Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Genome-wide mining of B-type cytokinin response regulators in wheat reveals the involvement of TaRR5.1-6A in drought and salt tolerance

Yifeng Hu https://orcid.org/0000-0001-5009-1252 A # , Hongmei Cui A # , Pengliang Xia B # , Gensen Liu A , Xingyang Wu A C , Yiting Li A , Yan Yang A , Fansong Zeng C , Yan Li A C * and Dongfang Ma https://orcid.org/0000-0002-0724-0870 A C *
+ Author Affiliations
- Author Affiliations

A Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education/College of Agriculture, Yangtze University, Jingzhou 434000, China.

B Enshi Tobacco Company of Hubei Province, Enshi 445000, Hubei, China.

C Key Laboratory of Integrated Pest Management on Crop in Central China, Ministry of Agriculture/Hubei Province Key Laboratory for Control of Crop Diseases, Pest and Weeds/Institute of Plant Protection and Soil Science, Hubei Academy of Agricultural Sciences, Wuhan 430064, Hubei, China.

# These authors contributed equally to this paper

Handling Editor: Enrico Francia

Crop & Pasture Science 73(9) 997-1010 https://doi.org/10.1071/CP21766
Submitted: 20 August 2021  Accepted: 11 January 2022   Published: 21 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Cytokinin response regulators (RRs) are important components of the two component signal systems that are involved in the regulation of plant growth and development, and in the response to abiotic stresses. Plant cytokinin response regulators (RR) were divided into type A and type B. A-type RR proteins act as negative feedback to regulate cytokinin signals, while B-type RRs could regulate A-type RR gene expression, and B-type RR genes have proved to play important roles in regulating cytokinin signal transduction in various biological processes.

Aims: We aimed to explore and analyse B-type RR genes in wheat in a preliminary fashion.

Methods: Using bioinformatics methods, wheat type B RR genes were identified, and type B Triticum aestivum RR (TaRR) genes were analysed using quantitative real-time polymerase chain reaction. In order to further analyse the function of TaRR, staining experiments were performed.

Key results: Twenty-nine B-type TaRR genes were identified in the wheat genome, divided into three groups according to their phylogenetic relationships. Chromosome mapping showed that 29 TaRRs were evenly distributed on 12 chromosomes, while there were no genes located on the other nine chromosomes, which may have experienced gene loss during evolution. The polymerase chain reaction results showed that TaRRs were significantly up-regulated under polyethylene glycol treatments. Under sodium chloride stress, TaRRs were up-regulated to varying degrees, reaching the maximum at 24 h. The study also found that the expression pattern of TaRRs was different in the root and leaf under different abiotic stresses. In addition, staining experiments also showed that TaRR5.1-6A could induce the self-defence function of leaves.

Conclusions: These results form the basis for further exploring the role of B-type TaRR genes in plant response to drought stress and salt stress.

Implications: This study lays the molecular biology foundation for the functional study of the B-type TaRR genes.

Keywords: B-type RR, bioinformatics, cytokinin, drought stress, qRT-PCR, salt stress, TaRR5.1-6A, wheat.


References

Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin in Arabidopsis. Frontiers in Plant Science 3, 8
Gene regulation by cytokinin in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22639635PubMed |

Cao Y-P, Han Y-H, Meng D-D, Li D-H, Jin Q, Lin Y, Cai Y-P (2016) Structural, evolutionary, and functional analysis of the class III peroxidase gene family in Chinese pear (Pyrus bretschneideri). Frontiers in Plant Science 7, 1874
Structural, evolutionary, and functional analysis of the class III peroxidase gene family in Chinese pear (Pyrus bretschneideri).Crossref | GoogleScholarGoogle Scholar |

Chou K-C, Shen H-B (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5, e11335
Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization.Crossref | GoogleScholarGoogle Scholar | 20596258PubMed |

Chu ZX (2011) Analysis and regulation of maize cytokinin dual signal system genes. Masters Thesis, Anhui Agricultural University, China.
| Crossref |

Du L-M, Jiao F-C, Chu J, Jin G-L, Chen M, Wu P (2007) The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction. Genomics 89, 697–707.
The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction.Crossref | GoogleScholarGoogle Scholar |

Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schäfer E, Kudla J, Harter K (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. The EMBO Journal 23, 3290–3302.
The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15282545PubMed |

He Y-Q, Huang W-D, Yang L, Li Y-T, Lu C, Zhu Y-X, Ma D-F, Yin J-L (2020) Genome-wide analysis of ethylene-insensitive3 (EIN3/EIL) in Triticum aestivum. Crop Science 60, 2019–2037.
Genome-wide analysis of ethylene-insensitive3 (EIN3/EIL) in Triticum aestivum.Crossref | GoogleScholarGoogle Scholar |

Huang H, Tang YW (1984) Regulatory effects of abscisic acid and 6-benzylaminopurine on the formation of δ-aminolevulinic acid in isolated wheat leaves. Acta Phytophysiology 347–351.

Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389.
Two-component circuitry in Arabidopsis cytokinin signal transduction.Crossref | GoogleScholarGoogle Scholar | 11574878PubMed |

Jiang W-Q, Yang L, He Y-Q, Zhang H-T, Li W, Chen H-G, Ma D-F, Yin J-L (2019) Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum L.). PeerJ 7, e8062
Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |

Kiba T, Yamada H, Mizuno T (2002) Characterization of the arr15 and arr16 response regulators with special reference to the cytokinin signaling pathway mediated by the ahk4 histidine kinase in roots of Arabidopsis thaliana. Plant and Cell Physiology 43, 1059–1066.
Characterization of the arr15 and arr16 response regulators with special reference to the cytokinin signaling pathway mediated by the ahk4 histidine kinase in roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12354925PubMed |

Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 814–819.
Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16407152PubMed |

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Letunic I, Bork P (2018) 20 Years of the SMART protein domain annotation resource. Nucleic Acids Research 46, D493–D496.
20 Years of the SMART protein domain annotation resource.Crossref | GoogleScholarGoogle Scholar | 29040681PubMed |

Li SW, Xue LG, Feng HY, Xu SJ, An LZ (2007) H2O2 signal and its function in plants. Chinese Journal of Biochemistry and Molecular Biology 23, 7
H2O2 signal and its function in plants.Crossref | GoogleScholarGoogle Scholar |

Li L-b, Yu D-w, Zhao F-l, Pang C-y, Song M-z, Wei H-l, Fan S-l, Yu S-x (2015) Genome-wide analysis of the calcium-dependent protein kinase gene family in Gossypium raimondii. Journal of Integrative Agriculture 14, 29–41.
Genome-wide analysis of the calcium-dependent protein kinase gene family in Gossypium raimondii.Crossref | GoogleScholarGoogle Scholar |

Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 19346325PubMed |

Ling HQ, Zhao SC, Liu DC, et al. (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496, 87–90.
Draft genome of the wheat A-genome progenitor Triticum urartu.Crossref | GoogleScholarGoogle Scholar | 23535596PubMed |

Liu CZ, Zhang TT, Zhao J, Li XP (2012) Signal transduction mechanism of cytokinins. Anhui Agricultural Science 40, 4
Signal transduction mechanism of cytokinins.Crossref | GoogleScholarGoogle Scholar |

Lu LJ, Chen XY, Zhang YL, Liu X, Wang LM, Ma L, Li H (2018) Bioinformatics analysis of wheat GASA gene family. Crop Journal 6, 58–67.
Bioinformatics analysis of wheat GASA gene family.Crossref | GoogleScholarGoogle Scholar |

Mason MG, Jha D, Salt DE, et al. (2010) Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots. The Plant Journal 64, 753–763.
Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots.Crossref | GoogleScholarGoogle Scholar | 21105923PubMed |

Meng WJ (2018) ‘Molecular mechanism of Arabidopsis B class ARRs regulating the remodeling and maintenance of stem apical meristem.’ Doctoral dissertation, Shandong Agricultural University, China.

Nguyen KH, Ha CV, Nishiyama R, et al. (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proceedings of the National Academy of Sciences of the United States of America 113, 3090–3095.
Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought.Crossref | GoogleScholarGoogle Scholar | 26884175PubMed |

Paolacci A, Tanzarella O, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Molecular Biology 10, 11
Identification and validation of reference genes for quantitative RT-PCR normalization in wheat.Crossref | GoogleScholarGoogle Scholar | 19232096PubMed |

Qi Y, Shi HP, Li L (2004) Molecular mechanism of cytokinin signal transduction. Life Science Research 5
Molecular mechanism of cytokinin signal transduction.Crossref | GoogleScholarGoogle Scholar |

Sakai H, Honma T, Aoyama T, et al. (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519–1521.
ARR1, a transcription factor for genes immediately responsive to cytokinins.Crossref | GoogleScholarGoogle Scholar | 11691951PubMed |

Schaller GE, Kieber JJ, Shiu S-H (2008) Two-component signaling elements and histidyl-aspartyl phosphorelays. The Arabidopsis Book 2008, e0112
Two-component signaling elements and histidyl-aspartyl phosphorelays.Crossref | GoogleScholarGoogle Scholar |

Shao WN, Chen W, Zhu XG, et al. (2021) Genome-wide identification and characterization of wheat 14-3-3 genes unravels the role of TaGRF6-A in salt stress tolerance by binding MYB transcription factor. International Journal of Molecular Sciences 22, 1904
Genome-wide identification and characterization of wheat 14-3-3 genes unravels the role of TaGRF6-A in salt stress tolerance by binding MYB transcription factor.Crossref | GoogleScholarGoogle Scholar |

Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiology 132, 530–543.
Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12805585PubMed |

Thakur N Thakur N (2021) Genome-wide identification and analysis of GHMP kinase gene superfamily in bread wheat (Triticum aestivum L.). Plant Molecular Biology Reporter 39, 455–470.
Genome-wide identification and analysis of GHMP kinase gene superfamily in bread wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |

To JPC, Haberer G, Ferreira FJ, Deruère J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling[W]. The Plant Cell 16, 658–671.
Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling[W].Crossref | GoogleScholarGoogle Scholar |

Trapnell C, Roberts A, Goff L, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7, 562–578.
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks.Crossref | GoogleScholarGoogle Scholar | 22383036PubMed |

Wang SG (2000) The role of cytokinin in plant resistance and aging. Botany Bulletin 17, 121–126.
The role of cytokinin in plant resistance and aging.Crossref | GoogleScholarGoogle Scholar |

Yang MY (2018) ‘Wheat cytokinin response factor TaARR193, calmodulin TaCaM12, TaPC and TaNF-YB3;1 molecular characteristics and stress tolerance identification.’ (Hebei Agricultural University: China)

Yin J-L, Jia J-H, Lian Z-Y, Hu Y-H, Guo J, Huo H-Q, Zhu Y-X, Gong H-J (2019) Silicon enhances the salt tolerance of cucumber through increasing polyamine accumulation and decreasing oxidative damage. Ecotoxicology and Environmental Safety 169, 8–17.
Silicon enhances the salt tolerance of cucumber through increasing polyamine accumulation and decreasing oxidative damage.Crossref | GoogleScholarGoogle Scholar |

Yu Q, He L-S, Huo C-S, Jiang X-H, Chen H, Wang R, Tang M-Z, Dong L, Chen J, Li Y-H, Zhu S-Z, Liu W-H (2020) Genome-wide identification and expression analysis of heavy metal stress-responsive Metallothionein family genes in Nicotiana tabacum. Plant Molecular Biology Reporter 39, 443–454.
Genome-wide identification and expression analysis of heavy metal stress-responsive Metallothionein family genes in Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar |

Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics, Proteomics & Bioinformatics 4, 259–263.
KaKs_Calculator: calculating Ka and Ks through model selection and model averaging.Crossref | GoogleScholarGoogle Scholar |

Zhang T, Lv W, Zhang H, Ma L, Li P, Ge L, Li G (2018) Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize. BMC Plant Biology 18, 235
Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize.Crossref | GoogleScholarGoogle Scholar | 30326829PubMed |

Zhang P-G, Zhu Y-X, Ma D-F, Xu W-J, Zhou J-J, Yan H-W, Yang L, Yin J-L (2019) Screening, identification, and optimization of fermentation conditions of an antagonistic endophyte to wheat head blight. Agronomy 9, 476–509.
Screening, identification, and optimization of fermentation conditions of an antagonistic endophyte to wheat head blight.Crossref | GoogleScholarGoogle Scholar |