Genome-wide analysis of MYB transcription factor family and AsMYB1R subfamily contribution to ROS homeostasis regulation in Avena sativa under PEG-induced drought stress.
Transcription Factors
/ genetics
Droughts
Plant Proteins
/ genetics
Phylogeny
Reactive Oxygen Species
/ metabolism
Homeostasis
Avena
/ genetics
Gene Expression Regulation, Plant
Polyethylene Glycols
/ pharmacology
Multigene Family
Stress, Physiological
/ genetics
Genome-Wide Association Study
Genome, Plant
Avena sativa
Drought stress
MYB transcription factors
ROS
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
06 Jul 2024
06 Jul 2024
Historique:
received:
13
03
2024
accepted:
05
06
2024
medline:
6
7
2024
pubmed:
6
7
2024
entrez:
5
7
2024
Statut:
epublish
Résumé
The myeloblastosis (MYB) transcription factor (TF) family is one of the largest and most important TF families in plants, playing an important role in a life cycle and abiotic stress. In this study, 268 Avena sativa MYB (AsMYB) TFs from Avena sativa were identified and named according to their order of location on the chromosomes, respectively. Phylogenetic analysis of the AsMYB and Arabidopsis MYB proteins were performed to determine their homology, the AsMYB1R proteins were classified into 5 subgroups, and the AsMYB2R proteins were classified into 34 subgroups. The conserved domains and gene structure were highly conserved among the subgroups. Eight differentially expressed AsMYB genes were screened in the transcriptome of transcriptional data and validated through RT-qPCR. Three genes in AsMYB2R subgroup, which are related to the shortened growth period, stomatal closure, and nutrient and water transport by PEG-induced drought stress, were investigated in more details. The AsMYB1R subgroup genes LHY and REV 1, together with GST, regulate ROS homeostasis to ensure ROS signal transduction and scavenge excess ROS to avoid oxidative damage. The results of this study confirmed that the AsMYB TFs family is involved in the homeostatic regulation of ROS under drought stress. This lays the foundation for further investigating the involvement of the AsMYB TFs family in regulating A. sativa drought response mechanisms.
Sections du résumé
BACKGROUND
BACKGROUND
The myeloblastosis (MYB) transcription factor (TF) family is one of the largest and most important TF families in plants, playing an important role in a life cycle and abiotic stress.
RESULTS
RESULTS
In this study, 268 Avena sativa MYB (AsMYB) TFs from Avena sativa were identified and named according to their order of location on the chromosomes, respectively. Phylogenetic analysis of the AsMYB and Arabidopsis MYB proteins were performed to determine their homology, the AsMYB1R proteins were classified into 5 subgroups, and the AsMYB2R proteins were classified into 34 subgroups. The conserved domains and gene structure were highly conserved among the subgroups. Eight differentially expressed AsMYB genes were screened in the transcriptome of transcriptional data and validated through RT-qPCR. Three genes in AsMYB2R subgroup, which are related to the shortened growth period, stomatal closure, and nutrient and water transport by PEG-induced drought stress, were investigated in more details. The AsMYB1R subgroup genes LHY and REV 1, together with GST, regulate ROS homeostasis to ensure ROS signal transduction and scavenge excess ROS to avoid oxidative damage.
CONCLUSION
CONCLUSIONS
The results of this study confirmed that the AsMYB TFs family is involved in the homeostatic regulation of ROS under drought stress. This lays the foundation for further investigating the involvement of the AsMYB TFs family in regulating A. sativa drought response mechanisms.
Identifiants
pubmed: 38970019
doi: 10.1186/s12870-024-05251-w
pii: 10.1186/s12870-024-05251-w
doi:
Substances chimiques
Transcription Factors
0
Plant Proteins
0
Reactive Oxygen Species
0
Polyethylene Glycols
3WJQ0SDW1A
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
632Informations de copyright
© 2024. The Author(s).
Références
Verma A, Deepti S. Abiotic stress and crop improvement: current scenario. Adv Plants Agric Res. 2016; 4(4):345–6.
Hou P, Wang F, Luo B, Li A, Wang C, Shabala L et al. Antioxidant enzymatic activity and osmotic adjustment as components of the drought tolerance mechanism in Carex duriuscula. Plants. 2021;10(3).
Irigoyen JJ, Einerich DW, Sánchez-Díaz M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant. 1992;84(1):55–60.
doi: 10.1111/j.1399-3054.1992.tb08764.x
Daszkowska-Golec A, Szarejko I. Open or close the gate - stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci. 2013;4.
Hasanuzzaman M, Zhou MX, Shabala S. How does stomatal density and residual transpiration contribute to osmotic stress tolerance? Plants. 2023;12(3).
Nadarajah KK. ROS homeostasis in abiotic stress tolerance in plants. Int J Mol Sci. 2020;21(15).
Geng A, Lian W, Wang Y, Liu M, Zhang Y, Wang X et al. Molecular mechanisms and regulatory pathways underlying drought stress response in rice. Int J Mol Sci. 2024;25(2).
Rasane P, Jha A, Sabikhi L, Kumar A, Unnikrishnan VS. Nutritional advantages of oats and opportunities for its processing as value added foods - a review. J Food Sci Technol. 2015;52(2):662–75.
pubmed: 25694675
doi: 10.1007/s13197-013-1072-1
Kamal N, Tsardakas Renhuldt N, Bentzer J, Gundlach H, Haberer G, Juhász A et al. The mosaic oat genome gives insights into a uniquely healthy cereal crop. Nature. 2022;606(7912):113–9.
Isidro-Sánchez J, Prats E, Howarth CJ, Langdon T, Montilla-Bascón G. Genomic approaches for climate resilience breeding in oats. 2020: 133–69.
Han L, Liu H, Yu S, Wang W, Liu J. Potential application of oat for phytoremediation of salt ions in coastal saline-alkali soil. Ecol Eng. 2013;61:274–81.
doi: 10.1016/j.ecoleng.2013.09.034
Wu B, Hu Y, Huo P, Zhang Q, Chen X, Zhang Z. Transcriptome analysis of hexaploid hulless oat in response to salinity stress. PLoS ONE. 2017;12(2):e0171451.
pubmed: 28192458
pmcid: 5305263
doi: 10.1371/journal.pone.0171451
Hou P, Qu M, Yun P, Li A, Ahmed HAI, Peng Y, et al. Avena sativa under drought stress. Boca Raton: CRC; 2023.
doi: 10.1201/9781003242963-4
Peltonen-Sainio P, Mäkelä PSA. Comparison of physiological methods to assess drought tolerance in oats. Acta Agr Scand B-S P. 1995;45:32–8.
Gong D-S, Xiong Y, Ma B-L, Wang T-M, Ge J-P, Qin X, et al. Early activation of plasma membrane H+-ATPase and its relation to drought adaptation in two contrasting oat (Avena sativa L.) genotypes. Environ Exp Bot. 2010;69:1–8.
doi: 10.1016/j.envexpbot.2010.02.011
Munns R, Day DA, Fricke W, Watt M, Arsova B, Barkla BJ, et al. Energy costs of salt tolerance in crop plants. New Phytol. 2020;225(3):1072–90.
pubmed: 31004496
doi: 10.1111/nph.15864
Peng Y, Yan H, Guo L, Deng C, Wang C, Wang Y, et al. Reference genome assemblies reveal the origin and evolution of allohexaploid oat. Nat Genet. 2022;54(8):1248–58.
pubmed: 35851189
pmcid: 9355876
doi: 10.1038/s41588-022-01127-7
Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, Schippers JHM, Dijkwel PP. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci USA. 2012;109(42):p17129–17134.
doi: 10.1073/pnas.1209148109
Ma D, Constabel CP. MYB repressors as regulators of phenylpropanoid metabolism in plants. Trends Plant Sci. 2019;24(3):275–89.
pubmed: 30704824
doi: 10.1016/j.tplants.2018.12.003
Jiménez A, Sevilla F, Martí MC. Reactive oxygen species homeostasis and circadian rhythms in plants. J Exp Bot. 2021;72(16):5825–40.
pubmed: 34270727
doi: 10.1093/jxb/erab318
Li X, Guo C, Li Z, Wang G, Yang J, Chen L, et al. Deciphering the roles of tobacco MYB transcription factors in environmental stress tolerance. Front Plant Sci. 2022;13:998606.
pubmed: 36352868
pmcid: 9638165
doi: 10.3389/fpls.2022.998606
Liu D, Tang D, Xie M, Zhang J, Zhai L, Mao J, et al. Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus. Plant Physiol. 2023;191(3):1492–504.
pubmed: 36546733
doi: 10.1093/plphys/kiac588
Azuara-Liceaga EI, Sanchez-Buena S, Meneses E, Brieba LG, Orozco E. Identification of myb transcription factors in Entamoeba histolytica. Faseb J. 2007;21(6):A1031–1031.
Kundan M, Gani U, Fayaz M, Angmo T, Kesari R, Rahul VP, et al. Two R2R3-MYB transcription factors, CsMYB33 and CsMYB78 are involved in the regulation of anthocyanin biosynthesis in Cannabis sativa L. Ind Crops Prod. 2022;188:115546.
doi: 10.1016/j.indcrop.2022.115546
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010;15(10):573–81.
pubmed: 20674465
doi: 10.1016/j.tplants.2010.06.005
Ji K, Liu CY, Wu KY, Yue ZH, Dong Y, Gong BC et al. Genome-wide characterization of the R2R3-MYB gene family in Diospyros oleifera. Agriculture. 2023;13(5).
Li H, Wen X, Wei M, Huang X, Dai S, Ruan L et al. Genome-Wide identification, characterization, and expression pattern of MYB gene family in Melastoma candidum. Horticulturae. 2023;9(6):708.
Munné-Bosch S, Peñuelas J. Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea Angustifolia plants. Planta. 2003;217(5):758–66.
pubmed: 12698367
doi: 10.1007/s00425-003-1037-0
Smirnoff N. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 1993;125(1):27–58.
pubmed: 33874604
doi: 10.1111/j.1469-8137.1993.tb03863.x
Rudenko NN, Vetoshkina DV, Marenkova TV, Borisova-Mubarakshina MM. Antioxidants of non-enzymatic nature: their function in higher plant cells and the ways of boosting their biosynthesis. Antioxidants. 2023;12(11).
Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, et al. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na
Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signalling. J Exp Bot. 2014;65(5):1229–40.
pubmed: 24253197
doi: 10.1093/jxb/ert375
Linde AM, Eklund DM, Kubota A, Pederson ERA, Holm K, Gyllenstrand N, et al. Early evolution of the land plant circadian clock. New Phytol. 2017;216(2):576–90.
pubmed: 28244104
pmcid: 5638080
doi: 10.1111/nph.14487
Martin C, Paz-Ares J. MYB transcription factors in plants. Trends Genet. 1997;13(2):67–73.
pubmed: 9055608
doi: 10.1016/S0168-9525(96)10049-4
Zargarian L, Le Tilly V, Jamin N, Chaffotte A, Gabrielsen OS, Toma F et al. Myb-DNA recognition: role of tryptophan residues and structural changes of the minimal DNA binding domain of c-Myb. Biochemistry. 1999;38(6):1921–9.
Li H, Yang X, Niyitanga S, He Q, Chen S, Xu J, et al. Transcriptomes of different tissues for expression characteristics analysis of MYB gene family in kenaf (Hibiscus cannabinus L). Trop Plant Biology. 2022;15(4):261–75.
doi: 10.1007/s12042-022-09320-y
Tombuloglu H. Genome-wide identification and expression analysis of R2R3, 3R- and 4R-MYB transcription factors during lignin biosynthesis in flax (Linum usitatissimum). Genomics. 2020;112(1):782–95.
pubmed: 31128265
doi: 10.1016/j.ygeno.2019.05.017
Li X, Xue C, Li J, Qiao X, Li L, Yu L, et al. Genome-wide identification, evolution and functional divergence of MYB transcription factors in Chinese white pear (Pyrus Bretschneideri). Plant Cell Physiol. 2016;57(4):824–47.
pubmed: 26872835
doi: 10.1093/pcp/pcw029
Xu Q, He J, Dong J, Hou X, Zhang X. Genomic survey and expression profiling of the MYB gene family in watermelon. Hortic Plant J. 2018;4(1):1–15.
doi: 10.1016/j.hpj.2017.12.001
Li Z, Peng R, Tian Y, Han H, Xu J, Yao Q. Genome-wide identification and analysis of the MYB transcription factor superfamily in Solanum lycopersicum. Plant Cell Physiol. 2016;57(8):1657–77.
pubmed: 27279646
doi: 10.1093/pcp/pcw091
Li SJ, Huang H, Ma XN, Hu ZK, Li JY, Yin HF. Characterizations of MYB transcription factors in Camellia Oleifera reveal the key regulators involved in oil biosynthesis. Horticulturae. 2022;8(8).
Hajiebrahimi A, Owji H, Hemmati S. Genome-wide identification, functional prediction, and evolutionary analysis of the R2R3-MYB superfamily in Brassica napus. Genome. 2017;60(10):797–814.
pubmed: 28732175
doi: 10.1139/gen-2017-0059
Si Z, Wang L, Ji Z, Zhao M, Zhang K, Qiao Y. Comparative analysis of the MYB gene family in seven Ipomoea species. Front Plant Sci. 2023;14:1155018.
pubmed: 37021302
pmcid: 10067929
doi: 10.3389/fpls.2023.1155018
Yao C, Li X, Li Y, Yang G, Liu W, Shao B et al. Overexpression of a Malus baccata MYB transcription factor gene MbMYB4 increases cold and drought tolerance in Arabidopsis thaliana. Int J Mol Sci. 2022;23(3).
Chen T, Li W, Hu X, Guo J, Liu A, Zhang B. A cotton MYB transcription factor, GbMYB5, is positively involved in plant adaptive response to drought stress. Plant Cell Physiol. 2015;56(5):917–29.
pubmed: 25657343
doi: 10.1093/pcp/pcv019
Yang A, Dai X, Zhang WH. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot. 2012;63(7):2541–56.
pubmed: 22301384
pmcid: 3346221
doi: 10.1093/jxb/err431
Xiong H, Li J, Liu P, Duan J, Zhao Y, Guo X, et al. Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE. 2014;9(3):e92913.
pubmed: 24667379
pmcid: 3965499
doi: 10.1371/journal.pone.0092913
Gao S, Xu J, Song W, Dong J, Xie L, Xu B. Overexpression of BnMYBL2-1 improves plant drought tolerance via the ABA-dependent pathway. Plant Physiol Biochem. 2023;207:108293.
pubmed: 38181638
doi: 10.1016/j.plaphy.2023.108293
Jian L, Kang K, Choi Y, Suh MC, Paek NC. Mutation of OsMYB60 reduces rice resilience to drought stress by attenuating cuticular wax biosynthesis. Plant J. 2022;112(2):339–51.
pubmed: 35984735
doi: 10.1111/tpj.15947
Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, et al. Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell. 2010;22(3):672–89.
pubmed: 20305120
pmcid: 2861464
doi: 10.1105/tpc.109.073668
Zhang H, Xu C, He Y, Zong J, Yang X, Si H, et al. Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci U S A. 2013;110(1):76–81.
pubmed: 23256151
doi: 10.1073/pnas.1213041110
Chen L, Bernhardt A, Lee J, Hellmann H. Identification of Arabidopsis MYB56 as a novel substrate for CRL3BPM E3 ligases. Mol Plant. 2014.
Chen X, Zhao C, Yun P, Yu M, Zhou M, Chen ZH et al. Climate-resilient crops: lessons from xerophytes. Plant J. 2023.
Liang Y-K, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM. AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol. 2005;15(13):1201–6.
pubmed: 16005292
doi: 10.1016/j.cub.2005.06.041
Liang Y-K, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM. AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol. 2005;15:1201–6.
pubmed: 16005292
doi: 10.1016/j.cub.2005.06.041
Jung C, Seo JS, Han SW, Koo YJ, Kim C-H, Song SI, et al. Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis 1. Plant Physiol. 2007;146:623–35.
pubmed: 18162593
Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, et al. The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 2009;151(1):275–89.
pubmed: 19625633
pmcid: 2735973
doi: 10.1104/pp.109.144220
Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, et al. A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol. 2005;15:1196–200.
pubmed: 16005291
doi: 10.1016/j.cub.2005.05.048
Kamiya T, Borghi M, Wang P, Danku JM, Kalmbach L, Hosmani PS, et al. The MYB36 transcription factor orchestrates casparian strip formation. Proc Natl Acad Sci U S A. 2015;112(33):10533–8.
pubmed: 26124109
pmcid: 4547244
doi: 10.1073/pnas.1507691112
De Leone MJ, Hernando CE, Romanowski A, García-Hourquet M, Careno D, Casal J et al. The LNK gene family: at the crossroad between light signaling and the circadian clock. Genes. 2018;10(1).
Dubois M, Claeys H, Van den Broeck L, Inzé D. Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought. Plant Cell Environ. 2017;40(2):180–9.
pubmed: 27479938
doi: 10.1111/pce.12809
Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, et al. REVEILLE1, a myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA. 2009;106(39):16883–8.
pubmed: 19805390
pmcid: 2757846
doi: 10.1073/pnas.0813035106
Yin H, Guo HB, Weston DJ, Borland AM, Ranjan P, Abraham PE, et al. Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave. BMC Genomics. 2018;19(1):588.
pubmed: 30081833
pmcid: 6090859
doi: 10.1186/s12864-018-4964-7
Xu G, Guo H, Zhang D, Chen D, Jiang Z, Lin R. REVEILLE1 promotes NADPH: protochlorophyllide oxidoreductase A expression and seedling greening in Arabidopsis. Photosynth Res. 2015;126(2–3):331–40.
pubmed: 25910753
doi: 10.1007/s11120-015-0146-5
Luklová M, Novák J, Kopecká R, Kameniarová M, Gibasová V, Brzobohatý B et al. Phytochromes and their role in diurnal variations of ROS metabolism and plant proteome. Int J Mol Sci. 2022;23(22).
Hou P, Qu M, Yun P, Li A, Ahmed HAI, Peng Y, et al. Avena sativa under Drought stress. Boca Raton: CRC; 2023.
doi: 10.1201/9781003242963-4
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, et al. ROS signaling: the new wave? Trends Plant Sci. 2011;16(6):300–9.
pubmed: 21482172
doi: 10.1016/j.tplants.2011.03.007
Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658–9.
pubmed: 16731699
doi: 10.1093/bioinformatics/btl158
Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J, et al. TBtools-II: a one for all, all for one bioinformatics platform for biological big-data mining. Mol Plant. 2023;16(11):1733–42.
pubmed: 37740491
doi: 10.1016/j.molp.2023.09.010
Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, et al. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol. 2006;60(1):107–24.
pubmed: 16463103
doi: 10.1007/s11103-005-2910-y
Wang Y, Zhang Y, Fan C, Wei Y, Meng J, Li Z, et al. Genome-wide analysis of MYB transcription factors and their responses to salt stress in Casuarina equisetifolia. BMC Plant Biol. 2021;21(1):328.
pubmed: 34238224
pmcid: 8265015
doi: 10.1186/s12870-021-03083-6
Gong W, Ju Z, Chai J, Zhou X, Lin D, Su W, et al. Physiological and transcription analyses reveal the regulatory mechanism in oat (Avena sativa) seedlings with different drought resistance under PEG-Induced drought stress. Agronomy. 2022;12(5):1005.
doi: 10.3390/agronomy12051005
Yin H, Yin D, Zhang M, Gao Z, Tuluhong M, Li X et al. Validation of appropriate reference genes for qRT-PCR normalization in Oat (Avena sativa L.) under UV-B and high-light stresses. Int J Mol Sci. 2022;23(19).
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
Guo X, Niu J, Cao X. Heterologous expression of Salvia miltiorrhiza microRNA408 enhances tolerance to salt stress in Nicotiana Benthamiana. Int J Mol Sci. 2018;19(12).
Guan L, Haider MS, Khan N, Nasim M, Jiu S, Fiaz M et al. Transcriptome sequence analysis elaborates a complex defensive mechanism of grapevine (Vitis vinifera L.) in response to salt stress. Int J Mol Sci. 2018;19(12).