Abstract
The present study was carried out to investigate the effect of individual drought, heat, and combined drought and heat stress on tomato plants. Combined stress resulted in the higher accumulation of Proline (101.9%), MDA (38.55%), H2O2 (101.19%), and lower levels of RWC (53.84%). Individual drought and heat stress decreased photosynthetic pigments like total chlorophyll content by (45.45%) and (25.35%), respectively, higher rates of pigment reduction (79.42%) were observed under combined drought and heat stress. Combined stress decreased PSII efficiency (Fv/Fm), quantum yield (ΦPSII), and photochemical efficiency (qp) and increased non-photochemical quenching (NPQ) levels. Moreover, the gas exchange parameters E, A, and Pn decreased by 5.36%, 36.45%, and 51.00%, respectively, in comparison to control plants. Antioxidant enzymes, SOD, APX, CAT, and GR showed a two- to threefold increase under combined drought and heat stress; however, the non-enzymatic antioxidants AsA and GSH displayed one–twofold increase under combined stress. Moreover, 2- to 2.5-fold decrease was observed in MDHAR and DHAR enzyme transcripts under combined stress conditions. The transcripts corresponding to AsA–GSH pathway enzymes SOD, APX, GR, DHAR, and MDHAR were up-regulated by 8- to 12-fold under combined drought and heat. Furthermore, DREB and LEA transcripts were up-regulated under drought and combined stress and down-regulated under drought stress. In the same manner, HSP70 and HSP90 transcripts were up-regulated under heat and combined stress; however, the transcription levels got down-regulated under drought stress. Additionally, rbcL and RCA transcripts were down-regulated especially under combined stress in comparison to individual drought and heat conditions. PSIP680 relative expression levels were up-regulated under drought stress; however, the transcripts were down-regulated under heat and combined stress. Taken together, the results suggest that the combined stress has a predominant effect over individual stress.
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References
Agarwal P, Agarwal PK, Nair S, Sopory S, Reddy M (2007) Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. Mol Genet Genom 277:189–198
Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213. https://doi.org/10.1093/jxb/ers323
Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674. https://doi.org/10.1016/j.tplants.2010.08.002
Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2017) Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163–174. https://doi.org/10.1007/s00709-017-1140-x
Allakhverdiev SI et al (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49. https://doi.org/10.1078/0176-1617-00845
Alzahrani Y, Kuşvuran A, Alharby HF, Kuşvuran S, Rady MM (2018) The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicol Environ Saf 154:187–196. https://doi.org/10.1016/j.ecoenv.2018.02.057
Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wangggggg L (2016) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut. https://doi.org/10.1007/s11270-016-3187-2
Aprile A et al (2013) Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genom 14:821. https://doi.org/10.1186/1471-2164-14-821
Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466. https://doi.org/10.1111/j.1399-3054.2007.01029.x
Aref IM, Khan PR, Khan S, El-Atta H, Ahmed AI, Iqbal M (2016) Modulation of antioxidant enzymes in Juniperus procera needles in relation to habitat environment and dieback incidence. Trees 30:1669–1681. https://doi.org/10.1007/s00468-016-1399-0
Arend M, Brem A, Kuster TM, Günthardt-Goerg MS (2013) Seasonal photosynthetic responses of European oaks to drought and elevated daytime temperature. Plant Biol 15:169–176. https://doi.org/10.1111/j.1438-8677.2012.00625.x
Ashoub A, Baeumlisberger M, Neupaertl M, Karas M, Brüggemann W (2015) Characterization of common and distinctive adjustments of wild barley leaf proteome under drought acclimation, heat stress and their combination. Plant Mol Biol 87:459–471. https://doi.org/10.1007/s11103-015-0291-4
Asrar H, Hussain T, Hadi SMS, Gul B, Nielsen BL, Khan MA (2017) Salinity induced changes in light harvesting and carbon assimilating complexes of Desmostachya bipinnata (L.) Staph. Environ Exp Bot 135:86–95
Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KHM, Nayyar H (2014) Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Funct Plant Biol 41:1148. https://doi.org/10.1071/fp13340
Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev 2014:1–31. https://doi.org/10.1155/2014/360438
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413. https://doi.org/10.1071/bi9620413
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/bf00018060
Batra NG, Sharma V, Kumari N (2014) Drought-induced changes in chlorophyll fluorescence, photosynthetic pigments, and thylakoid membrane proteins of Vigna radiate. J Plant Interact 9:712–721
Batth R, Singh K, Kumari S, Mustafiz A (2017) Transcript profiling reveals the presence of abiotic stress and developmental stage specific ascorbate oxidase genes in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00198
Boyer JS (1982) Plant productivity and environment. Science 218:443–448. https://doi.org/10.1126/science.218.4571.443
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Brestic M, Zivcak M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. Molecular stress physiology of plants. Springer, India, pp 87–131
Čajánek M, Štroch M, Lachetová I, Kalina J, Spunda V (1998) Characterization of the photosystem II inactivation of heat-stressed barley leaves as monitored by the various parameters of chlorophyll a fluorescence and delayed fluorescence. J Photochem Photobiol B 47:39–45. https://doi.org/10.1016/s1011-1344(98)00197-3
Carvalho LSC, Vidigal PC, Amancio S (2015) Oxidative stress homeostasis in grapevine (Vitis vinifera L.). Front Environ Sci. https://doi.org/10.3389/fenvs.2015.00020
Chaves MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384. https://doi.org/10.1093/jxb/erh269
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239. https://doi.org/10.1071/fp02076
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Chew YH, Halliday KJ (2011) A stress-free walk from Arabidopsis to crops. Curr Opin Biotechnol 22:281–286. https://doi.org/10.1016/j.copbio.2010.11.011
Choi HG, Moon BY, Kang NJ (2016) Correlation between strawberry (Fragaria ananassa Duch.) productivity and photosynthesis-related parameters under various growth conditions. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01607
Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248. https://doi.org/10.1016/j.plantsci.2004.07.039
Cvikrová M, Gemperlová L, Martincová O, Vanková R (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiol Biochem 73:7–15. https://doi.org/10.1016/j.plaphy.2013.08.005
Dąbrowski P et al (2019) Exploration of chlorophyll a fluorescence and plant gas exchange parameters as indicators of drought tolerance in perennial ryegrass. Sensors 19:2736
Dar MI, Naikoo MI, Rehman F, Naushin F, Khan FA (2016) Proline accumulation in plants: roles in stress tolerance and plant development. Springer India. https://doi.org/10.1007/978-81-322-2616-1_9
Demirevska K, Simova-Stoilova L, Fedina I, Georgieva K, Kunert K (2010) Response of oryzacystatin I transformed tobacco plants to drought heat and light stress. J Agron Crop Sci 196:90–99. https://doi.org/10.1111/j.1439-037x.2009.00396.x
Digrado A et al (2017) Long-term measurements of chlorophyll a fluorescence using the JIP-test show that combined abiotic stresses influence the photosynthetic performance of the perennial ryegrass (Lolium perenne) in a managed temperate grassland. Physiol Plant 161:355–371
Dreesen FE, De Boeck HJ, Janssens IA, Nijs I (2012) Summer heat and drought extremes trigger unexpected changes in productivity of a temperate annual/biannual plant community. Environ Exp Bot 79:21–30. https://doi.org/10.1016/j.envexpbot.2012.01.005
Duxbury AC, Yentsch CS (1956) Plankton pigment nomographs. J Air Pollut Contr Assoc 16:145–150
Faseela P, Puthur JT (2018) The imprints of the high light and UV-B stresses in Oryza sativa L. ‘Kanchana’ seedlings are differentially modulated. J Photochem Photobiol B Biol 178:551–559
Feng B, Liu P, Li G, Dong ST, Wang FH, Kong LA, Zhang JW (2014) Effect of heat stress on the photosynthetic characteristics in flag leaves at the grain-filling stage of different heat-resistant winter wheat varieties. J Agron Crop Sci 200:143–155
Foyer C (1989) Responses of photosynthesis and the xanthophyll and ascorbate-glutathione cycles to changes in irradiance, photoinhibition and recovery. Plant Physiol Biochem 27:751–760
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/bf00386001
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
Gao S, Yuan L, Zhai H, Liu C, He S, Liu Q (2011) Transgenic sweetpotato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tissue Organ Cult (PCTOC) 107:205–213. https://doi.org/10.1007/s11240-011-9971-1
García-Gómez C, Obrador A, González D, Babín M, Fernández MD (2017) Comparative effect of ZnO NPs, ZnO bulk and ZnSO4 in the antioxidant defences of two plant species growing in two agricultural soils under greenhouse conditions. Sci Total Environ 589:11–24. https://doi.org/10.1016/j.scitotenv.2017.02.153
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Grigorova B, Vaseva II, Demirevska K, Feller U (2011) Expression of selected heat shock proteins after individually applied and combined drought and heat stress. Acta Physiol Plant 33:2041–2049. https://doi.org/10.1007/s11738-011-0733-9
Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836. https://doi.org/10.1016/j.plaphy.2006.10.024
Hall AE (2010) Breeding for Heat Tolerance. Wiley. doi: 10.1002/9780470650011.ch5
Harb A, Awad D, Samarah N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare L.) under controlled severe drought. J Plant Interact 10:109–116. https://doi.org/10.1080/17429145.2015.1033023
Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467. https://doi.org/10.1111/j.1365-3040.1993.tb00893.x
Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiate. Environ Exp Bot 69:105–112. https://doi.org/10.1016/j.envexpbot.2010.03.004
Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66:3339–3352. https://doi.org/10.1093/jxb/erv142
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052. https://doi.org/10.1111/j.1365-313x.2010.04124.x
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. https://doi.org/10.1139/b79-163
Hniličková H, Hnilička F, Martinkova J, Kraus K (2017) Effects of salt stress on water status, photosynthesis and chlorophyll fluorescence of rocket. Plant Soil Environ 63:362–367
Hossain Z, López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166:1391–1404. https://doi.org/10.1016/j.jplph.2009.02.012
Hundertmark M, Hincha DK (2008) LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118. https://doi.org/10.1186/1471-2164-9-118
Jiang Y, Huang B (2001) Physiological responses to heat stress alone or in combination with drought: a comparison between tall fescue and perennial ryegrass. HortScience 36:682–686. https://doi.org/10.21273/hortsci.36.4.682
Johnson SM, Lim F-L, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genom 15:456. https://doi.org/10.1186/1471-2164-15-456
Joshi P, Swami A (2009) Air pollution induced changes in the photosynthetic pigments of selected plant species. J Environ Biol 30:295–298
Kalaji HM et al (2018) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56:953–961
Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619. https://doi.org/10.1007/s10535-015-0549-3
Khatri K, Rathore MS (2019) Photosystem photochemistry, prompt and delayed fluorescence, photosynthetic responses and electron flow in tobacco under drought and salt stress. Photosynthetica 57:61–74
Koussevitzky S et al (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203. https://doi.org/10.1074/jbc.m806337200
Krasteva V et al (2013) Drought induced damages of photosynthesis in bean and plantain plants analyzed in vivo by chlorophyll a fluorescence Bulg. J Plant Physiol 19:39–44
Li C-X, Feng S-L, Shao Y, Jiang L-N, Lu X-Y, Hou X-L (2007) Effects of arsenic on seed germination and physiological activities of wheat seedlings. J Environ Sci 19:725–732. https://doi.org/10.1016/s1001-0742(07)60121-1
Li X et al (2014) Comparative physiological and proteomic analyses of poplar (Populus yunnanensis) plantlets exposed to high temperature and drought. PLoS ONE 9:e107605. https://doi.org/10.1371/journal.pone.0107605
Li M et al (2016) Brassinosteroid ameliorates zinc oxide nanoparticles-induced oxidative stress by improving antioxidant potential and redox homeostasis in tomato seedling. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00615
Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. Int Agrophys 27:463–477. https://doi.org/10.2478/intag-2013-0017
Liu S, Chen C, Chen G, Cao B, Chen Q, Lei J (2012) RNA-sequencing tag profiling of the placenta and pericarp of pungent pepper provides robust candidates contributing to capsaicinoid biosynthesis. Plant Cell Tissue Organ Cult (PCTOC) 110:111–121. https://doi.org/10.1007/s11240-012-0135-8
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Maclachlan S, Zalik S (1963) Plastid structure, chlorophyll concentration, and free amino acid composition of a chlorophyll mutant of barley. Can J Bot 41:1053–1062
Martinazzo EG, Ramm A, Bacarin MA (2012) The chlorophyll a fluorescence as an indicator of the temperature stress in the leaves of Prunus persica. Braz J Plant Physiol 24:237–246
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19. https://doi.org/10.1016/j.tplants.2005.11.002
Moreno-Galván AE et al (2020) Proline accumulation and glutathione reductase activity induced by drought-tolerant rhizobacteria as potential mechanisms to alleviate drought stress in Guinea grass. Appl Soil Ecol 147:103367
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998
Murshed R, Lopez-Lauri F, Keller C, Monnet F, Sallanon H (2008) Acclimation to drought stress enhances oxidative stress tolerance in Solanum lycopersicum L. fruits. Plant Stress 2:145–151
Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration-and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
Nath M, Bhatt D, Prasad R, Gill SS, Anjum NA, Tuteja N (2016) Reactive oxygen species generation-scavenging and signaling during plant-arbuscular mycorrhizal and Piriformospora indica interaction under stress condition. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01574
Nurdiani D, Widyajayantie D, Nugroho S (2018) OsSCE1 encoding SUMO E2-conjugating enzyme involves in drought stress response of Oryza sativa. Rice Sci 25:73–81. https://doi.org/10.1016/j.rsci.2017.11.002
Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198. https://doi.org/10.1016/s1369-5266(02)00259-5
Pandey P, Singh J, Achary VMM, Reddy MK (2015) Redox homeostasis via gene families of ascorbate-glutathione pathway. Front Environ Sci. https://doi.org/10.3389/fenvs.2015.00025
Petrov P, Petrova A, Dimitrov I, Tashev T, Olsovska K, Brestic M, Misheva S (2018) Relationships between leaf morpho-anatomy, water status and cell membrane stability in leaves of wheat seedlings subjected to severe soil drought. J Agron Crop Sci 204:219–227
Prasad PVV, Staggenborg SA, Ristic Z, Ahuja LR, Reddy VR, Saseendran SA, Yu Q (2008) Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. Am Soc Agron Crop Sci. https://doi.org/10.2134/advagricsystmodel1.c11
Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162:1849–1866. https://doi.org/10.1104/pp.113.221044
Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157. https://doi.org/10.1016/j.envexpbot.2017.02.010
Rampino P et al (2012) Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiol Biochem 56:72–78
Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073
Rizhsky L (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151. https://doi.org/10.1104/pp.006858
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide the response of arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696. https://doi.org/10.1104/pp.103.033431
Rollins JA, Habte E, Templer SE, Colby T, Schmidt J, von Korff M (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J Exp Bot 64:3201–3212. https://doi.org/10.1093/jxb/ert158
Sainz M, Díaz P, Monza J, Borsani O (2010) Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to Photosystem II in combined drought-heat stressed Lotus japonicus. Physiol Plant 140:46–56. https://doi.org/10.1111/j.1399-3054.2010.01383.x
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009. https://doi.org/10.1006/bbrc.2001.6299
Salvucci ME, Crafts-Brandner SJ (2004a) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186. https://doi.org/10.1111/j.0031-9317.2004.0173.x
Salvucci ME, Crafts-Brandner SJ (2004b) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plant 122:513–519. https://doi.org/10.1111/j.1399-3054.2004.00419.x
Salvucci ME, Crafts-Brandner SJ (2004c) Relationship between the Heat Tolerance of Photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470. https://doi.org/10.1104/pp.103.038323
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302. https://doi.org/10.1016/j.pbi.2007.04.014
Sharma AP, Tripathi BD (2008) Biochemical responses in tree foliage exposed to coal-fired power plant emission in seasonally dry tropical environment. Environ Monit Assess 158:197–212. https://doi.org/10.1007/s10661-008-0573-2
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2012) Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence. Funct Plant Biol 39:936. https://doi.org/10.1071/fp12100
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2015) Wheat cultivars selected for high Fv/Fmunder heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol Plant 153:284–298. https://doi.org/10.1111/ppl.12245
Siddiqui MH, Al-Khaishany MY, Al-Qutami MA, Al-Whaibi MH, Grover A, Ali HM, Al-Wahibi MS (2015) Morphological and physiological characterization of different genotypes of faba bean under heat stress. Saudi J Biol Sci 22:656–663. https://doi.org/10.1016/j.sjbs.2015.06.002
Šprtová M, Nedbal L, Marek MV (2000) Effect of enhanced UVB radiation on chlorophyll a fluorescence parameters in Norway spruce needles. J Plant Physiol 156:234–241
Stirbet A, Lazár D, Kromdijk J (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses. Photosynthetica 56:86–104
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. https://doi.org/10.1111/nph.12797
Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314. https://doi.org/10.1007/s00425-005-0214-8
Upreti K, Murti G, Bhatt R (2000) Response of pea cultivars to water stress: changes in morphophysiological characters, endogenous hormones and yield. Veg Sci 27:57–61
Vadez V et al (2011) Adaptation of grain legumes to climate change: a review. Agron Sustain Dev 32:31–44. https://doi.org/10.1007/s13593-011-0020-6
Verma A, Singh SN (2006) Biochemical and ultrastructural changes in plant foliage exposed to auto-pollution. Environ Monit Assess 120:585–602. https://doi.org/10.1007/s10661-005-9105-5
Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688. https://doi.org/10.1093/treephys/tpq015
Yang X et al (2006) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733. https://doi.org/10.1007/s00425-006-0380-3
Yuan L-Y, Du J, Yuan Y-H, Shu S, Sun J, Guo S-R (2013) Effects of 24-epibrassinolide on ascorbate–glutathione cycle and polyamine levels in cucumber roots under Ca(NO3)2 stress. Acta Physiol Plant 35:253–262. https://doi.org/10.1007/s11738-012-1071-2
Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2017) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12
Zhou R, Yu X, Kjær KH, Rosenqvist E, Ottosen C-O, Wu Z (2015) Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ Exp Bot 118:1–11. https://doi.org/10.1016/j.envexpbot.2015.05.006
Zhou R et al (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol. https://doi.org/10.1186/s12870-017-0974-x
Zivcak M et al (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117(1–3):529–546
Acknowledgements
The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP-2019/116), King Saud University, Riyadh, Saudi Arabia.
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Researchers Supporting Project Number (RSP-2019/116), King Saud University, Riyadh, Saudi Arabia.
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VR, SUQ, and PA conceived the experimental design and VR, SUQ performed the experiments. MNA performed the statistical analysis. VR and SUQ wrote the first draft of the manuscript. MNA and PA revised the manuscript to present form. All authors read and approved the same for publication.
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Raja, V., Qadir, S.U., Alyemeni, M.N. et al. Impact of drought and heat stress individually and in combination on physio-biochemical parameters, antioxidant responses, and gene expression in Solanum lycopersicum. 3 Biotech 10, 208 (2020). https://doi.org/10.1007/s13205-020-02206-4
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DOI: https://doi.org/10.1007/s13205-020-02206-4