–540
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351
Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 Transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29(6):1425–1439
Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23(4):1219–1230
Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868
Feng Y, Yin Y, Fei S (2015) Down-regulation of BdBRI1, a putative brassinosteroid receptor gene produces a dwarf phenotype with enhanced drought tolerance in Brachypodium distachyon. Plant Sci 234:163–173
Fu J, Liu Q, Wang C, Liang J, Liu L, Wang Q (2018) ZmWRKY79 positively regulates maize phytoalexin biosynthetic gene expression and is involved in stress response. J Exp Bot 69(3):497–510
Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279
Hao J, Yin Y, Fei S (2013) Brassinosteroid signaling network: implications on yield and stress tolerance. Plant Cell Rep 32:1017–1030
He JX, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307(5715):1634–1638
Hu YF, Li YP, Zhang J, Liu H, Tian M, Huang Y (2012) Binding of ABI4 to a CACCG motif mediates the ABA-induced expression of the ZmSSI gene in maize (Zea mays L.) endosperm. J Exp Bot 63(16):5979–5989
Jiang J, Zhang C, Wang X (2015) A recently evolved isoform of the transcription factor BES1 promotes brassinosteroid signaling and development in Arabidopsis thaliana. Plant Cell 27(2):361–374
Kang S, Yang F, Li L, Chen H, Chen S, Zhang J (2015) The Arabidopsis transcription factor BES1 is a direct substrate of MPK6 and regulates immunity. Plant Physiol 167(3):1076–1086
Kir G, Ye H, Nelissen H, Neelakandan AK, Kusnandar AS, Luo A, Inze D, Sylvester AW, Yin Y, Becraft PW (2015) RNA interference knockdown of brassinosteroid insensitive1 in maize reveals novel functions for brassinosteroid signaling in controlling plant architecture. Plant Physiol 169(1):826–839
Kondrashov F, Rogozin I, Wolf Y, Koonin E (2002) Selection in the evolution of gene duplications. Genome Biol 3(2):RESEARCH0008
Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J, Li D (2013) Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genom 14:433
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645
Lee HS, Kim Y, Pham G, Kim JW, Song JH, Lee Y, Hwang YS, Roux SJ, Kim SH (2015) Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation. J Exp Bot 66(15):4835–4849
Lescot M, Dehais P, Moreau Y, De Moor B, Rouze P, Rombauts S (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(1):325–327
Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189
Li L, Yu X, Thompson A, Guo M, Yoshida S, Asami T, Chory J, Yin Y (2009) Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J 58(2):275–286
Li L, Ye H, Guo H, Yin Y (2010) Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 107:3918–3923
Li QF, Huang LC, Wei K, Yu JW, Zhang CQ, Liu QQ (2017a) Light involved regulation of BZR1 stability and phosphorylation status to coordinate plant growth in Arabidopsis. Biosci Rep 37(2):BSR20170069
Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S (2017b) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10(4):545–559
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408
Long M, Deutsch M (1999) Association of intron phases with conservation at splice site sequences and evolution of spliceosomal introns. Mol Biol Evol 16(11):1528–1534
Lu X, Xiong Q, Cheng T, Li QT, Liu XL, Bi YD, Li W, Zhang WK, Ma B, Lai YC, Du WG, Man WQ, Chen SY, Zhang JS (2017) A PP2C-1 allele underlying a quantitative trait locus enhances soybean 100-seed weight. Mol Plant 10(5):670–684
Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Li C, Ding Z (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14(1):e1007144
Ma W, Zhao T, Li J, Liu B, Fang L, Hu Y, Zhang T (2016) Identification and characterization of the GhHsp20 gene family in Gossypium hirsutum. Sci Rep 6:32517
Martins S, Montiel-Jorda A, Cayrel A, Huguet S, Roux CP, Ljung K, Vert G (2017) Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat Commun 8(1):309
Miyaji T, Yamagami A, Kume N, Sakuta M, Osada H, Asami T, Arimoto Y, Nakano T (2014) Brassinosteroid-related transcription factor BIL1/BZR1 increases plant resistance to insect feeding. Biosci Biotechnol Biochem 78(6):960–968
Nolan T, Chen J, Yin Y (2017a) Cross-talk of brassinosteroid signaling in controlling growth and stress responses. Biochem J 474(16):2641–2661
Nolan TM, Brennan B, Yang M, Chen J, Zhang M, Li Z, Wang X, Bassham DC, Walley J, Yin Y (2017b) Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell 41:33–46
Oh E, Zhu JY, Wang ZY (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809
Ruvinsky A, Eskesen ST, Eskesen FN, Hurst LD (2005) Can codon usage bias explain intron phase distributions and exon symmetry? J Mol Evol 60(1):99–104
Ryu H, Cho H, Kim K, Hwang I (2010a) Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol Cell 29(3):283–290
Ryu H, Kim K, Cho H, Hwang I (2010b) Predominant actions of cytosolic BSU1 and nuclear BIN2 regulate subcellular localization of BES1 in brassinosteroid signaling. Mol Cell 29(3):291–296
Ryu H, Cho H, Bae W, Hwang I (2014) Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nat Commun 5:4138
Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Kang JG, Nou IS (2015) Molecular characterization of BZR transcription factor family and abiotic stress induced expression profiling in Brassica rapa. Plant Physiol Biochem 92:92–104
Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P (2016) Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci Rep 6:28298
Saini S, Sharma I, Pati PK (2015) Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Front Plant Sci 6:950
Salazar-Henao JE, Lehner R, Betegon-Putze I, Vilarrasa-Blasi J, Cano-Delgado AI (2016) BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of the Arabidopsis primary root. J Exp Bot 17:4951–4961
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66(4):553–563
Sharma I, Bhardwaj R, Pati PK (2015) Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. J Plant Growth Regul 34:509–518
Singh AP, Fridman Y, Friedlander-Shani L, Tarkowska D, Strnad M, Savaldi-oldstein S (2014) Activity of the brassinosteroid transcription factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 blocks developmental reprogramming in response to low phosphate availability. Plant Physiol 166(2):678–688
Song XJ (2017) Crop seed size: BR matters. Mol Plant 10(5):668–669
Stelpflug SC, Sekhon RS, Vaillancourt B, Hirsch CN, Buell CR, de Leon N, Kaeppler SM (2016) An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development. Plant Genome. https://doi.org/10.3835/plantgenome2015.04.0025
Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19(5):765–777
Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, Gendron JM, Jonassen EM, Lillo C, DeLong A, Burlingame AL, Sun Y, Wang ZY (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13:124–131
Tang Y, Liu H, Guo S, Wang B, Li Z, Chong K, Xu Y (2018) OsmiR396d miRNA affects gibberellin and brassinosteroid signaling to regulate plant architecture. Plant Physiol 176(1):946–959
Tong H, Chu C (2016) Reply: brassinosteroid regulates gibberellin synthesis to promote cell elongation in rice: critical comments on Ross and Quittenden’s letter. Plant Cell 28(4):833–835
Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26(11):4376–4393
Unterholzner SJ, Rozhon W, Papacek M, Ciomas J, Lange T, Kugler KG, Mayer KF, Sieberer T, Poppenberger B (2015) Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27(8):2261–2272
Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signaling. Nature 441(7089):96–100
Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, Chory J (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2(4):505–513
Wu P, Song XM, Wang Z, Duan WK, Hu R, Wang WL, Li Y, Hou XL (2016) Genome-wide analysis of the BES1 transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis). Plant Growth Regul. https://doi.org/10.1007/s10725-016-0166-y
Yang X, Tuskan GA, Cheng MZ (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830
Yang X, Bai Y, Shang J, Xin R, Tang W (2016) The antagonistic regulation of abscisic acid-inhibited root growth by brassinosteroids is partially mediated via direct suppression of ABSCISIC ACID INSENSITIVE 5 expression by BRASSINAZOLE RESISTANT 1. Plant Cell Environ 39(9):1994–2003
Yang M, Li C, Cai Z, Hu Y, Nolan T, Yu F, Yin Y, Xie Q, Tang G, Wang X (2017) SINAT E3 ligases control the light-mediated stability of the brassinosteroid-activated transcription factor BES1 in Arabidopsis. Dev Cell 41:47–58
Ye H, Li L, Yin Y (2011) Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J Int Plant Biol 53:455–468
Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin HY, Li L, Wang Y, Tong H, Zhang M, Chu C, Li Z, Aluru M, Aluru S, Schnable PS, Yin Y (2017) RD26 mediates crosstalk between drought and brassinosteroid signaling pathways. Nat Commun 8:14573
Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid regulated gene expression in Arabidopsis. Cell 120:249–259
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572
Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65(4):634–646
Yu HQ, Muhammad HBK, Lu FZ, Sun FA, Qu JT, Liu BL, Li WC, Fu FL (2018) Isolation and identification of a vegetative organ-specific promoter from maize. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-018-0546-z
Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K, Goldstein S, Pape L, Mehan MR, Churas C, Pasternak S, Forrest DK, Wise R, Ware D, Wing RA, Waterman MS, Livny M, Schwartz DC (2009) A single molecule scaffold for the maize genome. PLoS Genet 5:e1000711
Zhou Y, Xia X, Yu G, Wang J, Wu J, Wang M, Yang Y, Shi K, Yu Y, Chen Z, Gan J, Yu J (2015) Brassinosteroids play a critical role in the regulation of pesticide metabolism in crop plants. Sci Rep 5:9018
Acknowledgements
This work was supported by the Applied Basic Project of Science and Technology Department of Sichuan Province (2018JY0470), the National Key Science and Technology Special Project (2016ZX08003-004), and the Education Scientific Fund for Young Teacher of the Fujian Education Department (JA15470). The authors thank the technical support from the Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region.
Author information
Authors and Affiliations
Contributions
HQY, WQF, FAS and YYZ performed the experiment and drafted the manuscript; JTQ analyzed data; BLL, FZL and LY participated in the experiments; HQ Yu provided technical support; FLF and WCL provided ideas, designed the research, and edited the manuscript; all authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declared that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yu, H., Feng, W., Sun, F. et al. Cloning and characterization of BES1/BZR1 transcription factor genes in maize. Plant Growth Regul 86, 235–249 (2018). https://doi.org/10.1007/s10725-018-0424-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0424-2