Abstract
The Arabidopsis RRTF1 promoter is transiently activated by salt stress over 6 hours, before it quickly reverts to pre-stress levels, even if the salt stress continues. This allows the short-term expression of components that, although initially beneficial to the plant, will have negative effects if continuously produced at high levels. We therefore tested the application of the RRTF1 promoter to drive the activity of the SHO gene which is responsible for the production of certain cytokinin derivatives in plants. Transgenic plants with RRTF1 promoter-controlled SHO activity showed significant improvements in seed germination and survival rates under salt stress without any phenotypic alterations. In addition, the transgenic seedlings displayed significantly improved recovery rates from salt stress compared with the wild type. These observations support the use of the RRTF1 promoter for controlled cytokinin production alleviating the negative impact of salt stress without affecting plant morphology.
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13 November 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11105-021-01322-6
References
Albacete A, Ghanem ME, Martínez-Andújar C et al (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131. https://doi.org/10.1093/jxb/ern251
Balazadeh S, Wu A, Mueller-Roeber B (2010) Salt-triggered expression of the ANAC092-dependent senescence regulon in Arabidopsis thaliana. Plant Signal Behav 5:733–735. https://doi.org/10.4161/psb.5.6.11694
Bartrina I, Otto E, Strnad M et al (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80. https://doi.org/10.1105/tpc.110.079079
Bassel GW, Lan H, Glaab E et al (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci U S A 108:9709–9714. https://doi.org/10.1073/pnas.1100958108
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313X.1998.00343.x
De Buck S, Windels P, De Loose M, Depicker A (2004) Single-copy T-DNAs integrated at different positions in the Arabidopsis genome display uniform and comparable β-glucuronidase accumulation levels. Cell Mol Life Sci 61:2632–2645. https://doi.org/10.1007/s00018-004-4284-8
Fan Y, Yin X, Xie Q et al (2019) Co-expression of SpSOS1 and SpAHA1 in transgenic Arabidopsis plants improves salinity tolerance. BMC Plant Biol 19:74. https://doi.org/10.1186/s12870-019-1680-7
Ganguly M, Roychoudhury A, Sarkar SN et al (2011) Inducibility of three salinity/abscisic acid-regulated promoters in transgenic rice with gusA reporter gene. Plant Cell Rep 30:1617–1625. https://doi.org/10.1007/s00299-011-1072-4
Ghanem ME, Albacete A, Martinez-Andujar C et al (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050. https://doi.org/10.1093/jxb/ern153
Ha S, Vankova R, Yamaguchi-Shinozaki K et al (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179
Hellens RP, Anne Edwards E, Leyland NR et al (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832. https://doi.org/10.1023/A:1006496308160
Hernandez-Garcia CM, Bouchard RA, Rushton PJ et al (2010) High level transgenic expression of soybean (Glycine max) GmERF and Gmubi gene promoters isolated by a novel promoter analysis pipeline. BMC Plant Biol 10. https://doi.org/10.1186/1471-2229-10-237
Hönig M, Plíhalová L, Husičková A et al (2018) Role of cytokinins in senescence, antioxidant defence and photosynthesis. Int J Mol Sci 19
Huynh LN, VanToai T, Streeter J, Banowetz G (2005) Regulation of flooding tolerance of SAG12:ipt Arabidopsis plants by cytokinin. J Exp Bot 56:1397–1407. https://doi.org/10.1093/jxb/eri141
Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10
Kasuga M, Liu Q, Miura S et al (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291. https://doi.org/10.1038/7036
Klára H, Petr H (2020) New insights into the metabolism and role of cytokinin N-glucosides in plants. Front Plant Sci 11:741. https://doi.org/10.3389/fpls.2020.00741
Kurakawa T, Ueda N, Maekawa M et al (2007) Direct control of shoot meristem activity by a cytokinin- activating enzyme. Nature 445:652–655. https://doi.org/10.1038/nature05504
Kuroha T (2002) A trans-zeatin riboside in root xylem sap negatively regulates adventitious root formation on cucumber hypocotyls. J Exp Bot 53:2193–2200. https://doi.org/10.1093/jxb/erf077
Li XG, Su YH, Zhao XY et al (2010) Cytokinin overproduction-caused alteration of flower development is partially mediated by CUC2 and CUC3 in Arabidopsis. Gene 450:109–120. https://doi.org/10.1016/j.gene.2009.11.003
Liu QL, Xu KD, Zhao LJ et al (2011) Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco. Biotechnol Lett 33:2073–2082. https://doi.org/10.1007/s10529-011-0659-8
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −∆∆CT method. Methods 25:402–408
Merewitz EB, Gianfagna T, Huang B (2010) Effects of SAG12-ipt and HSP18.2-ipt expression on cytokinin production, root growth, and leaf senescence in creeping bentgrass exposed to drought stress. J Am Soc Hortic Sci 135:230–239. https://doi.org/10.21273/jashs.135.3.230
Nishiyama R, Watanabe Y, Fujita Y et al (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183. https://doi.org/10.1105/tpc.111.087395
Peach C, Velten J (1991) Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol Biol 17:49–60. https://doi.org/10.1007/BF00036805
Qiu W, Liu M, Qiao G et al (2012) An isopentyl transferase gene driven by the stress-inducible rd29A promoter improves salinity stress tolerance in transgenic tobacco. Plant Mol Biol Report 30:519–528. https://doi.org/10.1007/s11105-011-0337-y
Rivero RM, Kojima M, Gepstein A et al (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci U S A 104:19631–19636. https://doi.org/10.1073/pnas.0709453104
Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540. https://doi.org/10.1104/pp.109.139378
Sakakibara H (2006) CYTOKININS: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. https://doi.org/10.1146/annurev.arplant.57.032905.105231
Shan Y, Zhao P, Liu Z et al (2019) An isopentyl transferase gene driven by the senescence-inducible SAG12 promoter improves salinity stress tolerance in cotton. J Cott Res 2. https://doi.org/10.1186/s42397-019-0032-3
Soliman ERS, Meyer P (2019) Responsiveness and adaptation to salt stress of the REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) gene are controlled by its promoter. Mol Biotechnol 61:254–260. https://doi.org/10.1007/s12033-019-00155-9
Wang Y, Li L, Ye T et al (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J 68:249–261. https://doi.org/10.1111/j.1365-313X.2011.04683.x
Witcombe JR, Hollington PA, Howarth CJ et al (2008) Breeding for abiotic stresses for sustainable agriculture. Philos Trans R Soc B Biol Sci 363:703–716
Zhang H, Irving LJ, McGill C et al (2010) The effects of salinity and osmotic stress on barley germination rate: Sodium as an osmotic regulator. Ann Bot 106:1027–1035. https://doi.org/10.1093/aob/mcq204
Zhang YM, Liu ZH, Wen ZY et al (2012) The vacuolar Na +H + antiport gene TaNHX2 confers salt tolerance on transgenic alfalfa (Medicago sativa). Funct Plant Biol 39:708–716. https://doi.org/10.1071/FP12095
Zubko E, Adams CJ, Macháèková I et al (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808. https://doi.org/10.1046/j.1365-313x.2002.01256.x
Zubko E, Macháčková I, Malbeck J, Meyer P (2005) Modification of cytokinin levels in potato via expression of the Petunia hybrida Sho gene. Transgenic Res 14:615–618. https://doi.org/10.1007/s11248-005-2029-6
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• RRTF1 promoter provides conditional salt stress expression of SHO gene
• RRTF1pro::SHO transgenic lines display significant salt tolerance response
• RRTF1pro::SHO transgenic lines show no plant developmental alternation to wild type
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Soliman, E.R.S., Meyer, P. Expression of the SHO Gene Under Control of a Stress-Specific Promoter RRTF1 Improves Salt Tolerance in Arabidopsis. Plant Mol Biol Rep 39, 617–625 (2021). https://doi.org/10.1007/s11105-020-01275-2
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DOI: https://doi.org/10.1007/s11105-020-01275-2