Abstract
Drought stress is one of the most important environmental factors resulting in a variety of physiological and biochemical damages in plants. The objectives of this study were to (1) determine whether foliar application of ethionine (ETH) could effectively improve drought tolerance and (2) reveal how the foliar application of ETH alleviated drought stress from physiological and biochemical perspectives. Tall fescue (Festuca arundinacea cv. ‘Starfire’) was grown in a growth chamber and foliar applications were with 10 mL 250 mg·L−1 ETH every five days when plants were well-watered (control + ethionine) or unirrigated (drought + ethionine). Drought stress, in tall fescue, as expected, significantly decreased turf quality, relative leaf water content, photochemical efficiency, net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate. Drought stress increased electrolyte leakage as well as the content of malondialdehyde, hydrogen peroxide, and superoxide anion. Foliar application of ETH effectively mitigated drought damages by enhancing root viability, activities of antioxidant enzymes (peroxidase, catalase, ascorbate peroxidase, and monohydroascorbate reductase), and increasing contents of soluble sugars (sucrose, glucose, and fructose) and isopentenyladenosine. The results from this study suggested that the mitigation of ETH application on drought stress could be attributed to the enhanced drought tolerance through sustaining root viability, protecting cellular membrane integrity, enhancing osmotic adjustment, and regulating endogenous hormones in tall fescue.
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References
Alix JH (1982) Molecular aspects of the in vivo and in vitro effects of ethionine, an analog of methionine. Microbiol Rev 46:281–295. https://doi.org/10.1128/mr.46.3.281-295.1982
Arshad M, Frankenberger WTJ (1990) Response of Zea mays and Lycopersicon esculentum to the ethylene precursors, L-methionine and L-ethionine applied to soil. Plant Soil 122:219–227. https://doi.org/10.1007/bf02851979
Avashthi H, Pathak RK, Pandey N, Arora S, Mishra AK, Gupta VK, Ramteke PW, Kumar A (2018) Transcriptome-wide identification of genes involved in Ascorbate-Glutathione cycle (Halliwell–Asada pathway) and related pathway for elucidating its role in antioxidative potential in finger millet (Eleusine coracana (L.)). Biotech 8:499. https://doi.org/10.1007/s13205-018-1511-9
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity techniques for estimating water deficits in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/bi9620413
Blake PS, Taylor JM, Finch-Savage WE (2002) Identification of abscisic acid, indole-3-acetic acid, jasmonic acid, indole-3-acetonitrile, methyl jasmonate and gibberellins in developing, dormant and stratified seeds of ash (Fraxinus excelsior). Plant Growth Regul 37:119–125. https://doi.org/10.1023/a:1020504610172
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18. https://doi.org/10.1146/annurev.cellbio.16.1.1
Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47. https://doi.org/10.2135/cropsci1981.0011183x002100010013x
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2010) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122. https://doi.org/10.1111/j.1365-313X.2005.02615.x
Burgess P, Huang B (2014) Root protein metabolism in association with improved root growth and drought tolerance by elevated carbon dioxide in creeping bentgrass. Field Crop Res 165:80–91. https://doi.org/10.1016/j.fcr.2014.05.003
Burrell MM (1981) The mode of action of ethionine foliar sprays against potato common scab (Streptomyces scabies). Physiol Plant Pathol 18:369–378. https://doi.org/10.1016/s0048-4059(81)80087-2
Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629. https://doi.org/10.1093/jxb/44.10.1627
Chen XM, Qiu LL, Guo HP, Wang Y, Yuan HW, Yan DL, Zheng BS (2017) Spermidine induces physiological and biochemical changes in southern highbush blueberry under drought stress. Braz J Bot 40:841–851. https://doi.org/10.1007/s40415-017-0401-4
Couée I, Sulmon C, Gouesbet G, Amrani AEI (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459. https://doi.org/10.1093/jxb/erj027
DaCosta M, Huang B (2006) Changes in carbon partitioning and accumulation patterns during drought and recovery for colonial bentgrass, creeping bentgrass, and velvet bentgrass. J Am Soc Hort Sci 131:484–490. https://doi.org/10.1071/ZO9840789
DaCosta M, Wang Z, Huang B (2004) Physiological adaptation of kentucky bluegrass to localized soil drying. Crop Sci 44:1307–1314. https://doi.org/10.2135/cropsci2004.1307
Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285. https://doi.org/10.1007/s00344-005-0103-1
Devi MJ, Reddy VR (2020) Stomatal closure response to soil drying at different vapor pressure deficit conditions in maize. Plant Physiol Bioch 154:714–722. https://doi.org/10.1016/j.plaphy.2020.07.023
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Gagné-Bourque F, Bertrand A, Claessens A, Aliferis KA, Jabaji S (2016) Alleviation of drought stress and metabolic changes in timothy (Phleum pratense L.) colonized with bacillus subtilis B26. Front Plant Sci 7:584. https://doi.org/10.3389/fpls.2016.00584
Gholizadeh A, Kohnehrouz BB (2010) Activation of phenylalanine ammonia lyase as a key component of the antioxidative system of salt-challenged maize leaves. Braz J Plant Physiol 22:217–223. https://doi.org/10.1590/s1677-04202010000400001
Gupta NK, Gupta S, Kumar A (2000) Exogenous cytokinin application increases cell membrane and chlorophyll stability in wheat (Triticum aestivum L.). Cereal Res Commun 28:287–291. https://doi.org/10.1007/bf03543606
He X, Xu L, Pan C, Gong C, Yu Y (2020) Drought resistance of Camellia oleifera under drought stress: changes in physiology and growth characteristics. PLoS ONE 15:e235795. https://doi.org/10.1371/journal.pone.0235795
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. CalifAgr Exp Sta Circ 347:1–32. https://doi.org/10.1016/S0140-6736(00)73482-9
Hoffmann CM (2010) Sucrose accumulation in sugar beet under drought stress. J Agr Crop Sci 196:243–252. https://doi.org/10.1111/j.1439-037X.2009.00415.x
Huang BR, Duncan RR, Carrow RN (1997) Drought-resistance mechanisms of seven warm-season turfgrasses under surface soil drying: II Root Aspects. Crop Sci 37:1863–1869. https://doi.org/10.2135/cropsci1997.0011183X003700060033x
Huang BR, Liu XZ, Fry JD (1998) Effects of high temperature and poor soil aeration on root growth and viability of creeping bentgrass. Crop Sci 38:1618–1622. https://doi.org/10.2135/cropsci1998.0011183X003800060034x
Iqbal N, Hussain S, Raza MA, Yang CQ, Liu J (2019) Drought tolerance of soybean (Glycine max L. Merr) by improved photosynthetic characteristics and an efficient antioxidant enzyme activities under a split-root system. Front Physiol 10:786. https://doi.org/10.3389/fphys.2019.00786
Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017) Ethylene role in plant growth, development and senescence: Interaction with other phytohormones. Front Plant Sci 8:475. https://doi.org/10.3389/fpls.2017.00475
Jiang Y, Wu K, Lin F, Qu YN, Liu XX, Zhang Q (2014) Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis. Planta 239:565–575. https://doi.org/10.1007/s00425-013-1999-5
Jiménez A, Hernández JA, Pastori G, Río LAD, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335. https://doi.org/10.1104/pp.118.4.1327
Leopold AC, Noodén LD (1984) Hormonal regulatory systems in plants. In: Scott TK (ed) Horomonal regulation of development II. Encyclopedia of Plant Physiology (New Series). Springer, Berlin
Li D, Di Z, Wang H, Li Y, Li R (2017) Physiological response of plants to polyethylene glycol (PEG-6000) by exogenous melatonin application in wheat. Zemdirbyste 104:219–228. https://doi.org/10.13080/z-a.2017.104.028
Li Q, Li R, He F, Yang Z, Yu J (2022a) Growth and physiological effects of chitosan on heat tolerance in creeping bentgrass (Agrostis stolonifera). Grass Res 2:6. https://doi.org/10.48130/GR-2022-0006
Li X, Ji Y, Sheng Y, Sheng L, Guo W, Wang H, Zhang Y (2022b) Priming with the green leaf volatile (z)-3-hexeny-1-yl acetate enhances drought resistance in wheat seedlings. Plant Growth Regul 98:477–490. https://doi.org/10.1007/s10725-022-00855-4
Liu NQ, Shen YX, Huang BR (2015) Osmoregulants involved in osmotic adjustment for differential drought tolerance in different bentgrass genotypes. J Am Soc Hort Sci 140:605–613. https://doi.org/10.21273/JASHS.140.6.605
Ma XQ, Xu Q, Meyer WA, Huang BR (2016a) Hormone regulation of rhizome development in tall fescue (Festuca arundinacea) associated with proteomic changes controlling respiratory and amino acid metabolism. Ann Bot 118:481–494. https://doi.org/10.1093/aob/mcw120
Ma XQ, Zhang J, Huang BR (2016b) Cytokinin-mitigation of salt-induced leaf senescence in perennial ryegrass involving the activation of antioxidant systems and ionic balance. Environ Exp Bot 125:1–11. https://doi.org/10.1016/j.envexpbot.2016.01.002
McCann SE, Huang B (2008a) Drought responses of kentucky bluegrass and creeping bentgrass as affected by abscisic acid and trinexapac-ethyl. J Am Soc Hort Sci 133:20–26. https://doi.org/10.1590/S0102-05362008000100024
McCann SE, Huang B (2008b) Evaluation of drought tolerance and avoidance traits for six creeping bentgrass cultivars. HortScience 43:519–524. https://doi.org/10.1590/S0102-05362008000200033
Mcintosh AH, Burrell MM (1980) Movement of ethionine in potato plants after foliar application against common scab. Physiol Plant Pathol 17:205–212. https://doi.org/10.1016/0048-4059(80)90053-3
Mcintosh AH, Burrell MM, Bateman GL (1977) Mechanisms of action of foliar sprays of daminozide and ethionine against potato common scab. Proc 1977 Brit Crop Prot Conf (pest Dis) 1:87–93. https://doi.org/10.1016/0048-4059(80)90053-3
Merewitz EB, Gianfagna T, Huang BR (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 Hort Sci 135:230–239. https://doi.org/10.21273/jashs.135.3.230
Merewitz EB, Gianfagna T, Huang BR (2011a) Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis in Agrostis stolonifera. J Exp Bot 62:383–395. https://doi.org/10.1093/jxb/erq285
Merewitz EB, Gianfagna T, Huang BR (2011b) Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J Exp Bot 62:5311–5333. https://doi.org/10.1093/jxb/err166
Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403. https://doi.org/10.1016/j.jplph.2007.10.015
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Niether W, Glawe A, Pfohl K, Adamtey N, Schneider M, Karlovsky P, Pawelzik E (2020) The effect of short-term vs. long-term soil moisture stress on the physiological response of three cocoa (Theobroma cacao l.) cultivars. Plant Growth Regul 92:295–306. https://doi.org/10.1007/s10725-020-00638-9
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. https://doi.org/10.1146/annurev.arplant.49.1.249
Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992. https://doi.org/10.1038/nprot.2010.37
Patel KP, Hemantaranjan A, Sarma BK, Singh R (2011) Growth and antioxidant system under drought stress in Chickpea (Cicer arietinum L.) as sustained by salicylic acid. J Stress Physiol Biochem 7:130–144. https://doi.org/10.0000/cyberleninka.ru/article/n/growth-and-antioxidant-system-
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. https://doi.org/10.1016/j.pbi.2011.02.001
Qi W, Zhang JW, Wang KJ, Liu P, Dong ST (2010) Effects of drought stress on the grain yield and root physiological traits of maize varieties with different drought tolerance. J Appl Ecol 21:48–52. https://doi.org/10.3724/SP.J.1142.2010.40491
Reisch BI, Duke SH, Bingham ET (1981) Selection and characterization of ethionine-resistant alfalfa (Medicago sativa L.) cell lines. Theor Appl Genet 59:89–94. https://doi.org/10.1007/bf00285896
Sarul P, Vlahova M, Todorovska E, Atanassov A (1995) Inheritance of kanamycin and ethionine resistance introduced in alfalfa (Medicago Sativa L.) by gene transfer and cell selection. Biotechnol Biotechnol Equip 9:45–51. https://doi.org/10.1080/13102818.1995.10818821
Shan CJ, Wang BS, Sun HL, Gao S, Li H (2020) H2S induces NO in the regulation of AsA-GSH cycle in wheat seedlings by water stress. Protoplasma 257:1487–1493. https://doi.org/10.1007/s00709-020-01510-3
Silva CB, Simionatto E, Gebara SS, Poppi NR, Cândido ACS, Lima CP, Dias JFG, Zanin SMW, Peres MTLP, Moreira TF, Miguel OG, Miguel MD (2013) Polygala extra axillaris: oxidative stress in brachiaria decumbens mediated by volatile oils. Planta Daninha 31:793–804. https://doi.org/10.1590/s0100-83582013000400005
Silva VA, Prado FM, Antunes WC, Paiva RMC, Ferrão MAG, Andrade AC, Di Mascio P, Loureiro ME, DaMatta FM, Almeida AM (2018) Reciprocal grafting between clones with contrasting drought tolerance suggests a key role of abscisic acid in coffee acclimation to drought stress. Plant Growth Regul 85:221–229. https://doi.org/10.1007/s10725-018-0385-5
Taulavuori E, Tahkokorpi M, Laine K, Taulavuori K (2010) Drought tolerance of juvenile and mature leaves of a deciduous dwarf shrub Vaccinium myrtillus L. in a boreal environment. Protoplasma 241:19–27. https://doi.org/10.1007/s00709-009-0096-x
Towill LE, Mazur P (1975) Studies on the reduction of 2,3,5-triphenyltetrazolium chloride as a viability assay for plant tissue cultures. Can J Bot 53:1097–1102. https://doi.org/10.1139/b75-129
Turgeon A (2011) Turfgrass management, 9th edn. Prentice Hall, Hoboken
Turgeon R (1996) Phloem loading and plasmodesmata. Trends Plant Sci 1:418–423. https://doi.org/10.1016/s1360-1385(96)10045-5
Wang SQ, Xue ZS, Li C, Tang SY, Yang ZM (2020) Mitigation effect of ethionine on tall fescue under salt stress. J Yunnan Univ Nat Sci Ed 42:179–186. https://doi.org/10.7540/j.ynu.20190378
Xu LX, Han LB, Huang BR (2011) Antioxidant enzyme activities and gene expression patterns in leaves of kentucky bluegrass in response to drought and post-drought recovery. J Am Soc Hort Sci 136:247–255. https://doi.org/10.21273/jashs.136.4.247
Xu Y, Xu Q, Huang BR (2015) Ascorbic acid mitigation of water stress-inhibition of root growth in association with oxidative defense in tall fescue (Festuca arundinacea Schreb.). Front Plant Sci 6:807. https://doi.org/10.3389/fpls.2015.00807
Yan J, Li H, Li Y, Zhang N, Zhang S (2022) Abscisic acid synthesis and root water uptake contribute to exogenous methyl jasmonate-induced improved tomato drought resistance. Plant Biotechnol Rep 16:183–193. https://doi.org/10.1007/s11816-022-00753-1
Yang ZM, Chang ZL, Sun LH, Yu JJ, Huang BR (2014) Physiological and metabolic effects of 5-aminolevulinic acid for mitigating salinity stress in creeping bentgrass. PLoS ONE 9:e116283. https://doi.org/10.1371/journal.pone.0116283
Yang ZM, Xu LX, Yu JJ, DaCosta M, Huang BR (2013) Changes in carbohydrate metabolism in two kentucky bluegrass cultivars during drought stress and recovery. J Am Soc Hort Sci 138:24–30. https://doi.org/10.21273/JASHS.138.1.24
Yang ZM, Yu JJ, Merewitz E, Huang BR (2012) Differential effects of abscisic acid and glycine betaine on physiological responses to drought and salinity stress for two perennial grass species. J Amer Soc Hort Sci 137:96–106. https://doi.org/10.21273/JASHS.137.2.96
Zhang JX, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373. https://doi.org/10.1111/j.1469-8137.1996.tb01856.x
Zhang XZ, Goatley M, Mccall D, Kosiarski K, Reith F (2022) Humic acids-based biostimulants impact on root viability and hormone metabolism in creeping bentgrass putting greens. Int Turfgrass Soc Res J 14:288–294. https://doi.org/10.1002/its2.37
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
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Authors gratefully wish to thank the National Natural Science Foundation of China (31971771, 32171689) and China Postdoctoral Science Foundation (2019M651866) for the financial support.
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Funding for this study was provided by the National Natural Science Foundation of China (31971771, 32171689) and China Postdoctoral Science Foundation (2019M651866).
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The study conception and design were contributed by ZY, JY, and LZ., JY, NF, TH, YB, and QL prepared the materials and performed the experiment. Data analysis was finished by JY and NF. The first draft of the manuscript was written by JY and ZY. All authors participated in the revision of the manuscript. JY and LZ provided the funding. All authors read and approved the final manuscript.
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Yu, J., Fan, N., Hao, T. et al. Ethionine-mitigation of drought stress associated with changes in root viability, antioxidant defense, osmotic adjustment, and endogenous hormones in tall fescue. Plant Growth Regul 100, 119–132 (2023). https://doi.org/10.1007/s10725-022-00944-4
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DOI: https://doi.org/10.1007/s10725-022-00944-4