ERF54 regulates cold tolerance in Rosa multiflora through DREB/COR signalling pathways.
DREB/COR signalling pathway
RmDREB1E
RmERF54
Rosa multiflora
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
02 Jan 2024
02 Jan 2024
Historique:
revised:
10
12
2023
received:
25
07
2023
accepted:
15
12
2023
medline:
2
1
2024
pubmed:
2
1
2024
entrez:
2
1
2024
Statut:
aheadofprint
Résumé
Ethylene-responsive factors (ERFs) participate in a wide range of physiological and biological processes. However, many of the functions of ERFs in cold stress responses remain unclear. We, therefore, characterised the cold responses of RmERF54 in Rosa multiflora, a rose-related cold-tolerant species. Overexpression of RmERF54, which is a nuclear transcription factor, increases the cold resistance of transgenic tobacco and rose somatic embryos. In contrast, virus-induced gene silencing (VIGS) of RmERF54 increased cold susceptibility of R. multiflora. The overexpression of RmERF54 resulted in extensive transcriptional reprogramming of stress response and antioxidant enzyme systems. Of these, the levels of transcripts encoding the PODP7 peroxidase and the cold-related COR47 protein showed the largest increases in the somatic embryos with ectopic expression of RmERF54. RmERF54 binds to the promoters of the RmPODP7 and RmCOR47 genes and activates expression. RmERF54-overexpressing lines had higher antioxidant enzyme activities and considerably lower levels of reactive oxygen species. Opposite effects on these parameters were observed in the VIGS plants. RmERF54 was identified as a target of Dehydration-Responsive-Element-Binding factor (RmDREB1E). Taken together, provide new information concerning the molecular mechanisms by which RmERF54 regulates cold tolerance.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Ahamed, A., Murai-Hatano, M., Ishikawa-Sakurai, J., Hayashi, H., Kawamura, Y. & Uemura, M. (2012) Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant & Cell Physiology, 53(8), 1445-1456.
Akhtar, M., Jaiswal, A., Taj, G., Jaiswal, J.P., Qureshi, M.I. & Singh, N.K. (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. Journal of Genetics, 91(3), 385-395.
Allen, M.D., Yamasaki, K., Ohme-Takagi, M., Tateno, M. & Suzuki, M. (1998) A novel mode of DNA recognition by a β-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. The EMBO Journal, 17(18), 5484-5496.
Bui, L.T., Giuntoli, B., Kosmacz, M., Parlanti, S. & Licausi, F. (2015) Constitutively expressed ERF-VII transcription factors redundantly activate the core anaerobic response in Arabidopsis thaliana. Plant Science, 236, 37-43.
Chen, L., Chen, Y., Shen, Y., Xing, W., Cui, Y. & Luo, P. (2023) RhMYB1 and RhMYB123 form a positive feedback loop to regulate the proanthocyanidin biosynthesis in rose. Industrial Crops and Products, 196, 116492.
Cheng, M.C., Liao, P.M., Kuo, W.W. & Lin, T.P. (2013) The arabidopsis ethylene response factor1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiology, 162(3), 1566-1582.
Choudhury, F.K., Rivero, R.M., Blumwald, E. & Mittler, R. (2017) Reactive oxygen species, abiotic stress and stress combination. The Plant Journal, 90(5), 856-867.
Dahro, B., Wang, Y., Khan, M., Zhang, Y., Fang, T., Ming, R. et al. (2022) Two AT-Hook proteins regulate A/NINV7 expression to modulate sucrose catabolism for cold tolerance in Poncirus trifoliata. New Phytologist, 235(6), 2331-2349.
Dai, W., Wang, M., Gong, X. & Liu, J.H. (2018) The transcription factor FcWRKY40 of Fortunella crassifolia functions positively in salt tolerance through modulation of ion homeostasis and proline biosynthesis by directly regulating SOS2 and P5CS1 homologs. New Phytologist, 219(3), 972-989.
Ding, Y., Shi, Y. & Yang, S. (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytologist, 222(4), 1690-1704.
Dubois, A., Carrere, S., Raymond, O., Pouvreau, B., Cottret, L., Roccia, A. et al. (2012) Transcriptome database resource and gene expression atlas for the rose. BMC Genomics, 13, 638.
Gao, J., Dou, T., He, W., Sheng, O., Bi, F., Deng, G. et al. (2021) MaMAPK3-MaICE1-MaPODP7 pathway, a positive regulator of cold tolerance in banana. BMC Plant Biology, 21(1), 97.
Geng, J. & Liu, J.H. (2018) The transcription factor CsbHLH18 of sweet orange functions in modulation of cold tolerance and homeostasis of reactive oxygen species by regulating the antioxidant gene. Journal of Experimental Botany, 69(10), 2677-2692.
Gibbs, D.J., Conde, J.V., Berckhan, S., Prasad, G., Mendiondo, G.M. & Holdsworth, M.J. (2015) Group VII ethylene response factors coordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiology, 169(1), 23-31.
Gill, S.S. & Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930.
Gong, X., Zhang, J., Hu, J., Wang, W., Wu, H., Zhang, Q. et al. (2015) FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant, Cell & Environment, 38(11), 2248-2262.
Guy, C.L., Anderson, J.V., Haskell, D.W. & Li, Q.B. (1994) Caps, cors, dehydrins, and molecular chaperones: their relationship with low temperature responses in spinach. Springer Berlin Heidelbery, 86, 479-499.
Huang, X.S., Wang, W., Zhang, Q. & Liu, J.H. (2013) A basic helix-loop-helix transcription factor, PtrbHLH, of poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiology, 162(2), 1178-1194.
Ji, C.Y., Jin, R., Xu, Z., Kim, H.S., Lee, C.J., Kang, L. et al. (2017) Overexpression of Arabidopsis P3B increases heat and low temperature stress tolerance in transgenic sweet potato. BMC Plant Biology, 17(1), 139.
Jia, Y., Ding, Y., Shi, Y., Zhang, X., Gong, Z. & Yang, S. (2016) The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytologist, 212(2), 345-353.
Khan, M., Hu, J., Dahro, B., Ming, R., Zhang, Y., Wang, Y. et al. (2021) ERF108 from Poncirus trifoliata (L.) Raf. functions in cold tolerance by modulating raffinose synthesis through transcriptional regulation of PtrRafS. The Plant Journal, 108(3), 705-724.
Lee, H.G. & Seo, P.J. (2015) The MYB96-HHP module integrates cold and abscisic acid signaling to activate the CBF-COR pathway in Arabidopsis. The Plant Journal, 82(6), 962-977.
Li, A.L., Zhu, Y.F., Tan, X.M., Wang, X., Wei, B., Guo, H.Z. et al. (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Molecular Biology, 66, 429-443.
Li, H., Ye, K., Shi, Y., Cheng, J., Zhang, X. & Yang, S. (2017) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Molecular Plant, 10(4), 545-559.
Li, X.L., Meng, D., Li, M.J., Zhou, J., Yang, Y.Z., Zhou, B.B. et al. (2023) Transcription factors MhDREB2A/MhZAT10 play a role in drought and cold stress response crosstalk in apple. Plant Physiology, 192, 2203-2220.
Li, Z., Chen, W., Zhang, C., Du, C., Shao, G., Cui, Y. et al. (2019) RcMYBPA2 of Rosa chinensis functions in proanthocyanidin biosynthesis and enhances abiotic stress tolerance in transgenic tobacco. Plant Cell, Tissue and Organ Culture (PCTOC), 137, 441-454.
Liorzou, M., Pernet, A., Li, S., Chastellier, A., Thouroude, T., Michel, G. et al. (2016) Nineteenth century French rose (Rosa sp.) germplasm shows a shift over time from a European to an Asian genetic background. Journal of Experimental Botany, 67(15), 4711-4725.
Liu, X., Bulley, S.M., Varkonyi-Gasic, E., Zhong, C. & Li, D. (2023) Kiwifruit bZIP transcription factor AcePosF21 elicits ascorbic acid biosynthesis during cold stress. Plant Physiology, 192(2), 982-999.
Liu, X., Chen, L., Shi, W., Xu, X., Li, Z., Liu, T. et al. (2021) Comparative transcriptome reveals distinct starch-sugar interconversion patterns in potato genotypes contrasting for cold-induced sweetening capacity. Food Chemistry, 334, 127550.
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402-408.
Lou, Q., Guo, H., Li, J., Han, S., Khan, N.U., Gu, Y. et al. (2022) Cold-adaptive evolution at the reproductive stage in Geng/japonica subspecies reveals the role of OsMAPK3 and OsLEA9. The Plant Journal, 111(4), 1032-1051.
Lu, X., Zhang, L., Zhang, F., Jiang, W., Shen, Q., Zhang, L. et al. (2013) AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytologist, 198(4), 1191-1202.
Luo, P., Chen, L., Chen, Y., Shen, Y. & Cui, Y. (2022) RmZAT10, a novel Cys2/His2 zinc finger transcription factor of Rosa multiflora, functions in cold tolerance through modulation of proline biosynthesis and ROS homeostasis. Environmental and Experimental Botany, 198, 104845.
Luo, P., Li, Z., Chen, W., Xing, W., Yang, J. & Cui, Y. (2020) Overexpression of RmICE1, a bHLH transcription factor from Rosa multiflora, enhances cold tolerance via modulating ROS levels and activating the expression of stress-responsive genes. Environmental and Experimental Botany, 178, 104160.
Mansour, M.M.F. & Ali, E.F. (2017) Evaluation of proline functions in saline conditions. Phytochemistry, 140, 52-68.
Mehrotra, S., Verma, S., Kumar, S., Kumari, S. & Mishra, B.N. (2020) Transcriptional regulation and signalling of cold stress response in plants: an overview of current understanding. Environmental and Experimental Botany, 180, 104243.
Mizoi, J., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1819(2), 86-96.
Nadarajah, K.K. (2020) ROS homeostasis in abiotic stress tolerance in plants. International Journal of Molecular Sciences, 21(15), 5208.
Nakamura, N., Hirakawa, H., Sato, S., Otagaki, S., Matsumoto, S., Tabata, S. et al. (2017) Genome structure of rosa multiflora, a wild ancestor of cultivated roses. DNA Research, 25(2), 113-121.
Ning, G., Xiao, X., Lv, H., Li, X., Zuo, Y. & Bao, M. (2012) Shortening tobacco life-cycle accelerates functional gene identification in genomic research. Plant Biology, 14(6), 934-943.
Park, S., Lee, C.M., Doherty, C.J., Gilmour, S.J., Kim, Y. & Thomashow, M.F. (2015) Regulation of the arabidopsis CBF regulon by a complex low-temperature regulatory network. The Plant Journal, 82(2), 193-207.
Peng, T., Zhu, X., Duan, N. & Liu, J.H. (2014) PtrBAM1, a β-amylase-coding gene of Poncirus trifoliata, is a CBF regulon member with function in cold tolerance by modulating soluble sugar levels. Plant, Cell & Environment, 37(12), 2754-2767.
Puhakainen, T., Hess, M.W., Mäkelä, P., Svensson, J., Heino, P. & Palva, E.T. (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Molecular Biology, 54(5), 743-753.
Rashotte, A.M., Mason, M.G., Hutchison, C.E., Ferreira, F.J., Schaller, G.E. & Kieber, J.J. (2006) A subset of arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proceedings of the National Academy of Sciences, 103(29), 11081-11085.
Tian, J., Pei, H., Zhang, S., Chen, J., Chen, W., Yang, R. et al. (2014) TRV-GFP: a modified tobacco rattle virus vector for efficient and visualizable analysis of gene function. Journal of Experimental Botany, 65(1), 311-322.
Tian, Z., He, Q., Wang, H., Liu, Y., Zhang, Y., Shao, F. et al. (2015) The potato ERF transcription factor StERF3 negatively regulates resistance to Phytophthora infestans and salt tolerance in potato. Plant and Cell Physiology, 56(5), 992-1005.
Vogel, J.T., Zarka, D.G., Van Buskirk, H.A., Fowler, S.G. & Thomashow, M.F. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal, 41(2), 195-211.
Wang, J., Sun, P.P., Chen, C.L., Wang, Y., Fu, X.Z. & Liu, J.H. (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. Journal of Experimental Botany, 62(8), 2899-2914.
Wang, M., Dai, W., Du, J., Ming, R., Dahro, B. & Liu, J.H. (2019) ERF109 of trifoliate orange (Poncirus trifoliata (L.) raf.) contributes to cold tolerance by directly regulating expression of prx1 involved in antioxidative process. Plant Biotechnology Journal, 17(7), 1316-1332.
Wang, X., Han, H., Yan, J., Chen, F. & Wei, W. (2015) A new AP2/ERF transcription factor from the oil plant Jatropha curcas confers salt and drought tolerance to transgenic tobacco. Applied Biochemistry and Biotechnology, 176(2), 582-597.
Wu, H., Fu, B., Sun, P., Xiao, C. & Liu, J.H. (2016) A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance. Plant Physiology, 172(3), 1532-1547.
Xi, J., Xu, P. & Xiang, C.B. (2012) Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana. The Plant Journal, 69(5), 782-791.
Xing, C., Liu, Y., Zhao, L., Zhang, S. & Huang, X. (2019) A novel MYB transcription factor regulates ascorbic acid synthesis and affects cold tolerance. Plant, Cell & Environment, 42(3), 832-845.
Xu, W., Yu, Y., Zhou, Q., Ding, J., Dai, L., Xie, X. et al. (2011) Expression pattern, genomic structure, and promoter analysis of the gene encoding stilbene synthase from Chinese wild Vitis pseudoreticulata. Journal of Experimental Botany, 62(8), 2745-2761.
Xu, Z.S., Xia, L.Q., Chen, M., Cheng, X.G., Zhang, R.Y., Li, L.C. et al. (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Molecular Biology, 65(6), 719-732.
Yang, G., Yu, Z., Gao, L. & Zheng, C. (2019) SnRK2s at the crossroads of growth and stress responses. Trends in Plant Science, 24(8), 672-676.
Yang, Y. & Guo, Y. (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist, 217(2), 523-539.
Yu, D., Zhang, L., Zhao, K., Niu, R., Zhai, H. & Zhang, J. (2017) VaERD15, a transcription factor gene associated with cold-tolerance in Chinese Wild Vitis amurensis. Frontiers in Plant Science, 8, 297.
Zhang, X., Zhang, J., Zhang, W., Yang, T., Xiong, Y. & Che, D. (2016) Transcriptome sequencing and de novo analysis of rosa multiflora under cold stress. Acta Physiologiae Plantarum, 38, 164.
Zhang, Z., Wang, J., Zhang, R. & Huang, R. (2012) The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. The Plant Journal, 71(2), 273-287.
Zhao, C., Zhang, Z., Xie, S., Si, T., Li, Y. & Zhu, J.K. (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in arabidopsis. Plant Physiology, 171(4), 2744-2759.
Zhao, L., Liu, F., Xu, W., Di, C., Zhou, S., Xue, Y. et al. (2009) Increased expression of OsSPX1 enhances cold/subfreezing tolerance in tobacco and Arabidopsis thaliana. Plant Biotechnology Journal, 7(6), 550-561.
Zhou, M.L., Ma, J.T., Pang, J.F., Zhang, Z.L., Tang, Y.X. & Wu, Y.M. (2010) Regulation of plant stress response by dehydration responsive element binding (DREB) transcription factors. African Journal of Biotechnology, 9(54), 9255-9269.
Zhu, J.K. (2016) Abiotic stress signaling and responses in plants. Cell, 167(2), 313-324.