Стресс-индуцируемая потеря электролитов клетками корня высших растений: история вопроса, механизм и физиологическая роль
Аннотация
Утечка (отток) электролитов из тканей является одной из центральных реакций растительного организма на стресс. Она наблюдается практически при любом виде стрессового воздействия как абиотической, так и биотической природы, приводя к потере ключевых электролитов, перестройке метаболизма и в некоторых случаях к гибели клеток и организма. Долгое время считалось, что утечка электролитов связана с нарушением целостности клеток и плазматических мембран и является нерегулируемым процессом. Тем не менее в последние годы получено множество данных, свидетельствующих о том, что в большинстве случаев утечка электролитов ингибируется блокаторами ионных каналов, т. е. связана с переносом ионов через белковые транспортные системы. Имеются экспериментальные доказательства того, что выходящий поток электролитов у растений при засолении, засухе, атаке патогенных организмов, воздействии тяжелых металлов, гипо- и гипертермии, а также окислительном стрессе опосредован несколькими типами ионных каналов, включая K+-селективные каналы, анионные каналы и неселективные катионные каналы как минимум трех семейств. Продемонстрировано, что первичными реакциями, которые индуцируют утечку электролитов, являются деполяризация плазматической мембраны и генерация активных форм кислорода, приводящие к активации редокс-регулируемых K+-каналов наружного выпрямления, таких как SKOR и GORK. Выход K+ стимулирует отток противоионов (анионов) через конститутивные анионные каналы, которые, вероятно, кодируются генами семейства ALMT. Регуляция утечки электролитов на уровне ионных каналов и соответствующая селекция по свойствам ионных каналов могут стать важным звеном направленного управления стрессоустойчивостью высших растений. Это может быть применено на практике при выведении новых линий и сортов растений, а также разработке современных агромелиоративных приемов.
Литература
- Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V. Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany. 2015;65(5):1259–1270. DOI: 10.1093/jxb/eru004.
- Dexter ST, Tottingham WE, Graber LF. Investigation of the hardiness of plants by measurement of electrical conductivity. Plant Physiology. 1932;7(1):63–78. DOI: 10.1104/pp.7.1.63.
- Demidchik V. Reactive oxygen species and their role in plant oxidative stress. In: Shabala S, editor. Plant stress physiology. Wallingford: CABI; 2017. p. 64–96. DOI: 10.1079/9781780647296.0064.
- Bajji M, Kinet J-M, Lutts S. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regulation. 2002;36(1):61–70. DOI: 10.1023/A:1014732714549.
- Demidchik V. Mechanisms and physiological roles of K+ efflux from root cells. Journal of Plant Physiology. 2014;171(9):696–707. DOI: 10.1016/j.jplph.2014.01.015.
- Demidchik V, Tyutereva EV, Voitsekhovskaja OV. The role of ion disequilibrium in induction of root cell death and autophagy by environmental stresses. Functional Plant Biology. 2018;45(2):28–46. DOI: 10.1071/FP16380.
- Leigh RA, Jones RGW. A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytologist. 1984;97(1):1–13. DOI: 10.1111/J.1469-8137.1984.TB04103.X.
- Demidchik V. Characterisation of root plasma membrane Ca2+-permeable cation channels: techniques and basic concepts. In: Volkov AG, editor. Plant electrophysiology: signaling and responses. Berlin: Springer-Verlag; 2012. p. 339–369.
- Osterhaut WJV. Injury, recovery, and death, in relation to conductivity and permeability. Philadelphia: J. B. Lippincott Company; 1922. 259 p.
- Palta JP, Levitt J, Stadelmann EJ. Freezing injury in onion bulb cells. I. Evaluation of the conductivity method and analysis of ion and sugar efflux from injured cells. Plant Physiology. 1977;60(3):393–397. DOI: 10.1104/pp.60.3.393.
- Blum А, Ebercon А. Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Science. 1981;21(1):43–47. DOI: 10.2135/CROPSCI1981.0011183X002100010013X.
- Leopold CA, Musgrave ME, Williams KM. Solute leakage resulting from leaf desiccation. Plant Physiology. 1981;68(6):1222–1225. DOI: 10.1104/pp.68.6.1222.
- Atkinson MM, Midland SL, Sims JJ, Keen NT. Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalisation in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiology. 1996;112(1):297–302. DOI: 10.1104/pp.112.1.297.
- Murphy AS, Eisinger WR, Shaff JE, Kochian LV, Taiz L. Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiology. 1999;121(4):1375–1382. DOI: 10.1104/pp.121.4.1375.
- Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, et al. Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ -permeable channels. Plant Physiology. 2006;141(4):1653–1665. DOI: 10.1104/pp.106.082388.
- Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, et al. Arabidopsis root K+ efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science. 2010;123(9):1468–1479. DOI: 10.1242/jcs.064352.
- Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II. Na+ – K+ transport in roots under salt stress. Plant Signaling and Behavior. 2008;3(6):401–403. DOI: 10.4161/psb.3.6.5429.
- Shabala S, Cuin TA, Pottosin I. Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Letters. 2007;581(10):1993–1999. DOI: 10.1016/j.febslet.2007.04.032.
- Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM. Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. Journal of Cell Science. 2003;116(1):81–88. DOI: 10.1242/jcs.00201.
- Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, et al. Zea mays annexins modulate cytosolic free Ca2+ form a Ca2+-permeable conductance and have peroxidase activity. The Plant Cell. 2009;21(2):479–493. DOI: 10.1105/tpc.108.059550.
- Demidchik V, Shang Z, Shin R, Colaço R, Laohavisit A, Shabala S, et al. Receptor-like activity evoked by extracellular ADP in Arabidopsis thaliana root epidermal plasma membrane. Plant Physiology. 2011;156(3):1375–1385. DOI: 10.1104/pp.111.174722.
- Shabala S. Plant stress physiology. Wallingford: CABI; 2017. 376 p.
- Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, et al. An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiology. 2009;151(4):2006–2017. DOI: 10.1104/pp.109.147462.
- Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil. 2009;321(1):5–33. DOI: 10.1007/s11104-009-9925-0.
- Flowers TJ, Colmer TD. Plant salt tolerance: adaptations in halophytes. Annals of Botany. 2015;115(3):327–331. DOI: 10.1093/aob/mcu267.
- Munns R, Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology. 2008;59:651–681. DOI: 10.1146/annurev.arplant.59.032607.092911.
- Zvanarou S, Vágnerová R, Mackievic V, Usnich S, Smolich I, Sokolik A, et al. Salt stress triggers generation of oxygen free radicals and DNA breaks in Physcomitrella patens protonema. Environmental and Experimental Botany. 2020;180:104236. DOI: 10.1016/j.envexpbot.2020.104236.
- Shabala S. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany. 2013;112(7):1209–1221. DOI: 10.1093/aob/mct205.
- Negrão S, Schmöckel SM, Tester M. Evaluating physiological responses of plants to salinity stress. Annals of Botany. 2017;119(1):1–11. DOI: 10.1093/aob/mcw191.
- Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, et al. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Agricultural Advances. 2014;19(10):623–630. DOI: 10.1016/j.tplants.2014.06.013.
- Roy SJ, Negrão S, Tester M. Salt resistant crop plants. Current Opinion in Biotechnology. 2014;26:115–124. DOI: 10.1016/j.copbio.2013.12.004.
- Munns R, Termaat A. Whole-plant responses to salinity. Australian Journal of Plant Physiology. 1986;13(1):143–160. DOI: 10.1071/PP9860143.
- Demidchik V, Tester M. Sodium fluxes through non-selective cation channels in the plasma membrane of protoplasts from Arabidopsis thaliana roots. Plant Physiology. 2002;128(2):379–387. DOI: 10.1104/pp.010524.
- Levitt J. Responses of plant to environmental stress: water, radiation, salt and other stresses. New York: Academic Press; 1980. 607 p.
- Levitt J. Responses of plants to environmental stresses. London: Academic Press; 1972. 697 p.
- Nassery H. The effects of salt and osmotic stress on the retention of potassium by excised barley and bean roots. New Phytologist. 1975;75(1):63–67. DOI: 10.1111/j.1469-8137.1975.tb01371.x.
- Nassery H. Salt induced loss of potassium from plant roots. New Phytologist. 1979;83(1):23–27. DOI: 10.1111/j.1469-8137.1979.tb00722.x.
- Maathuis FJM, Amtmann A. K+ nutrition and Na+ toxicity: the basis of cellular K+ / Na+ ratios. Annals of Botany. 1999;84(2):123–133. DOI: 10.1006/anbo.1999.0912.
- Cuin TA, Betts SA, Chalmandrier R, Shabala S. A root’s ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany. 2008;59(10):2697–2706. DOI: 10.1093/jxb/ern128.
- Hryvusevich P, Navaselsky I, Talkachova Yu, Straltsova D, Keisham M, Viatoshkin A, et al. Sodium influx and potassium efflux currents in sunflower root cells under high salinity. Frontiers in Plant Science. 2021;11:613936. DOI: 10.3389/fpls.2020.613936.
- Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, et al. Root plasma membrane transporters controlling K+/ Na+ homeostasis in salt-stressed barley. Plant Physiology. 2007;145(4):1714–1725. DOI: 10.1104/pp.107.110262.
- Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K. New insights on plant salt tolerance mechanisms and their potential use for breeding. Frontiers in Plant Science. 2016;7:1787. DOI: 10.3389/fpls.2016.01787.
- Ahmed W, Imran M, Yaseen M, ul Haq T, Jamshaid MU, Rukh S, et al. Role of salicylic acid in regulating ethylene and physiological characteristics for alleviating salinity stress on germination, growth and yield of sweet pepper. PeerJ. 2020;27(8):e8475. DOI: 10.7717/peerj.8475.
- Ebel J, Mithöfer A. Early events in the elicitation of plant defence. Planta. 1998;206:335–348. DOI: 10.1007/s004250050409.
- Zimmermann S, Nürnberger T, Frachisse J-M, Wirtz W, Guern J, Hedrich R, et al. Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(6):2751–2755. DOI: 10.1073/pnas.94.6.2751.
- Kato T, Ueda T, Fljimoto K. New insecticidally active chrysanthemates. Agricultural and Biological Chemistry. 1964;28(12):914–915. DOI: 10.1080/00021369.1964.10858319.
- Cook A, Stall R. Effect of Xanthomonas vesicatoria on loss of electrolytes from leaves of Capsicum annuum. Phytopathology. 1968;58:617–619.
- Pellizzari ED, Kuc J, Williams EB. The hypersensitive reaction in Malus species: changes in the leakage of electrolytes from apple leaves after inoculation with Venturia inaequalis. Phytopathology. 1970;60:373–376. DOI: 10.1094/Phyto-60-373.
- Atkinson MM, Huang J-S, Knopp JA. The hypersensitive reaction of tobacco to Pseudomonas syringae pv. pisi: activation of a plasmalemma K+ / H+ exchange mechanism. Plant Physiology. 1985;79(3):843–847. DOI: 10.1104/pp.79.3.843.
- Atkinson MM, Keppler LD, Orlandi EW, Baker CJ, Mischke CF. Involvement of plasma membrane calcium influx in bacterial induction of the K+ / H+ and hypersensitive responses in tobacco. Plant Physiology. 1990;92(1):215–221. DOI: 10.1104/pp.92.1.215.
- Dunkle LD, Wolpert TJ. Independence of milo disease symptoms and electrolyte leakage induced by the host-specific toxin from Periconia circinata. Physiological Plant Pathology. 1981;18(3):315–323. DOI: 10.1016/S0048-4059(81)80082-3.
- Pennazio S, Sapetti C. Electrolyte leakage in relation to viral and abiotic stresses inducing necrosis in cowpea leaves. Biologia Plantarum. 1982;24(3):218–225. DOI: 10.1007/BF02883667.
- Finlayson JE, Pritchard MK, Rimmer SR. Electrolyte leakage and storage decay of five carrot cultivars in response to infection by Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology. 1989;11(3):313–316. DOI: 10.1080/07060668909501119.
- Stover EW, Swartz HJ, Burr TJ. Crown gall formation in a diverse collection of Vitis genotypes inoculated with Agrobacterium vitis. American Journal of Enology and Viticulture. 1997;48:26–32.
- Sriram S, Raguchander T, Babu S, Nandakumar R, Shanmugam V, Vidhyasekaran P, et al. Inactivation of phytotoxin produced by the rice sheath blight pathogen Rhizoctonia solani. Canadian Journal of Microbiology. 2000;46(6):520–524. DOI: 10.1139/w00-018.
- Ádám AL, Galal AA, Manninger K, Barna B. Inhibition of the development of leaf rust (Puccinia recondita) by treatment of wheat with allopurinol and production of a hypersensitive-like reaction in a compatible host. Plant Pathology. 2000;49(3):317–323. DOI: 10.1046/j.1365-3059.2000.00455.x.
- Mohanraj D, Padmanaban P, Karunakaran M. Effect of phytotoxin of Colletotrichum falcatum Went. (Physalospora tucumanensis) on sugarcane in tissue culture. Acta Phytopathologica et Entomologica Hungarica. 2003;38(1–2):21–28. DOI: 10.1556/APhyt.38.2003.1-2.4.
- Dewir YH, El Mahrouk ME, Hafez YM, Rihan HZ, Sáez CA, Fuller MP. Antioxidative capacity and electrolyte leakage in healthy versus phytoplasma infected tissues of Euphorbia coerulescens and Orbea gigantea. Journal of Plant Physiology & Pathology. 2015;3(1):1–6. DOI: 10.4172/2329-955X.1000139.
- Colcombet J, Mathieu Y, Peyronnet R, Agier N, Lelièvre F, Barbier-Brygoo H, et al. R-type anion channel activation is an essential step for ROS-dependent innate immune response in Arabidopsis suspension cells. Functional Plant Biology. 2009;36(9):832–843. DOI: 10.1071/FP09096.
- Roelfsema MRG, Hedrich R, Geiger D. Anion channels: master switches of stress responses. Trends in Plant Science. 2012;17(4):221–229. DOI: 10.1016/j.tplants.2012.01.009.
- Wei Guo, Chengcheng Wang, Zhangli Zuo, Jin-Long Qiu. The roles of anion channels in Arabidopsis immunity. Plant Signaling and Behavior. 2014;9(7):e29230. DOI: 10.4161/psb.29230.
- Chester KS. The problem of acquired physiological immunity in plants. Quarterly Review of Biology. 1933;8(2):129–154.
- Klement Z, Goodman RN. The hypersensitive reaction to infection by bacterial plant pathogens. Annual Review of Phytopathology. 1967;5:17–44. DOI: 10.1146/annurev.py.05.090167.000313.
- Balint‐Kurti P. The plant hypersensitive response: concepts, control and consequences. Molecular Plant Pathology. 2019;20(8):1163–1178. DOI: 10.1111/mpp.12821.
- Goodman RN, Novacky AJ. The hypersensitive reaction in plants to pathogens: a resistance phenomenon. Chicago: American Phytopathological Society; 1994. 244 p.
- Ward HM. On the relations between host and parasite in the bromes and their brown rust, Puccinia dispersa (Erikss.). Annals of Botany. 1902;os-16(2):233–316. DOI: 10.1093/oxfordjournals.aob.a088874.
- Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(17):9750–9754. DOI: 10.1073/pnas.95.17.9750.
- Dropkin VH. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology. 1969;59:1632–1637.
- Mohamed A, Ellicott A, Housley TL, Ejeta G. Hypersensitive response to Striga infection in Sorghum. Crop Science. 2003;43(4):1320–1324. DOI: 10.2135/cropsci2003.1320.
- Swarbrick PJ, Huang K, Liu G, Slate J, Press MC, Scholes JD. Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytologist. 2008;179(2):515–529. DOI: 10.1111/j.1469-8137.2008.02484.x.
- Jennings DB, Daub ME, Pharr DM, Williamson JD. Constitutive expression of a celery mannitol dehydrogenase in tobacco enhances resistance to the mannitol-secreting fungal pathogen Alternaria alternate. The Plant Journal. 2002;32(1):41–49. DOI: 10.1046/j.1365-313x.2001.01399.x.
- Govrin EM, Rachmilevitch S, Tiwari BS, Solomon M, Levine A. An elicitor from Botrytis cinerea induces the hypersensitive response in Arabidopsis thaliana and other plants and promotes the gray mold disease. Phytopathology. 2006;96(3):299–307. DOI: 10.1094/PHYTO-96-0299.
- Blatt MR, Grabov A, Brearley J, Hammond-Kosack K, Jones JDG. K+ channels of Cf-9-transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9. The Plant Journal. 1999;19(4):453–462. DOI: 10.1046/j.1365-313x.1999.00534.x.
- Pasechnik T, Aver’yanov AA, Lapikova VP, Kovalenko ED, Kolomietz TM. The involvement of activated oxygen in the expression of the vertical and horizontal resistance of rice to blast disease. Russian Journal of Plant Physiology. 1998;45(3):371–378.
- Doke N. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiological Plant Pathology. 1983;23(3):345–357. DOI: 10.1016/0048-4059(83)90019-X.
- De Gara L, de Pinto MC, Tommasi F. The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiology and Biochemistry. 2003;41(10):863–870. DOI: 10.1016/S0981-9428(03)00135-9.
- Errakhi R, Dauphin A, Meimoun P, Lehner A, Reboutier D, Vatsa P, et al. An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. Journal of Experimental Botany. 2008;59(15):4259–4270. DOI: 10.1093/jxb/ern267.
- Zhang W-H, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD. Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant and Cell Physiology. 2008;49(9):1316–1330. DOI: 10.1093/pcp/pcn107.
- De Vos CHR, Schat H, De Waal MAM, Vooijs R, Ernst WHO. Increased resistance to copper induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiologia Plantarum. 1991;82(4):523–528. DOI: 10.1111/j.1399-3054.1991. tb02942.x.
- De Vos CHR, Schat H, Vooijs R, Ernst WHO. Copper induced damage to the permeability barrier in roots of Silene cucubalus. Journal of Plant Physiology. 1989;135(2):164–165. DOI: 10.1016/S0176-1617(89)80171-3.
- De Vos CHR, Ten Bookum WM, Vooijs R, Schat H, De Kok LJ. Effect of copper on fatty acid composition and peroxidation of lipids in the roots of copper tolerant and sensitive Silene cucubalus. Plant Physiology and Biochemistry. 1993;31(2):151–158.
- Murphy A, Taiz L. Correlation between potassium efflux and copper sensitivity in ten Arabidopsis ecotypes. New Phytologist. 1997;136(2):211–222.
- Demidchik V, Sokolik A, Yurin V. The effect of Cu2+ on ion transport systems of the plant cell plasmalemma. Plant Physiology. 1997;114(4):1313–1325. DOI: 10.1104/pp.114.4.1313.
- Demidchik V, Sokolik A, Yurin V. Characteristics of non-specific permeability and H+ -ATPase inhibition induced in the plasma membrane of Nitella flexilis by excessive Cu2+. Planta. 2001;212:583–590. DOI: 10.1007/s004250000422.
- Demidchik V, Maathuis FJM. Physiological roles of non-selective cation channels in plants: from salt stress to signalling and development. New Phytologist. 2007;175(3):387–405. DOI: 10.1111/j.1469-8137.2007.02128.x.
- Laohavisit A, Shang Z, Rubio L, Cuin TA, Véry AA, Wang A, et al. Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+- and K+ -permeable conductance in root cells. The Plant Cell. 2012;24(4):1522–1533. DOI: 10.1105/tpc.112.097881.
- Kai H, Iba K. Temperature stress in plants. eLS [Internet]. 2014 [cited 2022 February 1]. Available from: https://onlinelibrary. wiley.com/doi/epdf/10.1002/9780470015902.a0001320.pub2. DOI: 10.1002/9780470015902.a0001320.pub2.
- Meryman HT. Freezing injury and its prevention in living cells. Annual Review of Biophysics and Bioengineering. 1974;3:341–363. DOI: 10.1146/annurev.bb.03.060174.002013.
- Givelberg A, Horowitz M, Poljakoff-Mayber A. Solute leakage from Solanum nigrum L. seeds exposed to high temperatures during imbibition. Journal of Experimental Botany. 1984;35(12):1754–1763. DOI: 10.1093/jxb/35.12.1754.
- Gay C, Corbineau F, Côme D. Effects of temperature and oxygen on seed germination and seedling growth in sunflower (Helianthus annuus L.). Environmental and Experimental Botany. 1991;31(2):193–200. DOI: 10.1016/0098-8472(91)90070-5.
- Leinonen I, Hänninen H, Repo T. Testing of frost hardiness models for Pinus sylvestris in natural conditions and in elevated temperature. Silva Fennica. 1996;30(2–3):5583. DOI: 10.14214/sf.a9228.
- Janda T, Szalai G, Ducruet J-M, Páldi E. Changes in photosynthesis in inbred maize lines with different degrees of chilling tolerance grown at optimum and suboptimum temperatures. Photosynthetica. 1998;35:205–212. DOI: 10.1023/A:1006954605631.
- Kang HM, Saltveit ME. Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiologia Plantarum. 2002;115(4):571–576. DOI: 10.1034/j.1399-3054.2002.1150411.x.
- Zhou W, Leul M. Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regulation. 1998;26(1):41–47. DOI: 10.1023/A:1006004921265.
- Ismail AM, Hall AE. Reproductive-stage heat tolerance, leaf membrane thermostability and plant morphology in cowpea. Crop Physiology & Metabolism. 1999;39(6):1762–1768. DOI: 10.2135/cropsci1999.3961762x.
- Saelim S, Zwiazek JJ. Preservation of thermal stability of cell membranes and gas exchange in high temperature acclimated Xylia xylocarpa seedlings. Journal of Plant Physiology. 2000;156(3):380–385. DOI: 10.1016/S0176-1617(00)80077-2.
- Coursolle C, Bigras FJ, Margolis HA. Assessment of root freezing damage of two-year-old white spruce, black spruce and jack pine seedlings. Scandinavian Journal of Forest Research. 2000;15(3):343–353. DOI: 10.1080/028275800447977.
- Campos PS, Quartin V, Ramalho JC, Nunes MA. Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. Journal of Plant Physiology. 2003;160(3):283–292. DOI: 10.1078/0176-1617-00833.
- Clarke SM, Mur LAJ, Wood JE, Scott IM. Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. The Plant Journal. 2004;38(3):432–447. DOI: 10.1111/j.1365-313X.2004.02054.x.
- Wahid A, Shabbir A. Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regulation. 2005;46(2):133–141. DOI: 10.1007/s10725-005-8379-5.
- Sayyari M, Babalar M, Kalantari S, Serrano M, Valero D. Effect of salicylic acid treatment on reducing chilling injury in stored pomegranates. Postharvest Biology and Technology. 2009;53(3):152–154. DOI: 10.1016/j.postharvbio.2009.03.005.
- Biswas SK, Pandey NK, Rajik M. Inductions of defense response in tomato against Fusarium wilt through inorganic chemicals as inducers. Journal of Plant Pathology & Microbiology. 2012;3(4):128–135. DOI: 10.4172/2157-7471.1000128.
- Hara M, Terashima S, Fukaya T, Kuboi T. Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta. 2003;217(2):290–298. DOI: 10.1007/s00425-003-0986-7.
- Hayes S, Schachtschabel J, Mishkind M, Munnik T, Arisz SA. Hot topic: thermosensing in plants. Plant Cell and Environment. 2021;44(7):2018–2033. DOI: 10.1111/pce.13979.
- Finka A, Cuendet AFH, Maathuis FJM, Saidi Y, Goloubinoff P. Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell. 2012;24(8):3333–3348. DOI: 10.1105/tpc.112.095844.
- Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, et al. The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell. 2009;21(9):2829–2843. DOI: 10.1105/tpc.108.065318.
- Yongmei Cui, Shan Lu, Zhan Li, Jiawen Cheng, Peng Hu, Tianquan Zhu, et al. Cyclic nucleotide-gated ion channels 14 and 16 promote tolerance to heat and chilling in rice. Plant Physiology. 2020;183(4):1794–1808. DOI: 10.1104/pp.20.00591.
- Rahman Ar, Kawamura Y, Maeshima M, Rahman Ab, Uemura M. Plasma membrane aquaporin members PIPs act in concert to regulate cold acclimation and freezing tolerance responses in Аrabidopsis thaliana. Plant and Cell Physiology. 2020;61(4):787–802. DOI: 10.1093/pcp/pcaa005.
- Bewley JD. Physiological aspects of desiccation tolerance. Annual Review of Plant Physiology. 1979;30:195–238. DOI: 10.1146/annurev.pp.30.060179.001211.
- McKersie BD, Stinson RH. Effect of dehydration on leakage and membrane structure in Lotus corniculatus L. seeds. Plant Physiology. 1980;66(2):316–320.
- McKersie BD, Tomes DT. Effects of dehydration treatments on germination, seedling vigour, and cytoplasmic leakage in wild oats and birdsfoot trefoil. Canadian Journal of Botany. 1980;58(4):471–476. DOI: 10.1139/b80-056.
- Becwar MR, Stanwood PC, Roos EE. Dehydration effects on imbibitional leakage from desiccation-sensitive seeds. Plant Physiology. 1982;69(5):1132–1135. DOI: 10.1104/pp.69.5.1132.
- Senaratna T, McKersie BD. Dehydration injury in germinating soybean (Glycine max L. Merr.) seeds. Plant Physiology. 1983;72(3):620–624. DOI: 10.1104/pp.72.3.620.
- Yongchao Liang, Qin Chen, Qian Liu, Wenhua Zhang, Ruixing Ding. Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). Journal of Plant Physiology. 2003;160(10):1157–1164. DOI: 10.1078/0176-1617-01065.
- Nayyar H, Gupta D. Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. Environmental and Experimental Botany. 2006;58(1–3):106–113. DOI: 10.1016/j.envexpbot.2005.06.021.
- Fang-Zheng Wang, Qing-Bin Wang, Suk-Yoon Kwon, Sang-Soo Kwak, Wei-Ai Su. Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. Journal of Plant Physiology. 2005;162(4):465–472. DOI: 10.1016/j.jplph.2004.09.009.
- Guo Z, Ou W, Lu S, Zhong Q. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiology and Biochemistry. 2006;44(11–12):828–836. DOI: 10.1016/j.plaphy.2006.10.024.
- Hayat S, Hasan SA, Fariduddin Q, Ahmad A. Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. Journal of Plant Interactions. 2008;3(4):297–304. DOI: 10.1080/17429140802320797.
- Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, et al. Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. Journal of Experimental Botany. 2011;62(8):2599–2613. DOI: 10.1093/jxb/erq432.
- Chao Li, Dun-Xian Tan, Dong Liang, Cong Chang, Dongfeng Jia, Fengwang Ma. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. Journal of Experimental Botany. 2015;66(3):669–680. DOI: 10.1093/jxb/eru476.
- Guadagno CR, Ewers BE, Speckman HN, Aston TL, Huhn BJ, DeVore SB, et al. Dead or alive? Using membrane failure and chlorophyll a fluorescence to predict plant mortality from drought. Plant Physiology. 2017;175(1):223–234. DOI: 10.1104/pp.16.00581.
- Kamali S, Mehraban A. Effects of nitroxin and arbuscular mycorrhizal fungi on the agro-physiological traits and grain yield of sorghum (Sorghum bicolor L.) under drought stress conditions. PLoS One. 2020;15(12):e0243824. DOI: 10.1371/journal.pone.0243824.
- Kashtoh H, Baek KH. Structural and functional insights into the role of guard cell ion channels in abiotic stress-induced stomatal closure. Plants. 2021;10(12):2774. DOI: 10.3390/plants10122774.
- Xue Feng, Wenxing Liu, Cheng-Wei Qiu, Fanrong Zeng, Yizhou Wang, Guoping Zhang, et al. HvAKT2 and HvHAK1 confer drought tolerance in barley through enhanced leaf mesophyll H+ homoeostasis. Plant Biotechnology Journal. 2020;18(8):1683–1696. DOI: 10.1111/pbi.13332.
- Xue Feng, Wenxing Liu, Fangbin Cao, Yizhou Wang, Guoping Zhang, Zhong-Hua Chen. Overexpression of HvAKT1 improves drought tolerance in barley by regulating root ion homeostasis and ROS and NO signaling. Journal of Experimental Botany. 2020;71(20):6587–6600. DOI: 10.1093/jxb/eraa354.
- Verma H, Devi K, Baruah AR, Sarma RN. Relationship of root aquaporin genes, OsPIP1;3, OsPIP2;4, OsPIP2;5, OsTIP2;1 and OsNIP2;1 expression with drought tolerance in rice. Indian Journal of Genetics and Plant Breeding. 2020;80(1):50–57. DOI: 10.31742/IJGPB.80.1.6.
- Xi-Dong Li, Yong-Qiang Gao, Wei-Hua Wu, Li-Mei Chen, Yi Wang. Two calcium-dependent protein kinases enhance maize drought tolerance by activating anion channel ZmSLAC1 in guard cells. Plant Biotechnology Journal. 2022;20(1):143–157. DOI: 10.1111/pbi.13701.
- Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 5th edition. New York: Oxford University Press; 2015. 944 p. DOI: 10.1093/acprof:oso/9780198717478.001.0001.
- Koppenol WH. The centennial of the Fenton reaction. Free Radical Biology and Medicine. 1993;15(6):645–651. DOI: 10.1016/0891-5849(93)90168-t.
- Lee DH, Lal NK, Lin Z-JD, Ma S, Liu J, Castro B, et al. Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nature Communications. 2020;11(1):1838. DOI: 10.1038/s41467-020-15601-5.
- Byeong-ha Lee, Hojoung Lee, Liming Xiong, Jian-Kang Zhu. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. The Plant Cell. 2002;14(6):1235–1251. DOI: 10.1105/tpc.010433.
- Edreva A, Yordanov I, Kardjieva R, Gesheva E. Heat shock responses of bean plants: involvement of free radicals, antioxidants and free radical /active oxygen scavenging systems. Biologia Plantarum. 1998;41:185–191. DOI: 10.1023/A:1001846009471.
- Chengrun Wang, Xiaorong Wang, Yuan Tian, Yingang Xue, Xianghua Xu, Yunxia Sui, et al. Oxidative stress and potential biomarkers in tomato seedlings subjected to soil lead contamination. Ecotoxicology and Environmental Safety. 2008;71(3):685–691. DOI: 10.1016/j.ecoenv.2008.01.002.
- Ning Hui Song, Xiao Le Yin, Guo Feng Chen, Hong Yang. Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere. 2007;68(9):1779–1787. DOI: 10.1016/j.chemosphere.2007.03.023.
- Vera-Estrella R, Blumwald E, Higgins VJ. Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells 1: evidence for the involvement of active oxygen species. Plant Physiology. 1992;99(3):1208–1215. DOI: 10.1104/pp.99.3.1208.
- Garcia-Mata C, Wang J, Gajdanowicz P, Gonzalez W, Hills A, Donald N, et al. A minimal cysteine motif required to activate the SKOR K channel of Arabidopsis by the reactive oxygen species H2O2. The Journal of Biological Chemistry. 2010; 285(38):29286–29294. DOI: 10.1074/jbc.M110.141176.
- Demidchik V. Cation channels are sensors of ROS and oxidative stress in plants. In: Proceedings of 4th International symposium on plant signaling and behaviour; 2016 June 19–24; Saint Petersburg, Russia. Saint Petersburg: SINEL Co. Ltd.; 2016. p. 55–56.
- Makavitskaya M, Svistunenko D, Navaselsky I, Hryvusevich P, Mackievic V, Rabadanova C, et al. Novel roles of ascorbate in plants: induction of cytosolic Ca2+ signals and efflux from cells via anion channels. Journal of Experimental Botany. 2018;69(14):3477–3489. DOI: 10.1093/jxb/ery056.
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