Abstract
Brassinosteroids (BRs) and abscisic acid (ABA) both play positive roles in plant resistance to cold stress. Despite the recent report on the involvement of ABA in BR-induced enhanced tolerance to cold stress, the underlying molecular mechanisms of stress tolerance remain unclear. Moreover, whether there are ABA-independent pathways for BR-induced enhancement of cold stress tolerance in grapevines needs to be clarified. Herein, the potential involvement of ABA in BR-induced cold resistance in grapevines was investigated by contrasting the different responses among ABA, BR, and the combination of BR and NDGA (an inhibitor of endogenous ABA biosynthesis) treatments under cold stress. Results showed BR and ABA foliar application alone increased the chlorophyll fluorescence parameters, regulated the antioxidant system, and alleviated oxidative damage induced by cold stress. Interestingly, NDGA blocked the BR-induced cold resistance by increasing reactive oxygen species content and reducing antioxidant enzyme activity. Transcriptomic analysis suggested that exposure to cold stress resulted in very different patterns of gene expression and enriched pathway responses. Among them, ERF transcription factors were observed to be up-regulated in both BR and ABA treatment, calcium-binding protein genes were up-regulated only under BR treatment alone, and xyloglucosyl transferase genes were up-regulated only under ABA treatment. Overall, we concluded that ABA was involved in BR-induced cold resistance in grapevines, but there was also a different candidate pathway between ABA and BR treatments under cold stress.
Similar content being viewed by others
Data availability
All data supporting the findings of this study are available within the article (and its supplementary information files).
References
An SM, Liu Y, Sang KQ, Wang T, Yu JQ, Zhou YH, Xia XJ (2023) Brassinosteroid signaling positively regulates abscisic acid biosynthesis in response to chilling stress in tomato. J Integr Plant Biol 65(1):10–24. https://doi.org/10.1111/jipb.13356
Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9(12):591–596. https://doi.org/10.1016/j.tplants.2004.10.007
Chen ZY, Wang YT, Pan XB, Xi ZM (2019) Amelioration of cold-induced oxidative stress by exogenous 24-epibrassinolide treatment in grapevine seedlings: toward regulating the ascorbate–glutathione cycle. Sci Hortic 244:379–387. https://doi.org/10.1016/j.scienta.2018.09.062
Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23(4):1219–1230. https://doi.org/10.1105/tpc.111.084475
Devireddy AR, Zandalinas SI, Fichman Y, Mittler R (2021) Integration of reactive oxygen species and hormone signaling during abiotic stress. Plant J 105(2):459–476. https://doi.org/10.1111/tpj.15010
Ding YL, Shi YT, Yang SH (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222(4):1690–2170. https://doi.org/10.1111/nph.15696
Fang PP, Yan MY, Chi C, Wang MQ, Zhou YH, Zhou J, Shi K, Xia XJ, Foyer CH, Yu JQ (2019) Brassinosteroids act as a positive regulator of photoprotection in response to chilling stress. Plant Physiol 180(4):2061–2076. https://doi.org/10.1104/pp.19.00088
Finkelstein R (2013) Abscisic acid synthesis and response. Arab B 11: e0166. https://doi.org/10.1199/tab.0166
Fu JJ, Wu Y, Miao YJ, Xu YM, Zhao EH, Wang J, Sun HE, Liu Q, Xue YW, Xu YF, Hu TM (2017) Improved cold tolerance in Elymus nutans by exogenous application of melatonin may involve ABA-dependent and ABA-independent pathways. Sci Rep 7:39865. https://doi.org/10.1038/srep39865
Guo XY, Liu DF, Chong K (2018) Cold signaling in plants: Insights into mechanisms and regulation. J Integr Plant Biol 60(9):745–756. https://doi.org/10.1111/jipb.12706
Ha Y, Shang Y, Nam KH (2016) Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. J Exp Bot 67(22):6297–6308. https://doi.org/10.1093/jxb/erw385
Han Y, Han SK, Ban QY, He YH, Jin MJ, Rao JP (2017) Overexpression of persimmon DkXTH1 enhanced tolerance to abiotic stress and delayed fruit softening in transgenic plants. Plant Cell Rep 36(4):583–596. https://doi.org/10.1007/s00299-017-2105-4
Huang XB, Shi HY, Hu ZR, Liu A, Amombo E, Chen L, Fu JM (2017) ABA is involved in regulation of cold stress response in bermudagrass. Front Plant Sci 8:1613. https://doi.org/10.3389/fpls.2017.01613
Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467. https://doi.org/10.1038/nature06148
Janda T, Szalai G, Tari I, Paaldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta. https://doi.org/10.1007/s004250050547
Jia YX, Ding YL, Shi YT, Zhang XY, Gong ZZ, Yang SH (2016) The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol 212(2):345–353. https://doi.org/10.1111/nph.14088
Jin Y, Pan WY, Zheng XF, Cheng X, Liu MM, Ma H, Ge XC (2018) OsERF101, an ERF family transcription factor, regulates drought stress response in reproductive tissues. Plant Mol Biol 98(1–2):51–65. https://doi.org/10.1007/s11103-018-0762-5
Knight H, Zarka DG, Okamoto H, Thomashow ME, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135(3):1710–1717. https://doi.org/10.1104/pp.104.043562
Li H, Ye KY, Shi YT, Cheng JK, Zhang XY, Yang SH (2017) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10(4):545–559. https://doi.org/10.1016/j.molp.2017.01.004
Li QQ, Xu F, Chen Z, Teng ZF, Sun K, Li XC, Yu JY, Zhang GX, Liang Y, Huang XH, Du L, Qian YW, Wang YC, Chu CC, Tang JY (2021) Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nat Plants 7(8):1108–1118. https://doi.org/10.1038/s41477-021-00959-1
Li BB, Fu YS, Li XX, Yin HN, Xi ZM (2022) Brassinosteroids alleviate cadmium phytotoxicity by minimizing oxidative stress in grape seedlings: Toward regulating the ascorbate-glutathione cycle. Sci Hortic. https://doi.org/10.1016/j.scienta.2022.111002
Liu YJ, Jiang HF, Zhao ZG, An LZ (2011) Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana. J Plant Physiol 168(9):853–862. https://doi.org/10.1016/j.jplph.2010.09.020
Liu L, Han T, Liu WJ, Han GQ, Di PC, Yu XY, Yan JW, Zhang AY (2020) Thr420 and Ser454 of ZmCCaMK play a crucial role in brassinosteroid-induced antioxidant defense in maize. Biochem Biophys Res Commun 525(3):537–542. https://doi.org/10.1016/j.bbrc.2020.02.078
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Londo JP, Kovaleski AP, Lillis JA (2018) Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine (Vitis vinifera). Hortic Res 5:10. https://doi.org/10.1038/s41438-018-0020-7
Miao YY, Zhu ZB, Guo QS, Zhu YH, Yang XH, Sun Y (2016) Transcriptome analysis of differentially expressed genes provides insight into stolon formation in tulipa edulis. Front Plant Sci 7:409. https://doi.org/10.3389/fpls.2016.00409
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Ming RH, Zhang Y, Wang Y, Khan M, Dahro B, Liu JH (2021) The JA-responsive MYC2-BADH-like transcriptional regulatory module in Poncirus trifoliata contributes to cold tolerance by modulation of glycine betaine biosynthesis. New Phytol 229(5):2730–2750. https://doi.org/10.1111/nph.17063
Mittler R (2017) ROS are Good. Trends Plant Sci 22(1):11–19. https://doi.org/10.1016/j.tplants.2016.08.002
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):86–96. https://doi.org/10.1016/j.bbagrm.2011.08.004
Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39(5):1140–1160. https://doi.org/10.1111/pce.12726
Northey JGB, Liang S, Jamshed M, Deb S, Foo E, Reid JB, McCourt P, Samuel MA (2016) Farnesylation mediates brassinosteroid biosynthesis to regulate abscisic acid responses. Nat Plants 2(8):16114. https://doi.org/10.1038/nplants.2016.114
Ramirez VE, Poppenberger B (2020) Modes of brassinosteroid activity in cold stress tolerance. Front Plant Sci. https://doi.org/10.3389/fpls.2020.583666
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. https://doi.org/10.1038/ncomms5138
Shi, Y.T., Yang, S.H., 2014. ABA regulation of the cold stress response in plants. In: abscisic acid: metabolism, transport and signaling. Springer, Netherlands, pp. 337–363. https://doi.org/10.1007/978-94-017-9424-4_17.
Straltsova D, Chykun P, Subramaniam S, Sosan A, Kolbanov D, Sokolik A, Demidchik V (2015) Cation channels are involved in brassinosteroid signalling in higher plants. Steroids 97:98–106. https://doi.org/10.1016/j.steroids.2014.10.008
Sun XM, Zhao TT, Gan SH, Ren XD, Fang LC, Karungo SK, Wang Y, Chen L, Li SH, Xin HP (2016) Ethylene positively regulates cold tolerance in grapevine by modulating the expression of ETHYLENE RESPONSE FACTOR 057. Sci Rep 6:24066. https://doi.org/10.1038/srep24066
Sun XM, Zhang LL, Wong DCJ, Wang Y, Zhu ZF, Xu GZ, Wang QF, Li SH, Liang ZC, Xin HP (2019) The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance. Plant J 99(5):988–1002. https://doi.org/10.1111/tpj.14378
Takahashi D, Gorka M, Erban A, Graf A, Kopka J, Zuther E, Hincha DK (2019) Both cold and sub-zero acclimation induce cell wall modification and changes in the extracellular proteome in Arabidopsis thaliana. Sci Rep 9:2289. https://doi.org/10.1038/s41598-019-38688-3
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Tian LX, Li J (2018) The effects of exogenous ABA applied to maize (Zea mays L.) roots on plant responses to chilling stress. Acta Physiol Plant. https://doi.org/10.1007/s11738-018-2655-2
Wang F, Guo ZX, Li HZ, Wang MM, Onac E, Zhou J, Xia XJ, Shi K, Yu JQ, Zhou YH (2016) Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol 170(1):459–471. https://doi.org/10.1104/pp.15.01171
Wang Y, Xin HP, Fan PG, Zhang JS, Liu YB, Dong Y, Wang ZM, Yang YZ, Zhang Q, Ming R, Zhong GY, Li SH, Liang ZC (2021a) The genome of Shanputao (Vitis amurensis) provides a new insight into cold tolerance of grapevine. Plant J 105(6):1495–1506. https://doi.org/10.1111/tpj.15127
Wang ZM, Wong DCJ, Wang Y, Xu GZ, Ren C, Liu YF, Kuang YF, Fan PG, Li SH, Xin HP, Liang ZC (2021b) GRAS-domain transcription factor PAT1 regulates jasmonic acid biosynthesis in grape cold stress response. Plant Physiol 186(3):1660–1678. https://doi.org/10.1093/plphys/kiab142
Wang YT, Jiang QQ, Wang XF, Xi ZM (2022) Brassinosteroid stimulates hydrogen peroxide biosynthesis and reduces the effect of cold stress. J PLANT GROWTH REGUL. https://doi.org/10.1007/s00344-022-10835-7
Xia XJ, Fang PP, Guo X, Qian XJ, Zhou J, Shi K, Zhou YH, Yu JQ (2018) Brassinosteroid-mediated apoplastic H2O2-glutaredoxin 12/14 cascade regulates antioxidant capacity in response to chilling in tomato. Plant Cell Environ 41(5):1052–1064. https://doi.org/10.1111/pce.13052
Xie ZL, Nolan ROR, Jiang H, Tang BY, Zhang MC, Li ZH, Yin YH (2019) The AP2/ERF transcription factor TINY modulates brassinosteroid-regulated plant growth and drought responses in Arabidopsis. Plant Cell 31(8):1788–1806. https://doi.org/10.1105/tpc.18.00918
Zhang AY, Zhang J, Zhang JH, Ye NH, Zhang H, Tan MP, Jiang MY (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52(1):181–192. https://doi.org/10.1093/pcp/pcq187
Zhang LY, Song JN, Lin R, Tang MJ, Shao SJ, Yu JQ, Zhou YH (2022) Tomato SlMYB15 transcription factor targeted by sly-miR156e-3p positively regulates ABA-mediated cold tolerance. J Exp Bot. https://doi.org/10.1093/jxb/erac370
Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, Chen ZX, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65(15):4371–4383. https://doi.org/10.1093/jxb/eru217
Zhou YL, Huo SF, Wang LT, Meng JF, Zhang ZW, Xi ZM (2018) Exogenous 24-epibrassinolide alleviates oxidative damage from copper stress in grape (Vitis vinifera L.) cuttings. Plant Physiol Biochem 130:555–565. https://doi.org/10.1016/j.plaphy.2018.07.029
Funding
This work was supported by the Key R&D Programme Projects of Shaanxi Province of China (2022NY-113) and the China Agriculture Research System for Grape (CARS-29-zp-6).
Author information
Authors and Affiliations
Contributions
ZX designed the experiments and acquired the funding. ZC and YW performed the entire experimental work. SD reviewed and edited the paper. QJ and JZ analyzed the data. YW, BD and SD prepared the manuscript. XW edited the manuscript. The paper has been read and approved by all authors.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest in the submission of this paper, and all authors agree that the manuscript should be published.
Additional information
Communicated by Ben Zhang.
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
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.
About this article
Cite this article
Wang, Y., Ding, S., Chen, Z. et al. Transcriptomic analysis provides insights into the abscisic acid mediates brassinosteroid-induced cold resistance of grapevine (Vitis vinifera L.). Plant Growth Regul 101, 845–860 (2023). https://doi.org/10.1007/s10725-023-01060-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-01060-7