Special Issue:
园艺-分子生物合辑Horticulture — Genetics · Breeding
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Overexpression of MdMIPS1 enhances drought tolerance and water-use efficiency in apple |
HU Ling-yu, YUE Hong, ZHANG Jing-yun, LI Yang-tian-su, GONG Xiao-qing, ZHOU Kun, MA Feng-wang |
State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, P.R.China |
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摘要
肌醇及其衍生物在调节植物非生物逆境耐受性过程中发挥着重要作用。肌醇-1-磷酸合成酶MIPS(myo-inositol-1-phosphate synthase)是肌醇生物合成限速酶,本研究发现,在苹果植株中过表达MdMIPS1基因不仅能提高肌醇生物合成,而且还能提高植株耐旱性。研究表明,肌醇可能通过提高渗透保护剂(如葡萄糖、蔗糖和脯氨酸)的积累和改善活性氧清除相关抗氧化酶活性,提高苹果干旱耐受性。此外,在模拟黄土高原土壤环境的长期中度水分亏缺条件下,MdMIPS1过表达苹果植株表现为水分利用效率显著提高,这可能主要与肌醇生物合成增加协同调节植株渗透平衡和气孔孔径密切相关。综上所述,本研究揭示了苹果MdMIPS1介导的肌醇生物合成在植株耐旱性和水分利用效率调控过程中的积极作用。
Abstract Myo-inositol and its derivatives play important roles in the tolerance of higher plants to abiotic stresses, and myo-inositol-1-phosphate synthase (MIPS) is the rate-limiting enzyme in myo-inositol biosynthesis. In this study, we found that increased myo-inositol biosynthesis enhanced drought tolerance in MdMIPS1-overexpressing apple lines under short-term progressive drought stress. The effect of myo-inositol appeared to be mediated by the increased accumulation of osmoprotectants such as glucose, sucrose, and proline, and by the increased activities of antioxidant enzymes that eliminate reactive oxygen species. Moreover, enhanced water-use efficiency (WUE) was observed in MdMIPS1-overexpressing apple lines under long-term moderate water deficit conditions that mimicked the water availability in the soil of the Loess Plateau. Enhanced WUE may have been associated with the synergistic regulation of osmotic balance and stomatal aperture mediated by increased myo-inositol biosynthesis. Taken together, our findings shed light on the positive effects of MdMIPS1-mediated myo-inositol biosynthesis on drought tolerance and WUE in apple.
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Received: 26 May 2020
Accepted: 23 August 2021
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Fund: This work was supported by the National Key Research and Development Program of China (2018YFD1000303) and the China Agriculture Research System of MOF and MARA (CARS-27). |
About author: Correspondence MA Feng-wang, Tel: +86-29-87082648, E-mail: fwm64@sina.com, fwm64@nwsuaf.edu.cn |
Cite this article:
HU Ling-yu, YUE Hong, ZHANG Jing-yun, LI Yang-tian-su, GONG Xiao-qing, ZHOU Kun, MA Feng-wang.
2022.
Overexpression of MdMIPS1 enhances drought tolerance and water-use efficiency in apple. Journal of Integrative Agriculture, 21(7): 1968-1981.
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Ahn C, Park U, Park P B. 2011. Increased salt and drought tolerance by D-ononitol production in transgenic Arabidopsis thaliana. Biochemical and Biophysical Research Communications, 415, 669–674.
Bartels D, Sunkar R. 2005. Drought and salt tolerance in plants. Critical Reviews in Plant Sciences, 24, 23–58.
Blum A. 2017. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell & Environment, 40, 4–10.
Carvalho D M H C. 2008. Drought stress and reactive oxygen species production, scavenging and signaling. Plant Signaling & Behavior, 3, 156–165.
Chaves M M, Maroco J P, Pereira J S. 2003. Understanding plant responses to drought - from genes to the whole plant. Functional Plant Biology, 30, 239–264.
Chen T H, Murata N. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology, 5, 250–257.
Dai W S, Wang M, Gong X Q, 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, 972–989.
Deng C N, Zhang D Y, Pan X L, Chang F Q, Wang S Z. 2013. Toxic effects of mercury on PSI and PSII activities, membrane potential and transthylakoid proton gradient in Microsorium pteropus. Journal of Photochemistry and Photobiology (B: Biology), 127, 1–7.
Donahue J L, Alford S R, Torabinejad J, Kerwin R E, Nourbakhsh A, Ray W K, Hernick M, Huang X, Lyons B M, Hein P P, Gillaspy G E. 2010. The Arabidopsis thaliana myo-inositol-1-phosphate synthase1 gene is required for myo-inositol synthesis and suppression of cell death. The Plant Cell, 22, 888–903.
Duan B, Yang Y, Lu Y, Korpelainen H, Berninger F, Li C. 2007. Interactions between drought stress, ABA and genotypes in Picea asperata. Journal of Experimental Botany, 58, 3025–3036.
Dunn J, Hunt L, Afsharinafar M, Meselmani M A, Mitchell A, Howells R, Wallington E, Fleming A J, Gray J E. 2019. Reduced stomatal density in bread wheat leads to increased water-use efficiency. Journal of Experimental Botany, 70, 4737–4748.
Ehdaie B. 1995. Variation in water-use efficiency and its components in wheat: II. Pot and field experiments. Crop Science, 35, 294–299.
Fang Y J, Xiong L Z. 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences, 72, 673–689.
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S M A. 2009. Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development, 29, 185–212.
Filippou P, Bouchagier P, Skotti E, Fotopoulos V. 2014. Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environmental and Experimental Botany, 97, 1–10.
Foyer C H, Fletcher J M. 2001. Plant antioxidants: Colour me healthy. Biologist, 48, 115–120.
Franks P J, Farquhar G D. 1999. A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant Cell & Environment, 22, 1337–1349.
Galvani A. 2007. The challenge of the food sufficiency through salt tolerant crops. Reviews in Environmental and Science and Biotechnology, 6, 3–16.
Gill S S, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.
Goswami L, Sengupta S, Mukherjee S, Ray S, Mukherjee R, Majumder A L. 2014. Targeted expression of L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka confers multiple stress tolerance in transgenic crop plants. Journal of Plant Biochemistry and Biotechnology, 23, 316–330.
Gupta A, Rico-Medina A, Caño-Delgado A I. 2020. The physiology of plant responses to drought. Science, 368, 266–269.
Harrison E L, Cubas L A, Gray J E, Hepworth C. 2020. The influence of stomatal morphology and distribution on photosynthetic gas exchange. The Plant Journal, 101, 768–779.
Hu L Y, Zhou K, Li Y T S, Chen X F, Liu B B, Li C Y, Gong X Q, Ma F W. 2018. Exogenous myo-inositol alleviates salinity-induced stress in Malus hupehensis Rehd. Plant Physiology and Biochemistry, 133, 116–126.
Hu L Y, Zhou K, Liu Y, Yang S L, Zhang J Y, Gong X Q, Ma F W. 2020a. Overexpression of MdMIPS1 enhances salt tolerance by improving osmosis, ion balance, and antioxidant activity in transgenic apple. Plant Science, 301, 110654.
Hu L Y, Zhou K, Ren G J, Yang S L, Liu Y, Zhang Z J, Li Y T S, Gong X Q, Ma F W. 2020b. Myo-inositol mediates reactive oxygen species-induced programmed cell death via salicylic acid- and ethylene-dependent pathways in apple. Horticulture Research, 7, 138.
Ismail A, Takeda S, Nick P. 2014. Life and death under salt stress: Same players, different timing? Journal of Experimental Botany, 65, 2963–2979.
Jaleel C A, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R. 2007. Induction of drought stress tolerance by ketoconazole in Catharanthus roseus is mediated by enhanced antioxidant potentials and secondary metabolite accumulation. Colloids and Surfaces (B: Biointerfaces), 60, 201–206.
Jaleel C A, Mamivannan P, Wahid A, Farooq M, Al-Juburi H J, Somasundaram R, Panneerselvam R. 2009. Drought stress in plants: A review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology, 11, 100–105.
Kaur H, Verma P, Petla B P, Rao V, Saxena S C, Majee M. 2013. Ectopic expression of the ABA-inducible dehydration-responsive chickpea L-myo-inositol-1-phosphate synthase 2 (CaMIPS2) in Arabidopsis enhances tolerance to salinity and dehydration stress. Planta, 237, 321–335.
Kubiś J, Floryszak-Wieczorek J, Arasimowicz-Jelonek M. 2014. Polyamines induce adaptive responses in water deficit stressed cucumber roots. Journal of Plant Research, 127, 151–158.
Lawson T, Blatt M R. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology, 164, 1556–1570.
Liang W J, Ma X L, Wan P, Liu L Y. 2017. Plant salt-tolerance mechanism: A review. Biochemical and Biophysical Research Communications, 495, 1–6.
Lichtenthaler H K, Wellburn A R. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591–592.
Loewus F A, Murthy P P N. 2000. Myo-inositol metabolism in plants. Plant Science, 150, 1–19.
McManus M T, Bieleski R L, Caradus J R, Barker D J. 2000. Pinitol accumulation in mature leaves of white clover in response to a water deficit. Environmental and Experimental Botany, 43, 11–18.
Meng P H, Raynaud C, Tcherkez G, Blanchet S, Massoud K, Domenichini S, Henry Y, Soubigou-Taconnat L, Lelarge-Trouverie C, Saindrenan P, Renou J P, Bergounioux C. 2009. Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE, 4, e7364.
Mishra A K, Singh V P. 2010. A review of drought concepts. Journal of Hydrology, 391, 202–216.
Morgan P W. 1990. Effects of abiotic stresses on plant hormone systems. In: Alscher R G, Cumming J R, eds., Stress Responses in Plants: Adaptation and Acclimation Mechanisms. Wiley-Liss, USA. pp. 113–146.
Munné-Bosch S, Penuelas J. 2003. Photo and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta, 217, 758–766.
Mutwakil M Z, Hajrah N H, Atef A, Edris S, Sabir M J, Al-Ghamdi A K, Sabir M J S M, Nelson C, Makki R M, Ali H M, El-Domyati F M, Al-Hajar A S M, Gloaguen Y, Al-Zahrani H S, Sabir J S M, Jansen R K, Bahieldin A, Hall N. 2017. Transcriptomic and metabolic responses of Calotropis procera to salt and drought stress. BMC Plant Biology, 17, 231.
Nilson S E, Assmann S M. 2007. The control of transpiration insights from Arabidopsis. Plant Physiology, 143, 19–27.
Per T S, Khan N A, Reddy P S, Masood A, Hasanuzzaman M, Khan M I R, Anjum N A. 2017. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiology and Biochemistry, 115, 126–140.
Radford P J. 1967. Growth analysis formulae - Their use and abuse. Crop Science, 7, 171–175.
Reddy A R, Chaitanya K V, Vivekanandan M. 2004. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology, 161, 1189–1202.
Sairam R K, Srivastava G C, Agarwal S, Meena R C. 2005. Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum, 49, 85–91.
Sengupta S, Mukherjee S, Basak P, Majumder A L. 2015. Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Frontiers in Plant Science, 6, 656.
Shao H B, Chu L Y, Shao M A, Cheruth J A, Mi H M. 2008. Higher plant antioxidants and redox signaling under environmental stresses. Comptes Rendus Biologies, 331, 433–441.
Singh M, Kumar J, Singh S, Singh V P, Prasad S M. 2015. Roles of osmoprotectants in improving salinity and drought tolerance in plants: A review. Reviews in Environmental and Science and Biotechnology, 14, 407–426.
Sun X, Wang P, Jia X, Huo L Q, Che R M, Ma F W. 2018. Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnology Journal, 16, 545–557.
Tan J L, Wang C Y, Xiang B, Han R H, Guo Z F. 2013. Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell & Environment, 36, 288–299.
Thalhammer A, Hincha D K, Zuther E. 2014. Measuring freezing tolerance: Electrolyte leakage and chlorophyll fluorescence assays. Methods in Molecular Biology, 1166, 15–24.
Valluru R, Ende W V D. 2011. Myo-inositol and beyond-emerging networks under stress. Plant Science, 181, 387–400.
Wahid A, Rasul E. 2005. Photosynthesis in leaf, stem, flower and fruit. In: Handbook of Photosynthesis. 2nd ed. CRC Press, Florida. pp. 479–497.
Yancey P H, Clark M E, Hand S C, Bowlus R D, Somero G N. 1982. Living with water stress: Evolution of osmolyte systems. Science, 217, 1214–1222.
Yildizli A, Çevik S, Ünyayar S. 2018. Effects of exogenous myo-inositol on leaf water status and oxidative stress of Capsicum annuum under drought stress. Acta Physiologiae Plantarum, 40, 122.
Yoo C Y, Pence H E, Hasegawa P M, Mickelbart M V. 2009. Regulation of transpiration to improve crop water use. Critical Reviews in Plant Sciences, 28, 410–431.
Zhai H, Wang F B, Si Z Z, Huo J X, Xing L, An Y Y, He S Z, Liu Q C. 2015. A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnology Journal, 14, 592–602.
Zhou K, Hu L Y, Li P M, Gong X Q, Ma F W. 2017. Genome-wide identification of glycosyltransferases converting phloretin to phloridzin in Malus species. Plant Science, 265, 131–145.
Zhou K, Hu L Y, Li Y T S, Chen X F, Zhang Z J, Liu B B, Li P M, Gong X Q, Ma F W. 2019. MdUGT88F1-mediated phloridzin biosynthesis regulates apple development and Valsa canker resistance. Plant Physiology, 180, 2290–2305.
Zhou S S, Li M J, Guan Q M, Liu F, Zhang S, Chen W, Yin L H, Qin Y, Ma F W. 2015. Physiological and proteome analysis suggest critical roles for the photosynthetic system for high water-use efficiency under drought stress in Malus. Plant Science, 236, 44–60.
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