Abstract
Walnut is a popular nut tree species and usually suffers from drought stress. However, little information is available on the mechanism of walnut responding to drought stress, resulting in lack of basic understanding for its resistance. In order to excavate more functional genes that can respond to stressors, and enrich the theoretical basis for walnut resistance, in this study, 5 MYB genes with complete ORFs were identified from J. regia and the basic bio-information as well as expression patterns in different tissues and response to drought and ABA stresses were confirmed using qRT-PCR assay. The results showed that 2 JrMYB genes belong to R1-MYB subfamily and 3 JrMYBs belong to R2R3-MYB, encoding the proteins from 212 to 362 aa in length. The phylogenetic analysis categorized proteins of 5 JrMYBs and 40 Arabidopsis AtMYBs into 10 subgroups. JrMYBs in the same subgroup exhibited significant similarities in the composition of conserved domains and motifs in amino acid sequences and exon/intron organization in DNA sequences. The results of qRT-PCR analysis revealed that JrMYB genes diversely expressed in various tissues. Moreover, the expression values of JrMYBs were upregulated or downregulated significantly under drought and ABA stresses. Most attractively, in contrast with suffering from drought stress alone, the treatments with drought and additional ABA greatly enhanced the transcript levels of JrMYBs. All these results suggested that JrMYB genes play a vital role in plant biological processes and drought as well as ABA stress response, and possibly perform as ABA-dependent drought response transcription factors in plant.
Similar content being viewed by others
References
Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37(2):1125–1135
Alexander RD, Wendelboe-Nelson C, Morris PC (2019) The barley transcription factor HvMYB1 is a positive regulator of drought tolerance. Plant Physiol Bioch 142:246–253
Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5(6):241–246
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools - an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 18(3):1194–1202
Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15(13):1196–1200
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581
Fang Q, Jiang T, Xu L, Liu H, Mao H, Wang X, Jiao B, Duan Y, Wang Q, Dong Q, Yang L, Tian G, Zhang C, Zhou Y, Liu X, Wang H, Fan D, Wang B, Luo K (2017) A salt-stress-regulator from the Poplar R2R3 MYB family integrates the regulation of lateral root emergence and ABA signaling to mediate salt stress tolerance in Arabidopsis. Plant Physiol Biochem 114:100–110
Fang Q, Wang X, Wang H, Tang X, Liu C, Yin H, Ye S, Jiang Y, Duan Y, Luo K (2020) The poplar R2R3 MYB transcription factor PtrMYB94 coordinates with abscisic acid signaling to improve drought tolerance in plants. Tree Physiol 40(1):46–59
González-Villagra J, Cohen JD, Reyes-Díaz MM (2019) Abscisic acid is involved in phenolic compounds biosynthesis, mainly anthocyanins, in leaves of Aristotelia chilensis plants (Mol.) subjected to drought stress. Physiol Plantarum 165(4):855–866
Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41(41):95–98
Higginson T, Li S, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35(2):177–192
Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0 an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297
Kiran K, Ansari SA, Srivastava R, Lodhi N, Chaturvedi CP, Sawant SV, Tuli R (2006) The TATA-box sequence in the basal promoter contributes to determining light-dependent gene expression in plants. Plant Physiol 142(1):364–376
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer YVd, Rouzé 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
Leslie CA, Walawage SL, Uratsu SL, McGranahan G, Dandekar AM (2015) Walnuts (Juglans). Methods Mol Biol 1224(2):229–241
Li C, Ng CK-Y, Fan L-M (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91
Li G, Wang Z, Yokosho K, Ding B, Fan W, Gong Q, Li G, Wu Y, Yang J, Ma J, Zheng S (2018) Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol 219(1):149–162
Li X, Guo C, Ahmad S, Wang Q, Yu J, Liu C, Guo Y (2019) Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules 9(8):21
Li J, Liu H, Yang C, Wang J, Yan G, Si P, Bai Q, Lu Z, Zhou W, Xu L (2020) Genome-wide identification of MYB genes and expression analysis under different biotic and abiotic stresses in Helianthus annuus L. Ind Crop Prod 143:111924
Linger BR, Price CM (2009) Conservation of telomere protein complexes: shuffling through evolution. Crit Rev Biochem Mol Biol 44(6):434–446
Liu X, Yu W, Zhang X, Wang G, Cao F, Chen H (2017) Identification and expression analysis under abiotic stress of the R2R3-MYB genes in Ginkgo biloba L. Physiol Mol Biol Pla 23(3):503–516
Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83
Mmadi MA, Dossa K, Wang L, Zhou R, Wang Y, Cisse N, Sy MO, Zhang X (2017) Functional characterization of the versatile MYB gene family uncovered their important roles in plant development and responses to drought and waterlogging in sesame. Genes (basel) 8(12):362
Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu J-K, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63(3):417–429
Sabehat A, Weiss D, Lurie S (1998) Heat-shock proteins and cross-tolerance in plants. Physiol Plant 103(3):437–441
Schwechheimer C, Bevan M (1998) The regulation of transcription factor activity in plants. Trends Plant Sci 3(10):378–383
Shin B, Choi G, Yi H, Yang S, Cho I, Kim J, Lee S, Paek N-C, Kim J-H, Song P-S, Choi G (2002) AtMYB21, a gene encoding a flower-specific transcription factor, is regulated by COP1. Plant J 30(1):23–32
Song Y, Xuan A, Bu C, Ci D, Tian M, Zhang D (2019) Osmotic stress-responsive promoter upstream transcripts (PROMPTs) act as carriers of MYB transcription factors to induce the expression of target genes in Populus simonii. Plant Biotechnol J 17(1):164–177
Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34(4):519–528
Wei L, Wang L, Yang Y, Wang P, Guo T, Kang G (2015) Abscisic acid enhances tolerance of wheat seedlings to drought and regulates transcript levels of genes encoding ascorbate-glutathione biosynthesis. Front Plant Sci 6:458
Wen X, Wang J, Zhang D, Wang Y (2019) A Gene regulatory network controlled by BpERF2 and BpMYB102 in birch under drought conditions. Int J Mol Sci 20(12):3071
Xu F, Deng G, Cheng S, Zhang W, Huang X, Li L, Cheng H, Rong X, Li J (2012) Molecular cloning, characterization and expression of the phenylalanine ammonia-lyase gene from Juglans regia. Molecules 17(7):7810–7823
Xu Z, Ge Y, Zhang W, Zhao Y, Yang G (2018) The walnut JrVHAG1 gene is involved in cadmium stress response through ABA-signal pathway and MYB transcription regulation. BMC Plant Biol 18(1):19
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6(2):251–264
Yang G, Wang Y, Xia D, Gao C, Wang C, Yang C (2014) Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tiss Org 117(1):99–112
Zhang X, Lu G, Long W, Zou X, Li F, Nishio T (2014) Recent progress in drought and salt tolerance studies in Brassica crops. Breed Sci 64(1):60–73
Zhang C, Ma R, Xu J, Yan J, Guo L, Song J, Feng R, Yu M, Han Y (2018) Genome-wide identification and classification of MYB superfamily genes in peach. PLoS ONE 13(6):e0199192
Zhao P, Hou S, Guo X, Jia J, Yang W, Liu Z, Chen S, Li X, Qi D, Liu G, Cheng L (2019) A MYB-related transcription factor from sheepgrass, LcMYB2, promotes seed germination and root growth under drought stress. BMC Plant Biol 19(1):564
Zhao K, Cheng Z, Guo Q, Yao W, Liu H, Zhou B, Jiang T (2020) Characterization of the poplar R2R3-MYB gene family and over-expression of PsnMYB108 confers salt tolerance in transgenic tobacco. Front Plant Sci 11:571881
Zhou L, Yarra R, Jin L, Cao H (2020) Genome-wide identification and expression analysis of MYB gene family in oil palm (Elaeis guineensis Jacq) under abiotic stress conditions. Environ Exp Bot 180:104245
Funding
The current study was supported by National Natural Science Foundation of China (31800510), Special Financial Grant from the China Postdoctoral Science Foundation (2017T100782), Northwest A & F University Foundation (TGZX2020-05).
Author information
Authors and Affiliations
Contributions
Dapei Li and Guiyan Yang conceived and designed the experiments. Dapei Li, Yi He, and Ziyi Li performed the experiments. Shuwen Chen, Bin Ren, and Guiyan Yang assisted in data collection and analysis. Dapei Li, Guiyan Yang and Shaobing Peng drafted the manuscript. All authors read and approved this final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest.
Availability of data and material
All the data were presented in the main manuscript and additional supporting files.
Ethical approval
Not applicable.
Code availability
Not applicable.
Consent to participate
Written informed consent to participate was obtained from all the authors, who not only designed and performed the experiment, but also drafted and completed the manuscript.
Consent for publication
Written informed consent for publication was obtained from all the participants, who agreed with publication in the journal Molecular Breeding.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, D., Peng, S., Chen, S. et al. Identification and characterization of 5 walnut MYB genes in response to drought stress involved in ABA signaling. Physiol Mol Biol Plants 27, 1323–1335 (2021). https://doi.org/10.1007/s12298-021-01008-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-01008-z