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Environmental Science

A single seed treatment mediated through reactive oxygen species increases germination, growth performance, and abiotic stress tolerance in Arabidopsis and rice

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Pages 2597-2608 | Received 04 Jun 2020, Accepted 06 Aug 2020, Published online: 28 Aug 2020

References

  • Perdomo JA, Conesa MA, Medrano H, et al. Effects of long-term individual and combined water and temperature stress on the growth of rice, wheat and maize: relationship with morphological and physiological acclimation. Physiol Plant. 2015;155(2):149–165.
  • Silva EN, Vieira SA, Ribeiro RV, et al. Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat. J Plant Growth Regul. 2012;32(1):159–169.
  • Suzuki N, Rivero RM, Shulaev V, et al. Abiotic and biotic stress combinations. New Phytol. 2014;203(1):32–43.
  • Downing TE. The effects of climate change on agriculture and food security. Renew Energy. 1993;3(4–5):491–497.
  • Duke SH, Schrader LE, Miller MG. Low temperature effects on soybean (Glycine max [L.] Merr. cv. Wells) mitochondrial respiration and several dehydrogenases during imbibition and germination. Plant Physiol. 1977;60(5):716–722.
  • Hatfield JL, Egli DB. Effect of temperature on the rate of soybean hypocotyl elongation and field emergence. Crop Sci. 1974;14(3):423–426.
  • Leopold AC. Temperature effects on soybean imbibition and leakage. Plant Physiol. 1980;65(6):1096–1098.
  • Gill PK, Sharma AD, Singh P, et al. Changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Growth Regul. 2003;40(2):157–162.
  • Khan MSA, Hamid A, Karim MA. Effect of sodium chloride on germination and seedling characters of different types of rice (Oryza sativa L.). J Agron Crop Sci. 1997;179(3):163–169.
  • Zhang WJ, Niu Y, Bu SH, et al. Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage. PLoS One. 2014;9(1):e84750.
  • Kan G, Ning L, Li Y, et al. Identification of novel loci for salt stress at the seed germination stage in soybean. Breed Sci. 2016;66(4):530–541.
  • Mickky BM, Aldesuquy HS. Impact of osmotic stress on seedling growth observations, membrane characteristics and antioxidant defense system of different wheat genotypes. Egypt J Basic Appl Sci. 2019;4(1):47–54.
  • Pratap V, Sharma YK. Impact of osmotic stress on seed germination and seedling growth in black gram (Phaseolus mungo). J Environ Biol. 2010;31(5):721–726.
  • Wright E. The effect of high temperatures on seed germination. J For. 1931;29(5):679–687.
  • Pagamas P, Nawata E. Effect of high temperature during the seed development on quality and chemical composition of chili pepper seeds. Jpn J Trop Agr. 2007;51(1):22–29.
  • Boyer JS, Westgate ME. Grain yields with limited water. J Exp Bot. 2004;55(407):2385–2394.
  • Prasad PVV, Pisipati SR, Momčilović I, et al. Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. J Agron Crop Sci. 2011;197(6):430–441.
  • Maraghni M, Gorai M, Neffati M. Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. S Afr J Bot. 2010;76(3):453–459.
  • Lobell DB, Field CB. Global scale climate–crop yield relationships and the impacts of recent warming. Environ Res Lett. 2007;2(1):014002.
  • Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11(1):15–19.
  • Ray DK, Gerber JS, MacDonald GK, et al. Climate variation explains a third of global crop yield variability. Nat Commun. 2015;6:5989.
  • Xiao Z, Ximing C. Climate change impacts on global agricultural land availability. Environ Res Lett. 2011;6(1):014014.
  • Pandey P, Irulappan V, Bagavathiannan MV, et al. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci. 2017;8:537.
  • Ahanger MA, Akram NA, Ashraf M, et al. Plant responses to environmental stresses-from gene to biotechnology. AoB Plants. 2017;9(4):plx025.
  • Savvides A, Ali S, Tester M, et al. Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci. 2016;21(4):329–340.
  • Zhang JZ, Creelman RA, Zhu JK. From laboratory to field: using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol. 2004;135(2):615–621.
  • Chen K, Arora R. Dynamics of the antioxidant system during seed osmopriming, post-priming germination, and seedling establishment in spinach (Spinacia oleracea). Plant Sci. 2011;180(2):212–220.
  • Chen K, Fessehaie A, Arora R. Dehydrin metabolism is altered during seed osmopriming and subsequent germination under chilling and desiccation in Spinacia oleracea L. cv. Bloomsdale: possible role in stress tolerance. Plant Sci. 2012;183:27–36.
  • Gill SS, Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signal Behav. 2010;5(1):26–33.
  • Hossain MA, Bhattacharjee S, Armin SM, et al. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci. 2015;6:420.
  • Parra-Lobato MC, Gomez-Jimenez MC. Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. J Exp Bot. 2011;62(13):4447–4465.
  • Tanou G, Molassiotis A, Diamantidis G. Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol. 2009;166(17):1904–1913.
  • Li L, Wang Y, Shen W. Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals. 2012;25(3):617–631.
  • Bethke PC, Jones RL. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 2001;25(1):19–29.
  • Kimura S, Kaya H, Kawarazaki T, et al. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta. 2012;1823(2):398–405.
  • Kobayashi M, Ohura I, Kawakita K, et al. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell. 2007;19(3):1065–1080.
  • Miller G, Schlauch K, Tam R, et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2009;2(84):ra45.
  • Queval G, Issakidis-Bourguet E, Hoeberichts FA, et al. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J. 2007;52(4):640–657.
  • Mittler R. ROS are good. Trends Plant Sci. 2017;22(1):11–19.
  • Richards SL, Wilkins KA, Swarbreck SM, et al. The hydroxyl radical in plants: from seed to seed. J Exp Bot. 2015;66(1):37–46.
  • Liszkay A, van der Zalm E, Schopfer P. Production of reactive oxygen intermediates (O2·-, H2O2, and ·OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 2004;136(2):3114–3123.
  • Schopfer P, Liszkay A, Bechtold M, et al. Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta. 2002;214(6):821–828.
  • Schopfer P. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J. 2001;28(6):679–688.
  • Muller K, Linkies A, Vreeburg RA, et al. In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol. 2009;150(4):1855–1865.
  • Olkowski AA, Laarveld B, Tanino KK, inventors; University of Saskatchewan, assignee. Enhancement and control of seed germination with compositions comprising a transition metal catalyst and an oxidant (CA2949750A1). Canada; 2014.
  • Matros A, Peshev D, Peukert M, et al. Sugars as hydroxyl radical scavengers: proof-of-concept by studying the fate of sucralose in Arabidopsis. Plant J. 2015;82(5):822–839.
  • Vreeburg RA, Airianah OB, Fry SC. Fingerprinting of hydroxyl radical-attacked polysaccharides by N-isopropyl-2-aminoacridone labelling. Biochem J. 2014;463(2):225–237.
  • Khorobrykh SA, Khorobrykh AA, Yanykin DV, et al. Photoproduction of catalase-insensitive peroxides on the donor side of manganese-depleted photosystem II: evidence with a specific fluorescent probe. Biochemistry. 2011;50(49):10658–10665.
  • Galano A, Macias-Ruvalcaba NA, Medina Campos ON, et al. Mechanism of the OH radical scavenging activity of nordihydroguaiaretic acid: a combined theoretical and experimental study. J Phys Chem B. 2010;114(19):6625–6635.
  • Deng S, Yu M, Wang Y, et al. The antagonistic effect of hydroxyl radical on the development of a hypersensitive response in tobacco. Febs J. 2010;277(24):5097–5111.
  • Uemura M, Joseph RA, Steponkus PL. Cold acclimation of Arabidopsis thaliana: effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 1995;109(1):15–30.
  • Hacisalihoglu G, Paine DH, Hilderbrand MB, et al. Embryo elongation and germination rates as sensitive indicators of lettuce seed quality: priming and aging studies. HortScience. 1999;34(7):1240–1243.
  • Mastouri F, Bjorkman T, Harman GE. Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology. 2010;100(11):1213–1221.
  • Silva-Correia J, Freitas S, Tavares RM, et al. Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods. 2014;10(1):7.
  • Joosen RV, Kodde J, Willems LA, et al. GERMINATOR: a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination. Plant J. 2010;62(1):148–159.
  • El-Kassaby YA, Moss I, Kolotelo D. et al. Seed germination: mathematical representation and parameters extraction. For Sci. 2008;54(2):220–227.
  • Soltani E, Ghaderi-Far F, Baskin CC, et al. Problems with using mean germination time to calculate rate of seed germination. Aust J Bot. 2015;63(8):631–635.
  • Liu S, Oshita S, Kawabata S, et al. Identification of ROS produced by nanobubbles and their positive and negative effects on vegetable seed germination. Langmuir. 2016;32(43):11295–11302.
  • Gondim FA, Gomes-Filho E, Lacerda CF, et al. Pretreatment with H2O2 in maize seeds: effects on germination and seedling acclimation to salt stress. Braz J Plant Physiol. 2010;22:103–112.
  • Liheng H, Zhiqiang G, Runzhi L. Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings. Afr J Biotechnol. 2009;8(22):6151–6157.
  • Wahid A, Perveen M, Gelani S, et al. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol. 2007;164(3):283–294.
  • Foreman J, Demidchik V, Bothwell JH, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422(6930):442–446.
  • Fry SC. Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J. 1998;332((Pt 2)(2)):507–515.
  • Orman-Ligeza B, Parizot B, de Rycke R, et al. RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development. 2016;143(18):3328–3339.
  • Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signalling. J Exp Bot. 2014;65(5):1229–1240.
  • Mittler R, Blumwald E. The roles of ROS and ABA in systemic acquired acclimation. Plant Cell. 2015;27(1):64–70.
  • Laohavisit A, Richards SL, Shabala L, et al. Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin1. Plant Physiol. 2013;163(1):253–262.
  • Demidchik V, Cuin TA, Svistunenko D, et al. Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci. 2010;123(Pt 9):1468–1479.
  • Renew S, Heyno E, Schopfer P, et al. Sensitive detection and localization of hydroxyl radical production in cucumber roots and Arabidopsis seedlings by spin trapping electron paramagnetic resonance spectroscopy. Plant J. 2005;44(2):342–347.
  • Pospisil P. Production of reactive oxygen species by photosystem II. Biochim Biophys Acta. 2009;1787(10):1151–1160.
  • Nagasaki-Takeuchi N, Miyano M, Maeshima M. A plasma membrane-associated protein of Arabidopsis thaliana AtPCaP1 binds copper ions and changes its higher order structure. J Biochem. 2008;144(4):487–497.
  • Schwarzlander M, Finkemeier I. Mitochondrial energy and redox signaling in plants. Antioxid Redox Signal. 2013;18(16):2122–2144.
  • Kubala S, Garnczarska M, Wojtyla L, et al. Deciphering priming-induced improvement of rapeseed (Brassica napus L.) germination through an integrated transcriptomic and proteomic approach. Plant Sci. 2015;231:94–113.

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