Inhibition of gibberellin accumulation by water deficiency promotes fast and long-term 'drought avoidance' responses in tomato

. 2021 Dec ; 232 (5) : 1985-1998. [epub] 20210927

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34541677

Plants reduce transpiration to avoid dehydration during drought episodes by stomatal closure and inhibition of canopy growth. Previous studies have suggested that low gibberellin (GA) activity promotes these 'drought avoidance' responses. Using genome editing, molecular, physiological and hormone analyses, we examined if drought regulates GA metabolism in tomato (Solanum lycopersicum) guard cells and leaves, and studied how this affects water loss. Water deficiency inhibited the expression of the GA biosynthesis genes GA20 oxidase1 (GA20ox1) and GA20ox2 and induced the GA deactivating gene GA2ox7 in guard cells and leaf tissue, resulting in reduced levels of bioactive GAs. These effects were mediated by abscisic acid-dependent and abscisic acid-independent pathways, and by the transcription factor TINY1. The loss of GA2ox7 attenuated stomatal response to water deficiency and during soil dehydration, ga2ox7 plants closed their stomata later, and wilted faster than wild-type (WT) M82 cv. Mutations in GA20ox1 and GA20ox2, had no effect on stomatal closure, but reduced water loss due to the mutants' smaller canopy areas. The results suggested that drought-induced GA deactivation in guard cells, contributes to stomatal closure at the early stages of soil dehydration, whereas inhibition of GA synthesis in leaves suppresses canopy growth and restricts transpiration area.

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Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP. 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91-94.

Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P. 2008. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology 18: 656-660.

Balcke GU, Handrick V, Bergau N, Fichtner M, Henning A, Stellmach H, Tissier A, Hause B, Frolov A. 2012. An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8: 47.

Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP, Hao Y, Yifhar T, Yasuor H, Zouine M, Bouzayen M et al. 2016. AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genetics 12: e1005903.

Chen S, Wang X, Zhang L, Lin S, Liu D, Wang Q, Cai S, El Tanbouly R, Gan L, Wu H et al. 2016. Identification and characterization of tomato gibberellin 2-oxidases (GA2oxs) and effects of fruit-specific SlGA2ox1 overexpression on fruit and seed growth and development. Horticultural Research 3: 16059.

Colebrook EH, Thomas SG, Phillips AL, Hedden P. 2014. The role of gibberellin signalling in plant responses to abiotic stress. Journal of Experimental Biology 217: 67-75.

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61: 651-679.

Daviere JM, Achard P. 2013. Gibberellin signaling in plants. Development 140: 1147-1151.

Eziz A, Yan Z, Tian D, Han W, Tang Z, Fang J. 2017. Drought effect on plant biomass allocation: a meta-analysis. Ecology and Evolution 7: 11002-11010.

Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S et al. 2017. Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8: 1147.

Fukazawa J, Mori M, Watanabe S, Miyamoto C, Ito T, Takahashi Y. 2017. DELLA-GAF1 complex is a main component in gibberellin feedback regulation of GA20 oxidase 2. Plant Physiology 175: 1395-1406.

Geisler M, Nadeau J, Sack FD. 2000. Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12: 2075-2086.

Gupta A, Rico Medina A, Cano Delgado AI. 2020. The physiology of plant responses to drought. Science 386: 266-269.

Halperin O, Gebremedhin A, Wallach R, Moshelion M. 2017. High-throughput physiological phenotyping and screening system for the characterization of plant-environment interactions. The Plant Journal 4: 839-850.

Hauvermale AL, Ariizumi T, Steber CM. 2012. Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiology 160: 83-92.

Hedden P. 2020. The current status of research on gibberellin biosynthesis. Plant & Cell Physiology 61: 1832-1849.

Illouz Eliaz N, Nissan I, Nir I, Ramon U, Shohat H, Weiss D. 2020. Mutations in the tomato gibberellin receptors suppress xylem proliferation and reduce water loss under water-deficit conditions. Journal of Experimental Botany 71: 3603-3612.

Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi-Tanaka M, Matsuoka M, Suzuki K et al. 2009. Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant & Cell Physiology 50: 1201-1214.

Kooyers NJ. 2015. The evolution of drought escape and avoidance in natural herbaceous populations. Plant Science 234: 155-162.

Lata C, Prasad M. 2011. Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany 62: 4731-4748.

Li C, Zheng L, Wang X, Hu Z, Zheng Y, Chen Q, Hao X, Xiao X, Wang X, Wang G et al. 2019. Comprehensive expression analysis of Arabidopsis GA2-oxidase genes and their functional insights. Plant Science 285: 1-13.

Li J, Sima W, Ouyang BO, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y et al. 2012. Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. Journal of Experimental Botany 63: 695-709.

Li R, Sun S, Wang H, Wang K, Yu H, Zhou Z, Xin P, Chu J, Zhao T, Wang H et al. 2020. FIS1 encodes a GA2-oxidase that regulates fruit firmness in tomato. Nature Communications 11: 5844.

Locascio A, Blázquez MA, Alabadí D. 2013. Genomic analysis of DELLA protein activity. Plant & Cell Physiology 54: 1229-1237.

Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K. 2008. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. The Plant Journal 56: 613-626.

Mao L, Deng M, Jiang S, Zhu H, Yang Z, Yue Y, Zhao K. 2020. Characterization of the DREBA4-type transcription factor (SlDREBA4), which contributes to heat tolerance in tomatoes. Frontiers in Plant Science 11: 554520.

McCormick S. 1991. Transformation of tomato with Agrobacterium tumefaciens. Plant Tissue Culture Manual B6: 1-9.

Middleton AM, Ubeda-Tomas S, Griffiths J, Holman T, Hedden P, Thomas SG, Phillips AL, Holdsworth MJ, Bennett MJ, King JR et al. 2012. Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proceedings of the National Academy of Sciences, USA 109: 7571-7576.

Nakano T, Suzuki K, Fujimura T, Shinshi H. 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiology 140: 411-432.

Nelissen H, Sun X-H, Rymen B, Jikumaru Y, Kojima M, Takebayashi Y, Abbeloos R, Demuynck K, Storme V, Vuylsteke M et al. 2018. The reduction in maize leaf growth under mild drought affects the transition between cell division and cell expansion and cannot be restored by elevated gibberellic acid levels. Plant Biotechnology Journal 16: 615-627.

Nir I, Moshelion M, Weiss D. 2014. The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant, Cell & Environment 37: 113-123.

Nir I, Shohat H, Panizel I, Olszewski N, Aharoni A, Weiss D. 2017. The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. Plant Cell 29: 3186-3197.

Omena Garcia R, Martins A, Medeiros D, Vallarino J, Ribeiro D, Fernie A, Araujo W, Nunes NA. 2019. Growth and metabolic adjustments in response to gibberellin deficiency in drought stressed tomato plants. Environmental and Experimental Botany 159: 95-107.

Pattison RJ, Csukasi F, Zheng Y, Fei Z, Van Der Knaap E, Catala C. 2015. Comprehensive tissue-specific transcriptome analysis reveals distinct regulatory programs during early tomato fruit development. Plant Physiology 168: 1684-1701.

Rittenberg D, Foster GL. 1940. A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. Journal of Biological Chemistry 133: 737-744.

Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi SK. 2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold- inducible gene expression. Biochemical and Biophysical Research Communications 290: 998-1009.

Schrager Lavelle A, Gath NN, Devisetty UK, Carrera E, Lopez Diaz I, Blazquez MA, Maloof JN. 2019. The role of a class III gibberellin 2-oxidase in tomato internode elongation. The Plant Journal 97: 603-615.

Shohat H, Illouz Eliaz N, Kanno Y, Seo M, Weiss D. 2020. The tomato DELLA protein PROCERA promotes abscisic acid responses in guard cells by upregulating an abscisic acid transporter. Plant Physiology 184: 518-528.

Skirycz A, Inze D. 2010. More from less: plant growth under limited water. Current Opinion in Biotechnology 21: 197-203.

Tardieu F, Simonneau T, Muller B. 2018. The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annual Review of Plant Biology 69: 733-759.

Tuna AL, Kaya C, Dikilitas M, Higgs D. 2008. The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environmental and Experimental Botany 62: 1-9.

Urbanova T, Tarkowska D, Novak O, Hedden P, Strnad M. 2013. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112: 85-94.

Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. 2011. A modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6: e16765.

Xie Z, Nolan T, Jiang H, Tang B, Zhang M, Li Z, Yin Y. 2019. The AP2/ERF transcription factor TINY modulates brassinosteroid-regulated plant growth and drought responses in Arabidopsis. Plant Cell 31: 1788-1806.

Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59: 225-251.

Zawaski C, Busov VB. 2014. Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS ONE 9: e86217.

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