Skip to main content
Log in

Genome-Wide Identification and Expression Characteristics of Cytokinin Response Factors in Soybean

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The cytokinin response factors (CRFs) take crucial part in mediating plant development and stress response processes. However, hardly any information is known about CRF genes in the main crop plant soybean at present. Here, we carried out genome-wide dissection of CRF family in soybean and identified 26 members, which locate on 18 chromosomes of soybean. Sequence information was first observed to gain insight into the soybean CRF genes. Then, the gene duplication, phylogenetic relationships, protein motifs, and gene structure were analyzed in depth to better understand the CRF family in soybean. Cis-regulatory elements analysis showed that these CRFs contain many hormone- and stress-related elements on promoter regions, indicating their potential involvement in response to these factors. In addition, through investigating the public transcriptome data, we studied the expression patterns of those CRFs in different tissues/organs and various environments. The results revealed that expression of soybean CRFs not only exhibited spatial-diversity, but also differs in response to cold, drought, and salt stress. Our research offers new insights into soybean CRFs as well as useful information for future functional analysis of this gene family.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Data used or analyzed during the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  • Amalraj A, Luang S, Kumar MY, Sornaraj P, Eini O, Kovalchuk N, Bazanova N, Li Y, Yang N, Eliby S, Langridge P, Hrmova M, Lopato S (2016) Change of function of the wheat stress-responsive transcriptional repressor TaRAP2.1L by repressor motif modification. Plant Biotechnol J 14(2):820–832

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43(W1):W39–W49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Zhao J, Song J, Jameson PE (2020b) Cytokinin dehydrogenase: a genetic target for yield improvement in wheat. Plant Biotechnol J 18(3):614–630

    Article  CAS  PubMed  Google Scholar 

  • Cutcliffe JW, Hellmann E, Heyl A, Rashotte AM (2011) CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J Exp Bot 62(14):4995–5002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duanmu H, Wang Y, Bai X, Cheng S, Deyholos MK, Wong GK, Li D, Zhu D, Li R, Yu Y (2015) Wild soybean roots depend on specific transcription factors and oxidation reduction related genesin response to alkaline stress. Funct Integr Genomics 15(6):651–660

    Article  CAS  PubMed  Google Scholar 

  • Feng K, Hou XL, Xing GM, Liu JX, Duan AQ, Xu ZS, Li MY, Zhuang J, Xiong AS (2020) Advances in AP2/ERF super-family transcription factors in plant. Crit Rev Biotechnol 40(6):750–776

    Article  CAS  PubMed  Google Scholar 

  • Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Rashotte AM (2014) Expression patterns and regulation of SlCRF3 and SlCRF5 in response to cytokinin and abiotic stresses in tomato (Solanum lycopersicum). J Plant Physiol 171(3–4):349–358

    Article  CAS  PubMed  Google Scholar 

  • Hallmark HT, Rashotte AM (2019) Review—cytokinin response factors: responding to more than cytokinin. Plant Sci 289:110251

    Article  CAS  PubMed  Google Scholar 

  • Ijaz U, Pervaiz T, Ahmed T, Seemab R, Shahid M, Muhammad N, Majid N, Farrukh A (2020) Plant cis-regulatory elements: methods of identification and applications. Asian J Agr Biol 8(2):207–222

    Article  Google Scholar 

  • Jeon J, Cho C, Lee MR, Van Binh N, Kim J (2016) Cytokinin Response Factor2 (CRF2) and CRF3 regulate lateral root development in response to cold stress in Arabidopsis. Plant Cell 28(8):1828–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang W, Yang L, He Y, Zhang H, Li W, Chen H, Ma D, Yin J (2019) Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum). PeerJ 7:e8062

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang WB, Zhang XJ, Song XW, Yang JF, Pang YZ (2020) Genome-wide identification and characterization of APETALA2/Ethylene-responsive element binding factor superfamily genes in soybean seed sevelopment. Front Plant Sci 11:566647

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Peng D, Bai LP, Ma H, Chen LJ, Zhao MH, Xu ZJ, Guo ZF (2013) Molecular switch for cold acclimation—anatomy of the cold-inducible promoter in plants. Biochemistry (mosc) 78(4):342–354

    Article  CAS  PubMed  Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis book. American Society

    Google Scholar 

  • Kim J (2016) Cytokinin response factors gating environmental signals and hormones. Trends Plant Sci 21(12):993–996

    Article  CAS  PubMed  Google Scholar 

  • Kong L, Zhao K, Gao Y, Miao L, Chen C, Deng H, Liu Z, Yu X (2018) Comparative analysis of cytokinin response factors in Brassica diploids and amphidiploids and insights into the evolution of Brassica species. BMC Genomics 19(1):728

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(9):1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Xing M, Yang W, Mu X, Wang X, Lu F, Wang Y, Zhang L (2019) Genome-wide identification of and functional insights into the late embryogenesis abundant (LEA) gene family in bread wheat (Triticum aestivum). Sci Rep 9(1):13375

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Z, Ricci WA, Schmitz RJ, Zhang X (2018) Identification of cis-regulatory elements by chromatin structure. Curr Opin Plant Biol 42:90–94

    Article  CAS  PubMed  Google Scholar 

  • Melton AE, Zwack PJ, Rashotte AM, Goertzen LR (2019) Identification and functional characterization of the Marshallia (Asteraceae) Clade III Cytokinin response factor (CRF). Plant Signal Behav 14(9):1633886

    Article  PubMed  Google Scholar 

  • Miao L, Yang SN, Zhang K, He JB, Wu CH, Ren YH, Gai JY, Li Y (2020) Natural variation and selection in GmSWEET39 affect soybean seed oil content. New Phytol 225(4):1651–1666

    Article  CAS  PubMed  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell RV, Willett CR, Goertzen LR, Rashotte AM (2019) Lineage specific conservation of cis-regulatory elements in Cytokinin response factors. Sci Rep 9(1):13387

    Article  PubMed  PubMed Central  Google Scholar 

  • Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3(11):827–837

    Article  CAS  PubMed  Google Scholar 

  • Qin L, Wang L, Guo Y, Li Y (2017) An ERF transcription factor from Tamarix hispida, ThCRF1, can adjust osmotic potential and reactive oxygen species scavenging capability to improve salt tolerance. Plant Sci 265:154–166

    Article  CAS  PubMed  Google Scholar 

  • Rashotte AM, Goertzen LR (2010) The CRF domain defines cytokinin response factor proteins in plants. BMC Plant Biol 10(1):74

    Article  PubMed  PubMed Central  Google Scholar 

  • Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103(29):11081–11085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Medrano R, Xoconostle-Cazares B, Ham BK, Li G, Lucas WJ (2011) Vascular expression in Arabidopsis is predicted by the frequency of CT/GA-rich repeats in gene promoters. Plant J 67(1):130–144

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Gupta S, Rashotte AM (2014) Characterization of two tomato AP2/ERF genes, SlCRF1 and SlCRF2 in hormone and stress responses. Plant Cell Rep 33(1):35–45

    Article  CAS  PubMed  Google Scholar 

  • Striberny B, Melton AE, Schwacke R, Krause K, Fischer K, Goertzen LR, Rashotte AM (2017) Cytokinin response factor 5 has transcriptional activity governed by its C-terminal domain. Plant Signal Behav 12(2):e1276684

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, Song GS, Guo WJ, Wang WX, Zhao HK, Gao TT, Lv QX, Yang X, Xu F, Dong YS, Pu L (2019) Dynamic changes in genome-wide histone3 lysine27 trimethylation and gene expression of soybean roots in response to salt stress. Front Plant Sci 10:1031

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: mlecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Zhang H, Shi L, Xu F, Ding G (2020) Genome-wide dissection of the CRF gene family in Brassica napus indicates that BnaCRF8s specifically regulate root architecture and phosphate homeostasis against phosphate fluctuation in plants. Int J Mol Sci 21(10):3660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang J, Hu Z, Guo X, Tian S, Chen G (2019) Genome-wide analysis of the MADS-Box transcription factor family in Solanum lycopersicum. Int J Mol Sci 20(12):2961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei W, Liang DW, Bian XH, Shen M, Xiao JH, Zhang WK, Ma B, Lin Q, Lv J, Chen X, Chen SY, Zhang JS (2019) GmWRKY54 improves drought tolerance through activating genes in abscisic acid and Ca2+ signaling pathways in transgenic soybean. Plant J 100(2):384–398

    Article  CAS  PubMed  Google Scholar 

  • Wu WQ, Du K, Kang XY, Wei HR (2021) The diverse roles of cytokinins in regulating leaf development. Hortic Res 8(1):118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki Y, Randall SK (2016) Functionality of soybean CBF/DREB1 transcription factors. Plant Sci 246:80–90

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Li YL, Yan ZW, Duan XB (2022) The role of cytokinins in plant under salt stress. J Plant Growth Regul 41:2279–2291

    Article  CAS  Google Scholar 

  • Zhang W, Wang S, Yu F, Tang J, Shan X, Bao K, Yu L, Wang H, Fei Z, Li J (2019) Genome-wide characterization and expression profiling of SWEET genes in cabbage (Brassica oleracea var. Capitata L.) reveal their roles in chilling and clubroot disease responses. BMC Genomics 20(1):93

    Article  PubMed  PubMed Central  Google Scholar 

  • Zwack PJ, Compton MA, Adams CI, Rashotte AM (2016) Cytokinin response factor 4 (CRF4) is induced by cold and involved in freezing tolerance. Plant Cell Rep 35(3):573–584

    Article  CAS  PubMed  Google Scholar 

  • Zwack PJ, Robinson BR, Risley MG, Rashotte AM (2013) Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant Cell Physiol 54(6):971–981

    Article  CAS  PubMed  Google Scholar 

  • Zwack PJ, Shi X, Robinson BR, Gupta S, Compton MA, Gerken DM, Goertzen LR, Rashotte AM (2012) Vascular expression and C-terminal sequence divergence of cytokinin response factors in flowering plants. Plant Cell Physiol 53(10):1683–1695

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of Heilongjiang Province of China (YQ2019C027) and the Research Foundation for Doctors of Liaoning Province (2019-BS-171).

Funding

This work was supported by the Natural Science Foundation of Heilongjiang Province of China (YQ2019C027) and the Research Foundation for Doctors of Liaoning Province (2019-BS-171).

Author information

Authors and Affiliations

Authors

Contributions

XD and YY conceived and designed the work, XD, KZ, and HD contributed to experiment performance and data analysis, XD and HD wrote the manuscript, KZ and YY revised and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Huizi Duanmu or Yang Yu.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Additional information

Handling Editor: Václav Motyka.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duan, X., Zhang, K., Duanmu, H. et al. Genome-Wide Identification and Expression Characteristics of Cytokinin Response Factors in Soybean. J Plant Growth Regul 42, 4484–4496 (2023). https://doi.org/10.1007/s00344-023-10914-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-023-10914-3

Keywords

Navigation