‘Omics’ approaches in developing combined drought and heat tolerance in food crops

Aberkane H, Payne T, Kishi M, Smale M, Amri A, Jamora N (2020) Transferring diversity of goat grass to farmers’ fields through the development of synthetic hexaploid wheat. Food Secur 12:1017–1033. https://doi.org/10.1007/s12571-020-01051-w

Acuña-Galindo MA, Mason RE, Subramanian NK, Hays DB (2015) Meta-analysis of wheat QTL regions associated with adaptation to drought and heat stress. Crop Sci 55:477–492

Ahmadi A, Baker DA (2001) The effect of water stress on the sucrose to starch pathway. J Plant Growth Regul 35:81–91. https://doi.org/10.1023/A:1013827600528

Alhaithloul HAS (2019) Impact of combined heat on drought stress on the potential growth responses of the desert grass Artemisia sieberi alba: relation to biochemical and molecular adaptation. Plants 8:1–25. https://doi.org/10.3390/plants8100416

Alhaithloul HA, Soliman MH, Ameta KL, El-Esawi MA, Elkelish A (2020) Changes in ecophysiology, osmolytes, and secondary metabolites of the medicinal plants of Mentha piperita and Catharanthus roseus subjected to drought and heat stress. Biomolecules 10:1–21. https://doi.org/10.3390/biom10010043

Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803. BBA Bioenerget 1657:23–32. https://doi.org/10.1016/j.bbabio.2004.03.003

Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycine betaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. BBA Bioenerget 1767:1363–1371. https://doi.org/10.1016/j.bbabio.2007.10.005

Alseekh S, Fernie AR (2018) Metabolomics 20 years on: what have we learned and what hurdles remain? Plant J 94:933–942

Altunoglu YC, Keles M, Tevfik Hasan CA, Baloglu MC (2019) Identification of watermelon heat shock protein members and tissue-specific gene expression analysis under combined drought and heat stresses. Turk J Biol 43:404–419

An Y, Zhou P, Liang J (2014) Effects of exogenous application of abscisic acid on membrane stability, osmotic adjustment, photosynthesis and hormonal status of two lucerne (Medicago sativa L.) genotypes under high temperature stress and drought stress. Crop Pasture Sci 65:274–286. https://doi.org/10.1071/CP13162

Anderson CM, Kohorn BD (2001) Inactivation of Arabidopsis SIP1 leads to reduced levels of sugars and drought tolerance. J Plant Physiol 158:1215–1219. https://doi.org/10.1078/S0176-1617(04)70149-2

Andersen MN, Asch F, Wu Y, Jensen CR, Næsted H, Mogensen VO, Koch KE (2002) Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol 130:591–604. https://doi.org/10.1104/pp.005637

Aprile A, Havlickova L, Panna R, Marè C, Borrelli GM, Marone D, Perrotta C, Rampino P, De Bellis L, Curn V, Mastrangelo AM (2013) Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics 14:1–8

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

Asthir B, Koundal A, Bains NS (2012) Putrescine modulates antioxidant defense response in wheat under high temperature stress. Biol Plant 56:757–761. https://doi.org/10.1007/s10535-012-0209-1

Athar HH, Shengnan M, Saddam H, Chen Y, Shafaqat A, Zhang S, Longchang W (2019) Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-40362-7

Awasthi R, Kaushal N, Vadez V, Turner NC, Berger J, Siddique KH (2014) Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea. Funct Plant Biol 41:1148–1167. https://doi.org/10.1071/FP1334031

Awasthi R, Gaur P, Turner NC (2017) Effects of individual and combined heat and drought stress during seed filling on the oxidative metabolism and yield of chickpea (Cicer arietinum) genotypes differing in heat and drought tolerance. Crop Pasture Sci 68:823–884. https://doi.org/10.1071/CP17028

Bahar B, Yildirim M, Barutcular C, Ibrahim GENC (2008) Effect of canopy temperature depression on grain yield and yield components in bread and durum wheat. Not Bot Horti Agrobot Cluj Napoca 36:34–37

Balla K, Bedo Z, Veisz O (2006) Effect of heat and drought stress on the photosynthetic processes of wheat. Cereal Res Commun 34:381–384

Balota M, Payne WA, Evett SR, Peters TR (2008) Morphological and physiological traits associated with canopy temperature depression in three closely related wheat lines. Crop Sci 48:1897–1910. https://doi.org/10.2135/cropsci2007.06.0317

Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38. https://doi.org/10.1111/j.1365-3040.2007.01727.x

Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375

Behboudian MH, Ma Q, Turner NC, Palta JA (2001) Reactions of chickpea to water stress: yield and seed composition. J Sci Food Agric 81:1288–1291. https://doi.org/10.1002/jsfa.939

Bennett D, Reynolds M, Mullan D, Izanloo A, Kuchel H, Langridge P, Schnurbusch T (2012) Detection of two major grain yield QTL in bread wheat (Triticum aestivum L.) under heat, drought and high yield potential environments. Theor Applied Genet 125:1473–1485

Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

Bing YI, Zhou YF, Gao MY, Zhang Z, Han Yi, Yang D, Huang RD (2014) Effect of drought stress during flowering stage on starch accumulation and starch synthesis enzymes in sorghum grains. J Integr Agric 13:2399–2406. https://doi.org/10.1016/S2095-3119(13)60694-2

Bita C, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. https://doi.org/10.3389/fpls.2013.00273

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

Bohra A, Jha UC, Godwin ID, Varshney RK (2020) Genomic interventions for sustainable agriculture. Plant Biotechnol J. https://doi.org/10.1111/pbi.13472

Bonos SA, Murphy JA (1999) Growth responses and performance of Kentucky bluegrass under summer stress. Crop Sci 39:770–774. https://doi.org/10.2135/cropsci1999.0011183X0039000300226x

Brenner ML, Cheikh N (1995) The role of hormones in photosynthate partitioning and seed filling. In: Davies PJ (ed) Plant hormones, 1st edn. Springer, Dordrecht, pp 649–670

Cabañero FJ, Martínez V, Carvajal M (2004) Does calcium determine water uptake under saline conditions in pepper plants, or is it water flux which determines calcium uptake? Plant Sci 166:443–450. https://doi.org/10.1016/j.plantsci.2003.10.010

Cairns JE, Audebert A, Townend J, Price AH, Mullins CE (2004) Effect of soil mechanical impedance on root growth of two rice varieties under field drought stress. Plant Soil 267:309–318

Cairns JE, Crossa C, Zaidi PH, Grudloyma P, Sanchez C, Araus JL (2013) Identification of drought, heat and combined drought and heat tolerance donors in maize (Zea mays L.). Crop Sci 53:1335–1346. https://doi.org/10.2135/cropsci2012.09.0545

Cantalapiedra CP, García-Pereira MJ, Gracia MP, Igartua E, Casas AM, Contreras-Moreira B (2017) Large differences in gene expression responses to drought and heat stress between elite barley cultivar Scarlett and a spanish landrace. Front Plant Sci 8:647

Carmo-Silva AE, Gore MA, Andrade-Sanchez P, French AN, Hunsaker DJ, Salvucci ME (2012) Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ Exp Bot 83:1–11. https://doi.org/10.1016/j.envexpbot.2012.04.001

Casaretto JA, El-kereamy A, Zeng B, Stiegelmeyer SM, Chen X, Bi YM, Rothstein SJ (2016) Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics 17:1–5

Chandra K, Prasad R, Thakur P, Madhukar K, Prasad LC (2017) Heat tolerance in wheat-a key strategy to combat climate change through molecular markers. Int J Curr Microbiol Appl Sci 6:662–675

Chen J, Xu W, Velten J, Xin Z, Stout J (2012) Characterization of maize inbred lines for drought and heat tolerance. J Soil Water Conserv 67:354–364

Chew YH, Halliday KJ (2011) A stress-free walk from Arabidopsis to crops. Curr Opin Biotech 22:281–286. https://doi.org/10.1016/j.copbio.2010.11.011

Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechol Lett 31:597–606

Cohen I, Zandalinas SI, Huck C, Fritschi FB, Mittler R (2020) Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiol Plant. https://doi.org/10.1111/ppl.13203

Conde A, Chaves MM, Gerós H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 52:1583–1602. https://doi.org/10.1093/pcp/pcr107

Condon AG, Reynolds MP, Rebetzke GJ, Van Ginkel M, Richards RA, Farquhar GD (2007) Using stomatal aperture-related traits to select for high yield potential in bread wheat. Springer, Dodrecht, pp 617–624

Crafts-Brandner SJ, Salvucci ME (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol 129:1773–1780. https://doi.org/10.1104/pp.002170

Cvikrova M, Gemperlova L, Martincova O, Vankova 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

Das A, Eldakak M, Paudel B, Kim DW, Hemmati H, Basu C, Rohila JS (2016) Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. BioMed Res Int. https://doi.org/10.1155/2016/6021047

Diksaityt A, Viršilė A, Žaltauskaitė J, Januškaitienė I, Juozapaitienė G (2019) Growth and photosynthetic responses in Brassica napus differ during stress and recovery periods when exposed to combined heat, drought and elevated CO2. Plant Physiol Biochem 142:59–72. https://doi.org/10.1016/j.plaphy.2019.06.026

Djanaguiraman M, Perumal R, Jagadish SVK, Ciampitti IA, Welti R, Prasad PVV (2018) Sensitivity of sorghum pollen and pistil to high-temperature stress. Plant Cell Environ 41:1065–1082. https://doi.org/10.1111/pce.13089

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

Duan H, Wu J, Huang G, Zhou S, Liu W, Liao Y, Fan H (2017) Individual and interactive effects of drought and heat on leaf physiology of seedlings in an economically important crop. AoB Plants 9:1–16. https://doi.org/10.1093/aobpla/plw090

Egert M, Tevini M (2002) Influence of drought on some physiological parameters symptomatic for oxidative stress in leaves of chives (Allium schoenoprasum). Environ Exp Bot 48:43–49. https://doi.org/10.1016/S0098-8472(02)00008-4

El-Esawi MA, Alayafi AA (2019) Overexpression of rice Rab7 gene improves drought and heat tolerance and increases grain yield in rice (Oryza sativa L.). Genes 10:56. https://doi.org/10.3390/genes10010056

El-Esawi MA, Al-Ghamdi AA, Ali HM, Ahmad M (2019) Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestivum L.). Genes 10:163. https://doi.org/10.3390/genes10020163

Elferjani R, Soolanayakanahally R (2018) Canola responses to drought, heat, and combined stress: shared and specific effects on carbon assimilation, seed yield, and oil composition. Front Plant Sci 9:1–17. https://doi.org/10.3389/fpls.2018.01224

El-haddad N, Rajendran K, Smouni A, Es-Safi NE, Benbrahim N, Mentag R, Nayyar H, Maalouf F, Kumar S (2020) Screening the FIGS set of lentil (Lens culinaris Medikus) germplasm for tolerance to terminal heat and combined drought and heat stress. Agronomy 10:1036

Esmaeili N, Yang X, Cai Y, Sun L, Zhu X, Shen G, Payton P, Fang W, Zhang H (2019) Co-overexpression of AVP1 and OsSIZ1 in Arabidopsis substantially enhances plant tolerance to drought, salt, and heat stresses. Sci Rep 9;1–5.

Esmaeili N, Cai Y, Tang F, Zhu X, Smith J, Mishra N, Hequet E, Ritchie G, Jones D, Shen G, Payton P (2021) Towards doubling fibre yield for cotton in the semiarid agricultural area by increasing tolerance to drought, heat and salinity simultaneously. Plant Biotechnol J 19:462–476. https://doi.org/10.1111/pbi.13476

Fábián A, Sáfrán E, Szabó-Eitel G, Barnabás B, Jäger K (2019) Stigma functionality and fertility are reduced by heat and drought co-stress in wheat. Front Plant Sci 10:1–18. https://doi.org/10.3389/fpls.2019.00244

Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017a) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1–16. https://doi.org/10.3389/fpls.2017.01147

Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Huang J (2017b) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147. https://doi.org/10.3389/fpls.2017.01147

Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803–6817

Fang Y, Du Y, Wang J, Wu A, Qiao S, Xu B, Zheng S, Siddique KHM, Chen Y (2017) Moderate drought stress affected root growth and grain yield in old, modern and newly released cultivars of winter wheat. Front Plant Sci 8:1–14. https://doi.org/10.3389/fpls.2017.00672

Farooq M, Bramley H, Palta JA, Siddique KH (2011) Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30:491–507. https://doi.org/10.1080/07352689.2011.615687

Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2017) Drought stress in grain legumes during reproduction and grain filling. J Agron Crop Sci 203:81–102. https://doi.org/10.1111/jac.12169

Farooq M, Wahid A, Basra SMA (2009) Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 195:262–269. https://doi.org/10.1111/j.1439-037X.2009.00368.x

Flexas J, Díaz-Espejo A, Berry JA, Cifre J, Galmés J, Kaldenhoff R, Ribas-Carbó M (2007) Analysis of leakage in IRGA’s leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. J Exp Bot 58:1533–1543. https://doi.org/10.1093/jxb/erm027

Foyer CH, Noctor G (2000) Tansley review No. 112: oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388. https://doi.org/10.1046/j.1469-8137.2000.00667.x

França MG, Thi C, Pimentel ATP, Rossiello C, Pereyra RO, Zuily-Fodil Y, Laffray D (2000) Differences in growth and water relations among Phaseolus vulgaris cultivars in response to induced drought stress. Environ Exp Bot 43:227–237. https://doi.org/10.1016/S0098-8472(99)00060-X

Garcia M, Eckermann P, Haefele S, Satija S, Sznajder B, Timmins A, Baumann U, Wolters P, Mather DE, Fleury D (2019) Genome-wide association mapping of grain yield in a diverse collection of spring wheat (Triticum aestivum L.) evaluated in southern Australia. PLoS ONE 14:e0211730

Garg BK (2003) Nutrient uptake and management under drought: nutrient-moisture interaction. Curr Agric 27:1–8

Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought-and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615. https://doi.org/10.1104/pp.16.00434

Giri A, Heckathorn S, Mishra S, Krause C (2017) Heat stress decreases levels of nutrient-uptake and -assimilation proteins in tomato roots. Plants 6:1–15. https://doi.org/10.3390/plants6010006

Grigorova B, Vaseva I, Demirevska K, Feller U (2011a) Combined drought and heat stress in wheat: changes in some heat shock proteins. Biol Plant 55:105–111. https://doi.org/10.1007/s10535-011-0014-x

Grigorova B, Vaseva II, Demirevska K, Feller U (2011b) Expression of selected heat shock proteins after individually applied and combined drought and heat stress. Acta Physiol Plant 33:2041–2049

Guidi L, Lo Piccolo E, Landi M (2019) Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Front Plant Sci 10:1–11. https://doi.org/10.3389/fpls.2019.00174

Hamidou F, Halilou O, Vadez V (2013) Assessment of groundnut under combined heat and drought stress. J Agron Crop Sci 199:1–1

Handayani T, Watanabe K (2020) The combination of drought and heat stress has a greater effect on potato plants than single stresses. Plant Soil Environ 66(4):175–182. https://doi.org/10.17221/126/2020-PSE

Hanif S, Saleem MF, Sarwar M, Irshad M, Shakoor A, Wahid MA, Khan HZ (2020) Biochemically triggered heat and drought stress tolerance in rice by proline application. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10095-3

Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448. https://doi.org/10.1104/pp.124.3.1437

He GH, Xu JY, Wang YX, Liu JM, Li PS, Chen M, Ma YZ, Xu ZS (2016) Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biol 16:1–6

Heckathorn SA, Giri A, Mishra S, Bista D (2013) Heat stress and roots. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley, Weinheim, pp 109–136

Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162. https://doi.org/10.1016/j.tplants.2009.01.002

Hossain A, da Silva JA, Lozovskaya MV, Zvolinsky VP (2012) High temperature combined with drought affect rainfed spring wheat and barley in South-Eastern Russia: I. Phenology and growth. Saud J Biol Sci 19:473–487

Hu X, Liu R, Li Y, Wang W, Tai F, Xue R, Li C (2010) Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul 60:225–235. https://doi.org/10.1007/s10725-009-9436-2

Huang B, Rachmilevitch S, Xu J (2012) Root carbon and protein metabolism associated with heat tolerance. J Exp Bot 63:3455–3465. https://doi.org/10.1093/jxb/ers003

Hussain HA, Men S, Hussain S, Chen Y, Ali S, Zhang S, Wang L (2019a) Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-40362-7

Hussain HA, Men S, Hussain S, Chen Y, Ali S, Zhang S, Zhang K, Li Y, Xu Q, Liao C, Wang L (2019b) Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-40362-7

Iglesias-Acosta M, Martínez-Ballesta MC, Teruel JA, Carvajal M (2010) The response of broccoli plants to high temperature and possible role of root aquaporins. Environ Exp Bot 68:83–90. https://doi.org/10.1016/j.envexpbot.2009.10.007

Ionenko IF, Anisimov AV, Dautova NR (2010) Effect of temperature on water transport through aquaporins. Biol Plant 54:488–494. https://doi.org/10.1007/s10535-010-0086-z

IPCC (2014) Climate change 2014: impacts, adaptation and vulnerability. Working group II contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

Jagadish SVK, Muthurajan R, Oane R, Wheeler TR, Heuer S, Bennett J (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot 61:143–156. https://doi.org/10.1093/jxb/erp289

Jagadish SVK, Muthurajan R, Rang ZW et al (2011) Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice 4:1–11

Jain M, Prasad PV, Boote KJ, Hartwell AL, Chourey PS (2007) Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L Moench). Planta 227:67–79. https://doi.org/10.1007/s00425-007-0595-y

Janni M, Gullì M, Maestri E, Marmiroli M, Valliyodan B, Nguyen HT, Marmiroli N (2020) Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity. J Exp Bot 71:3780–3802

Jedmowski C, Ashoub A, Momtaz O, Brüggemann W (2015) Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). J Bot 2015:1–9. https://doi.org/10.1155/2015/120868

Jiang Y, Huang B (2000) Effects of drought or heat stress alone and in combination on Kentucky bluegrass. Crop Sci 40:1358–1362. https://doi.org/10.2135/cropsci2000.4051358x

Jiang Y, Huang B (2001a) Physiological responses to heat stress alone or in combination with drought: a comparison between tall fescue and perennial ryegrass. Hort Sci 36(4):682–686. https://doi.org/10.21273/HORTSCI.36.4.682

Jiang Y, Huang B (2001b) Physiological responses to heat stress alone or in combination with drought: a comparison between tall fescue and perennial ryegrass. Hort Science 36:682–686. https://doi.org/10.21273/HORTSCI.36.4.682

Jiang Y, Davis AR, Vujanovic V, Bueckert RA (2019) Reproductive development response to high daytime temperature in field pea. J Agron Crop Sci 205:324–333. https://doi.org/10.1111/jac.12328

Jin R, Shi H, Han C, Zhong B, Wang Q, Chan Z (2015) Physiological changes of purslane (Portulaca oleracea L.) after progressive drought stress and rehydration. Sci Hortic 194:215–221. https://doi.org/10.1016/j.scienta.2015.08.023

Johnson SM, Lim F, Finkler A et al (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics 15:456

Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1, 5-bisphosphate carboxylase/oxygenase. Planta 161:308–313. https://doi.org/10.1007/BF00398720

Jumrani K, Bhatia VS (2018) Impact of combined stress of high temperature and water deficit on growth and seed yield of soybean. Physiol Mol Biol Plants 24:37–50

Kaloki P, Trethowan R, Tan DK (2019) Effect of genotype× environment× management interactions on chickpea phenotypic stability. Crop Pasture Sci 70:453–462. https://doi.org/10.1071/CP18547

Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperature stress. Plant Physiol 126:120–128. https://doi.org/10.1111/j.1399-3054.2006.00604.x

Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Krishna H, Chandra S, Vadez V, Serraj R (2005) Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Euphytica 146:213–222. https://doi.org/10.1016/j.fcr.2005.02.012

Kebede H, Fisher DK, Young LD (2012) Determination of moisture deficit and heat stress tolerance in corn using physiological measurements and a low-cost microcontroller-based monitoring system. J Agron Crop Sci 198:118–129

Khan MS, Yu X, Kikuchi A, Asahina M, Watanabe KN (2009) Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol J 26:125–134. https://doi.org/10.5511/plantbiotechnology.26.125

Khan AR, Cheng Z, Ghazanfar B, Khan MA, Yongxing Z (2014) Acetyl salicylic acid and 24-epibrassinolide enhance root activity and improve root morphological features in tomato plants under heat stress. Acta Agric Scand B Soil Plant Sci 64:304–311. https://doi.org/10.1080/09064710.2014.906645

Kilian B, Dempewolf H, Guarino L, Werner P, Coyne C, Warburton ML (2021) Crop Science special issue: adapting agriculture to climate change: a walk on the wild side. Crop Sci 61:32–36. https://doi.org/10.1002/csc2.20418

Killi D, Bussotti F, Raschi A, Haworth M (2017) Adaptation to high temperature mitigates the impact of water deficit during combined heat and drought stress in C3 sunflower and C4 maize varieties with contrasting drought tolerance. Physiol Plant 159:130–147. https://doi.org/10.1111/ppl.12490

Killi D, Raschi A, Bussotti F (2020) Lipid peroxidation and chlorophyll fluorescence of photosystem II performance during drought and heat stress is associated with the antioxidant capacities of C3 sunflower and C4 maize varieties. Int J Mol Sci 21:1–21. https://doi.org/10.3390/ijms21144846

Kishor PK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KS, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88(3):424–438

Kitajima MBWL, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta Bioenerg 376:105–115. https://doi.org/10.1016/0005-2728(75)90209-1

Koevoets IT, Venema JH, Elzenga JT, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1–19. https://doi.org/10.3389/fpls.2016.01335

Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Mittler R (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

Kumar S, Kaushal N, Nayyar H, Gaur P (2012) Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. Acta Physiol Plant 34:1651–1658. https://doi.org/10.1007/s11738-012-0959-1

Kumar AN, Vijayalakshmi C, Vijayalakshmi D (2014) Chlorophyll and chlorophyll fluorescence as influenced by combined heat and drought stress in rice. Trends Biosci 7:1461–1465

Kumar J, Sen Gupta D, Djalovic I (2020) Breeding, genetics, and genomics for tolerance against terminal heat in lentil: current status and future directions. Legum 2:1–9. https://doi.org/10.1002/leg3.38

Kumari M, Pudake RN, Singh VP, Joshi AK (2013) Association of staygreen trait with canopy temperature depression and yield traits under terminal heat stress in wheat (Triticum aestivum L.). Euphytica 190:87–97. https://doi.org/10.1007/s10681-012-0780-3

Kumazaki A, Suzuki N (2019) Enhanced tolerance to a combination of heat stress and drought in Arabidopsis plants deficient in ICS1 is associated with modulation of photosynthetic reaction center proteins. Physiol Plant 165:232–246

Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:1–14. https://doi.org/10.3389/fchem.2018.00026

Lauriano JA, Lidon FC, Carvalho CA, Campos PS, do Céu Matos M, (2000) Drought effects on membrane lipids and photosynthetic activity in different peanut cultivars. Photosynthetica 38:7–12. https://doi.org/10.1023/A:1026775319916

Lawas LMF, Shi W, Yoshimoto MM, Hasegawa T, Hincha DK, Zuther E, Jagadish SK (2018a) Combined drought and heat stress impact during flowering and grain filling in contrasting rice cultivars grown under field conditions. Field Crops Res 229:66–77. https://doi.org/10.1016/j.fcr.2018.09.009

Lawas LMF, Zuther E, Jagadish SVK et al (2018b) Molecular mechanisms of combined heat and drought stress resilience in cereals. Curr Opin Plant Biol 45:212–217

Lawas LM, Li X, Erban A, Kopka J, Jagadish SK, Zuther E, Hincha DK (2019) Metabolic responses of rice cultivars with different tolerance to combined drought and heat stress under field conditions. GigaSci 8:giz050

Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294. https://doi.org/10.1046/j.0016-8025.2001.00814.x

Leopold AC, Musgrave ME, Williams KM (1981) Solute leakage resulting from leaf desiccation. Plant Physiol 68:1222–1225. https://doi.org/10.1104/pp.68.6.1222

Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125

Li Z, Hu Q, Zhou M, Vandenbrink J, Li D, Menchyk N, Reighard S, Norris A, Liu H, Sun D, Luo H (2013) Heterologous expression of OsSIZ1, a rice sumo E3 ligase, enhances broad abiotic stress tolerance in transgenic creeping bentgrass. Plant Biotech J 4:432–445

Li X, Yang Y, Sun X, Lin H, Chen J, Ren J, Yang Y (2014) Comparative physiological and proteomic analyses of poplar (Populus yunnanensis) plantlets exposed to high temperature and drought. PLoS ONE 9:1–15. https://doi.org/10.1371/journal.pone.0107605

Li R, Zeng Y, Xu J, Wang Q, Wu F, Cao M, Lan H, Liu Y, Lu Y (2015a) Genetic variation for maize root architecture in response to drought stress at the seedling stage. Breed Sci 65:298–307. https://doi.org/10.1270/jsbbs.65.298

Li X, Lawas LM, Malo R, Glaubitz U, Erban A, Mauleon R, Heuer S, Zuther E, Kopka J, Hincha DK, Jagadish KS (2015b) Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant Cell Environ 38:2171–2192. https://doi.org/10.1111/pce.12545

Li L, Mao X, Wang J, Chang X, Reynolds M, Jing R (2019) Genetic dissection of drought and heat-responsive agronomic traits in wheat. Plant Cell Environ 42:2540–2553

Liu X, Huang B (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci 40:503–510. https://doi.org/10.2135/cropsci2000.402503x

Liu X, Huang B (2008) Photosynthetic acclimation to high temperatures associated with heat tolerance in creeping bentgrass. J Plant Physiol 165:1947–1953. https://doi.org/10.1016/j.jplph.2008.05.001

Liu J, Xie X, Du J, Sun J, Bai X (2008) Effects of simultaneous drought and heat stress on Kentucky bluegrass. Sci Hortic 115:190–195. https://doi.org/10.1016/j.scienta.2007.08.003

Liu P, Guo W, Jiang Z, Pu H, Feng C, Zhu X, Peng Y, Kuang A, Little CR (2011) Effects of high temperature after anthesis on starch granules in grains of wheat (Triticum aestivum L.). J Agric Sci 149:159–169. https://doi.org/10.1017/S0021859610001024

Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:1–20

Liu Z, Qin J, Tian X, Xu S, Wang Y, Li H et al (2018) Global profiling of alternative splicing landscape responsive to drought, heat and their combination in wheat (Triticum aestivum L.). Plant Biotechnol J 16:714–726

Liu C, Sukumaran S, Claverie E, Sansaloni C, Dreisigacker S, Reynolds M (2019) Genetic dissection of heat and drought stress QTLs in phenology-controlled synthetic-derived recombinant inbred lines in spring wheat. Mol Breed 39:1–18. https://doi.org/10.1007/s11032-019-0938-y

Liu XH, Lyu YS, Yang W et al (2020) A membrane-associated NAC transcription factor OsNTL3 is involved in thermotolerance in rice. Plant Biotechnol J 18:1317–1329

Loka DA, Oosterhuis DM, Baxevanos D, Noulas C, Hu W (2020) Single and combined effects of heat and water stress and recovery on cotton (Gossypium hirsutum L.) leaf physiology and sucrose metabolism. Plant Physiol Biochem 148:166–179. https://doi.org/10.1016/j.plaphy.2020.01.015

Lynch JP, Brown KM (2001) Topsoil foraging-an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237. https://doi.org/10.1023/A:1013324727040

Machado S, Paulsen GM (2001) Combined effects of drought and high temperature water relations of wheat and sorghum. Plant Soil 233:179–187. https://doi.org/10.1023/A:1010346601643

Macková H, Hronková M, Dobrá J, Turečková V, Novák O, Lubovská Z, Motyka V, Haisel D, Hájek T, Prášil IT, Gaudinová A (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815

Mahalingam R, Bregitzer P (2019) Impact on physiology and malting quality of barley exposed to heat, drought and their combination during different growth stages under controlled environment. Physiol Plant 165:277–289. https://doi.org/10.1111/ppl.12841

Mahrookashani A, Siebert S, Hüging H, Ewert F (2017) Independent and combined effects of high temperature and drought stress around anthesis on wheat. J Agron Crop Sci 203:453–463. https://doi.org/10.1111/jac.12218

Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Biol 50:67–95. https://doi.org/10.1146/annurev.arplant.50.1.67

Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358. https://doi.org/10.1152/physrev.00008.2015

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659

Meseka S, Menkir A, Bossey B, Mengesha W (2018) Performance assessment of drought tolerant maize hybrids under combined drought and heat stress. Agronomy 8:274

Mickelbart MV, Hasegawa PM, Bailey-Serres J (2015) Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet 16:237–251

Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Breusegem FV, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67:3831–3844. https://doi.org/10.1093/jxb/erw080

Mishra N, Sun L, Zhu X, Smith J, Prakash Srivastava A, Yang X, Pehlivan N, Esmaeili N, Luo H, Shen G, Jones D, Auld D, Burke J, Payton P, Zhang H (2017) Overexpression of the rice sumo e3 ligase gene ossiz1 in cotton enhances drought and heat tolerance, and substantially improves fiber yields in the field under reduced irrigation and rainfed conditions. Plant Cell Physiol 58:735–746. https://doi.org/10.1093/pcp/pcx032

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 (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–21. https://doi.org/10.1016/j.tplants.2005.11.002

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009

Morris EC, Griffiths M, Golebiowska A, Mairhofer S, Burr-Hersey J, Goh T, Wangenheim DV, Atkinson B, Sturrock CJ, Lynch JP, Vissenberg K, Ritz K, Wells DM, Mooney SJ, Bennett MJ (2017) Shaping 3D root system architecture. Curr Biol 27(17):R919–R930. https://doi.org/10.1016/j.cub.2017.06.043

Mukamuhirwa A, Persson Hovmalm H, Bolinsson H, Ortiz R, Nyamangyoku O, Johansson E (2019) Concurrent drought and temperature stress in rice—a possible result of the predicted climate change: effects on yield attributes, eating characteristics, and health promoting compounds. Int J Environ Res Public Health 16:1–17. https://doi.org/10.3390/ijerph16061043

Nankishore A, Farrell AD (2016) The response of contrasting tomato genotypes to combined heat and drought stress. J Plant Physiol 202:75–82. https://doi.org/10.1016/j.jplph.2016.07.006

Nelimor C, Badu-Apraku B, Tetteh AY, N’guetta AY (2019) Assessment of genetic diversity for drought, heat and combined drought and heat stress tolerance in early maturing maize landraces. Plants 8:518

Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98:8777–8796. https://doi.org/10.1007/s00253-014-6020-0

Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Sarasa I, Yousf S, Araus JL, Cairns JE, Fernie AR (2015) Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 169:2665–2683

Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267. https://doi.org/10.1104/pp.97.3.1265

Oneto CD, Otegui ME, Baroli I, Beznec A, Faccio P, Bossio E, Lewi D (2016) Water deficit stress tolerance in maize conferred by expression of an isopentenyl transferase (IPT) gene driven by a stress-and maturation-induced promoter. J Biotechnol 220:66–77. https://doi.org/10.1016/j.jbiotec.2016.01.014

Onyemaobi I, Liu H, Siddique KH, Yan G (2017) Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat. Front Plant Sci 7:2071. https://doi.org/10.3389/fpls.2016.02071

Pan C, Yang D, Zhao X, Jiao C, Yan Y, Wang L-S, Q, Xu X, Fei Z, Lu G, (2018) Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway. Plant Cell Environ 42:1205–1221. https://doi.org/10.1111/pce.13444

Parry MA, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE, Alonso H, Whitney SM (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64:717–730. https://doi.org/10.1093/jxb/ers336

Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants—a review. Plant Soil Environ 54:89

Pasapula V, Shen G, Kuppu S, Paez-Valencia J, Mendoza M, Hou P, Chen J, Qiu X, Zhu L, Zhang X, Auld D (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought-and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9:88–99

Perdomo JA, Capó-Bauçà S, Carmo-Silva E, Galmés J (2017) Rubisco and rubisco activase play an important role in the biochemical limitations of photosynthesis in rice, wheat, and maize under high temperature and water deficit. Front Plant Sci 8:490. https://doi.org/10.3389/fpls.2017.00490

Pinto RS, Reynolds MP (2015) Common genetic basis for canopy temperature depression under heat and drought stress associated with optimized root distribution in bread wheat. Theor Appl Genet 128:575–585. https://doi.org/10.1007/s00122-015-2453-9

Pinto RS, Reynolds MP, Mathews KL, McIntyre CL, Olivares-Villegas JJ, Chapman SC (2010) Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects. Theor Appl Genet 121:1001–1021

Plaut Z, Butow BJ, Blumenthal CS, Wrigley CW (2004) Transport of dry matter into developing wheat kernels and its contribution to grain yield under post-anthesis water deficit and elevated temperature. Field Crops Res 86:185–198. https://doi.org/10.1016/j.fcr.2003.08.005

Pradhan GP, Prasad PV, Fritz AK, Kirkham MB, Gill BS (2012) Effects of drought and high temperature stress on synthetic hexaploid wheat. Funct Plant Biol 39:190–198

Prasad PVV, Pisipati SR, Momčilović I, Ristic Z (2011) 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 197:430–441. https://doi.org/10.1111/j.1439-037X.2011.00477.x

Premachandra GS, Saneoka H, Ogata S (1989) Nutrio-physiological evaluation of the polyethylene glycol test of cell membrane stability in maize. Crop Sci 29:1287–1292. https://doi.org/10.2135/cropsci1989.0011183X002900050040x

Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

Qaseem MF, Qureshi R, Muqaddasi QH, Shaheen H, Kousar R, Röder MS (2018) Genome-wide association mapping in bread wheat subjected to independent and combined high temperature and drought stress. PLoS ONE 13:e0199121

Qaseem MF, Qureshi R, Shaheen H (2019a) Effects of pre-anthesis drought, heat and their combination on the growth, yield and physiology of diverse wheat (Triticum aestivum L.) genotypes varying in sensitivity to heat and drought stress. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-43477-z

Qaseem MF, Qureshi R, Shaheen H, Shafqat N (2019b) Genome-wide association analyses for yield and yield-related traits in bread wheat (Triticum aestivum L) under pre-anthesis combined heat and drought stress in field conditions. PLoS ONE 14:1–22. https://doi.org/10.1371/journal.pone.0213407

Qin DD, Wu HY, Peng HR, Yao YY, Ni ZF, Li ZX, Zhou CL, Sun QX (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9:432

Qin H, Gu Q, Kuppu S, Sun L, Zhu X, Mishra N, Hu R, Shen G, Zhang J, Zhang Y, Zhu L (2013) Expression of the Arabidopsis vacuolar H+-pyrophosphatase gene AVP1 in peanut to improve drought and salt tolerance. Plant Biotechnol Rep 7:345–355. https://doi.org/10.1007/s11816-012-0269-5

Rahman H, Malik SA, Saleem M (2004) Heat tolerance of upland cotton during the fruiting stage evaluated using cellular membrane thermostability. Field Crops Res 85:149–158. https://doi.org/10.1016/S0378-4290(03)00159-X

Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37:255–263. https://doi.org/10.1071/FP09148

Raja V, Qadir SU, Alyemeni MN, Ahmad P (2020) Impact of drought and heat stress individually and in combination on physio-biochemical parameters, antioxidant responses, and gene expression in Solanum lycopersicum. 3 Biotech 10:1–18. https://doi.org/10.1007/s13205-020-02206-4

Rajendran K, Smouni A, Es-Safi NE, Benbrahim N, Mentag R, Nayyar H, Kumar S (2020) Screening the FIGS Set of Lentil (Lens culinaris Medikus) Germplasm for tolerance to terminal heat and combined drought-heat stress. Agronomy 10:1036. https://doi.org/10.3390/agronomy10071036

Rang ZW, Jagadish SVK, Zhou QM et al (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environ Exp Bot 70:58–65

Raza A (2020) Metabolomics: a systems biology approach for enhancing heat stress tolerance in plants. Plant Cell Rep 1–23

Rennenberg H, Loreto F, Polle A, Brilli F, Fares S, Beniwal R (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571. https://doi.org/10.1055/s-2006-924084

Reynolds MP, Nagarajan S, Razzaque MA, Ageeb OAA (2001) Heat tolerance. Application of physiology in wheat breeding. CIMMYT, pp 124–135

Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genome-wide association mapping of leaf metabolic pro les for dissecting complex traits in maize. Proc Natl Acad Sci USA 109:8872–8877

Rizhsky L, Liang H, Mittler R (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

Roca Paixão JF, Gillet FX, Ribeiro TP, Bournaud C, Lourenço-Tessutti IT, Noriega DD, Melo BP, de Almeida-Engler J, Grossi-de-Sa MF (2019) Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a histone acetyl transferase. Sci Rep 9:8080. https://doi.org/10.1038/s41598-019-44571-y

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

Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars: metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393. https://doi.org/10.4161/psb.4.5.8294

Ruan Y, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955. https://doi.org/10.1093/mp/ssq044

Sabagh AE, Hossain A, Islam MS, Barutcular C, Ratnasekera D, Gormus O, Hasanuzzaman M (2020) Drought and heat stress in cotton (Gossypium hirsutum L.): Consequences and their possible mitigation strategies. In: Hasanuzzaman M (ed) Agronomic crops. Springer, Singapore, pp 613–634

Saelim S, Zwiazek JJ (2000) Preservation of thermal stability of cell membranes and gas exchange in high temperature acclimated Xylia xylocarpa seedlings. J Plant Physiol 156:380–385. https://doi.org/10.1016/S0176-1617(00)80077-2

Safronov O, Kreuzwieser J, Haberer G, Alyousif MS, Schulze W, Al-Harbi N et al (2017) Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm). PLoS ONE 12:e0177883

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

Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171. https://doi.org/10.1046/j.0016-8025.2001.00790.x

Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827

Samakovli D, Tichá T, Vavrdová T, Ovečka M, Luptovčiak I, Zapletalová V, Kuchařová A, Křenek P, Krasylenko Y, Margaritopoulou T, Roka L, Milioni D, Komis G, Hatzopoulos P, Šamaj J (2020) YODA-HSP90 Module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis. Mol Plant 13:612–633. https://doi.org/10.1016/j.molp.2020.01.001 (Epub 2020 Jan 11 PMID: 31935463)

Sapra VT, Anaele AO (1991) Screening soybean genotypes for drought and heat tolerance. J Agron Crop Sci 167:96–102

Sattar A, Sher A, Ijaz M, Ul-Allah S, Rizwan MS, Hussain M, Cheema MA (2020) Terminal drought and heat stress alter physiological and biochemical attributes in flag leaf of bread wheat. PLoS ONE 15:1–14. https://doi.org/10.1371/journal.pone.0232974

Scandalios JG (1993) Oxygen stress and superoxide dismutases. Plant Physiol 101:7–12. https://doi.org/10.1104/pp.101.1.7

Schmidt J, Tricker PJ, Eckermann P, Kalambettu P, Garcia M, Fleury D (2020) Novel alleles for combined drought and heat stress tolerance in wheat. Front Plant Sci 10:1800. https://doi.org/10.3389/fpls.2019.01800

Sehgal A, Sita K, Kumar J, Kumar S, Singh S, Siddique KH, Nayyar H (2017) Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity. Front Plant Sci 8:1–19. https://doi.org/10.3389/fpls.2017.01776

Sehgal A, Sita K, Siddique KH, Kumar R, Bhogireddy S, Varshney RK, Nayyar H (2018) Drought or/and heat-stress effects on seed filling in food crops: impacts on functional biochemistry, seed yields, and nutritional quality. Front Plant Sci 9:1–19. https://doi.org/10.3389/fpls.2018.01705

Sehgal A, Sita K, Bhandari K, Kumar S, Kumar J, Vara Prasad PV, Siddique KHM, Nayyar H (2019) Influence of drought and heat stress, applied independently or in combination during seed development, on qualitative and quantitative aspects of seeds of lentil (Lens culinaris Medikus) genotypes, differing in drought sensitivity. Plant Cell Environ 42:198–211. https://doi.org/10.1111/pce.13328

Seidel SJ, Rachmilevitch S, Schütze N, Lazarovitch N (2016) Modelling the impact of drought and heat stress on common bean with two different photosynthesis model approaches. Environ Model Softw 81:111–121. https://doi.org/10.1016/j.envsoft.2016.04.001

Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Expt Bot 99:141–149. https://doi.org/10.1016/j.envexpbot.2013.11.010

Shaar-Moshe L, Blumwald E, Peleg Z (2017) Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat. Plant Physiol 174:421–434

Shah N, Paulsen GM (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil 257:219–226. https://doi.org/10.1023/A:1026237816578

Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS 8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216

Shim JS, Oh N, Chung PJ, Kim YS, Choi YD, Kim JK (2018) Overexpression of OsNAC14 improves drought tolerance in rice. Front Plant Sci 9:310. https://doi.org/10.3389/fpls.2018.00310

Siddiqui MH, Al-Khaishany MY, Al-Qutami MA, Al-Whaibi MH, Grover A, Ali HM (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.2015.06.00233

Singh TN, Aspinall D, Paleg LG (1972) Proline accumulation and varietal adaptability to drought in barley: a potential metabolic measure of drought resistance. Nat New Biol 236:188–190. https://doi.org/10.1038/newbio236188a0

Singh AK, Ganapathysubramanian B, Sarkar S, Singh A (2018) Deep learning for plant stress phenotyping: trends and future perspectives. Trends Plant Sci 23:883–898

Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109:435–442. https://doi.org/10.1034/j.1399-3054.2000.100410.x

Stevanović B, Šinzčar J, Glišić O (1997) Electrolyte leakage differences between poikilohydrous and homoiohydrous species of Gesneriaceae. Biol Plant 40:299–303. https://doi.org/10.1023/A:1001037124251

Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407. https://doi.org/10.1016/S1360-1385(99)01470-3

Sukumaran S, Reynolds MP, Sansaloni C (2018) Genome-wide association analyses identify QTL hotspots for yield and component traits in durum wheat grown under yield potential, drought, and heat stress environments. Front Plant Sci 9:81

Sun M, Huang D, Zhang A, Khan I, Yan H, Wang X, Zhang X, Zhang J, Huang L (2020) Transcriptome analysis of heat stress and drought stress in pearl millet based on Pacbio full-length transcriptome sequencing. BMC Plant Biol 20:1–5

Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139:1313–1322

Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699. https://doi.org/10.1016/j.pbi.2011.07.014

Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

Tahmasebi S, Heidari B, Pakniyat H, McIntyre CL (2016) Mapping QTLs associated with agronomic and physiological traits under terminal drought and heat stress conditions in wheat (Triticum aestivum L). Genome 60:26–45

Taiz L, Zeiger E (2010) Photosynthesis: carbon reactions. Plant physiology. Sunderland, England

Taiz L, Zeiger E (1991) Plant Physiology. Redwood City, United States.

Tani E, Chronopoulou EG, Labrou NE, Sarri E, Goufa Μ, Vaharidi X, Abraham ΕM (2019) Growth, physiological, biochemical, and transcriptional responses to drought stress in seedlings of Medicago sativa L, Medicago arborea L and their hybrid (Alborea). Agronomy 9:38. https://doi.org/10.3390/agronomy9010038

Templer SE, Ammon A, Pscheidt D et al (2017) Metabolite profiling of barley leaves under drought and combined heat and drought stress reveals metabolic QTLs for metabolites associated with antioxidant defense. J Exp Bot 68:1697–1713

Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environ Exp Bot 67:429–443. https://doi.org/10.1016/j.envexpbot.2009.09.004

Trachsel S, Stamp P, Hund A (2010) Effect of high temperatures, drought and aluminum toxicity on root growth of tropical maize (Zea mays L.) seedlings. Maydica 55:249–260

Trachsel S, Leyva M, Lopez M, Suarez EA, Mendoza A, Montiel NG, San Vicente F (2016) Identification of tropical maize germplasm with tolerance to drought, nitrogen deficiency, and combined heat and drought stresses. Crop Sci 56:3031–3045. https://doi.org/10.2135/cropsci2016.03.0182

Triboï E, Martre P, Triboï-Blondel A (2003) Environmentally-induced changes in protein composition in developing grains of wheat are related to changes in total protein content. J Exp Bot 54:1731–1742

Tricker PJ, Elhabti A, Schmidt J, Fleury D (2018) The physiological and genetic basis of combined drought and heat tolerance in wheat. J Exp Bot 69:3195–3210

Urban J, Ingwers MW, McGuire MA, Teskey RO (2017) Increase in leaf temperature opens stomata and decouples net photosynthesis from stomatal conductance in Pinus taeda and Populus deltoides x nigra. J Exp Bot 68:1757–1767. https://doi.org/10.1093/jxb/erx052

Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J (2014) Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21:1422–1441. https://doi.org/10.1089/ars.2013.5662

Varshney RK, Thudi M, Roorkiwal M, He W, Upadhyaya HD, Yang W, Bajaj P, Cubry P, Rathore A, Jian J, Doddamani D et al (2019) Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet 51:857–864

Vescio R, Abenavoli MR, Sorgona A (2021) Single and combined abiotic stress in maize root morphology. Plants 10:1–16. https://doi.org/10.3390/plants10010005

Wahid A (2007) Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 120:219–228. https://doi.org/10.1007/s10265-006-0040-5

Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

Wang GP, Zhang XY, Li F, Luo Y, Wang W (2010) Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica 48:117–126. https://doi.org/10.1007/s11099-010-0016-5

Wang Y, Xu H, Zhu H, Tao Y, Zhang G, Zhang L, Ma Z (2014) Classification and expression diversification of wheat dehydrin genes. Plant Sci 214:113–120. https://doi.org/10.1016/j.plantsci.2013.10.005

Wang B, Chen J, Chen L, Wang X, Wang R, Ma L, Chen Y (2015) Combined drought and heat stress in Camellia oleifera cultivars: leaf characteristics, soluble sugar and protein contents, and Rubisco gene expression. Trees 29:1483–1492. https://doi.org/10.1007/s00468-015-1229-9

Wardlaw IF (2002) Interaction between drought and chronic high temperature during kernel filling in wheat in a controlled environment. Ann Bot 90:469–476. https://doi.org/10.1093/aob/mcf219

Wen W, Li K, Alseekh S et al (2015) Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population. Plant Cell 27:1839–1856

Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21:455–467. https://doi.org/10.1046/j.1365-313x.2000.00695.x

Wijewardene I, Mishra N, Sun L, Smith J, Zhu X, Payton P, Shen G, Zhang H (2020) Improving drought-, salinity-, and heat-tolerance in transgenic plants by co-overexpressing Arabidopsis vacuolar pyrophosphatase gene AVP1 and Larrea Rubisco activase gene RCA. Plant Sci 15:110499

Wilhelm EP, Mullen RE, Keeling PL, Singletary GW (1999) Heat stress during grain filling in maize: effects on kernel growth and metabolism. Crop Sci 39:1733–1741. https://doi.org/10.2135/cropsci1999.3961733x

Wu W, Duncan RW, Ma BL (2017) Quantification of canola root morphological traits under heat and drought stresses with electrical measurements. Plant Soil 415:229–244. https://doi.org/10.1007/s11104-016-3155-z

Xiang J, Chen X, Hu W, Xiang Y, Yan M, Wang J (2018) Overexpressing heat-shock protein OsHSP50. 2 improves drought tolerance in rice. Plant Cell Rep 37:1585–1595. https://doi.org/10.1007/s00299-018-2331-4

Xu Y, Huang B (2018) Comparative transcriptomic analysis reveals common molecular factors responsive to heat and drought stress in Agrostis stolonifera. Sci Rep 8:1–2

Yang J, Zhang J (2006) Grain filling of cereal under soil drying. New Phytol 169:223–236. https://doi.org/10.1111/j.1469-8137.2005.01597.x

Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Lu C (2007) 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

Ye H, Roorkiwal M, Valliyodan B, Zhou L, Chen P, Varshney RK, Nguyen HT (2018) Genetic diversity of root system architecture in response to drought stress in grain legumes. J Exp Bot 69:3267–3277. https://doi.org/10.1093/jxb/ery082

Yin Y, Qin K, Song X et al (2018) BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase-mediated reactive oxygen species signaling in tomato. Plant Cell Physiol 59:2239–2254

Yu J, Chen L, Xu M, Huang B (2012) Effects of elevated CO2 on physiological responses of tall fescue to elevated temperature, drought stress, and the combined stresses. Crop Sci 52:1848–1858. https://doi.org/10.2135/cropsci2012.01.0030

Yuan Y, Cairns JE, Babu R, Gowda M, Makumbi D, Magorokosho C, Zhang A, Liu Y, Wang N, Hao Z, San Vicente F, Olsen MS, Prasanna BM, Lu Y, Zhang X (2019) Genome-Wide association mapping and genomic prediction analyses reveal the genetic architecture of grain yield and flowering time under drought and heat stress conditions in maize. Front Plant Sci 9:1919

Zafar SA, Hameed A, Khan AS, Ashraf M (2017) Heat shock induced morpho-physiological response in indica rice (Oryza sativa L.) at early seedling stage. Pak J Bot 49:453–463.

Zafar SA, Hameed A, Nawaz MA, Wei MA, Noor MA, Hussain M (2018) Mechanisms and molecular approaches for heat tolerance in rice (Oryza sativa L.) under climate change scenario. J Integr Agric 17:726–738. https://doi.org/10.1016/S2095-3119(17)61718-0

Zaharieva M, Gaulin E, Havaux M, Acevedo E, Monneveux P (2001) Drought and heat responses in the wild wheat relative Aegilops geniculata Roth: potential interest for wheat improvement. Crop Sci 41:1321–1329

Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A, Inupakutika MA, Mittler R (2016) ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J Exp Bot 67:5381–5390

Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12. https://doi.org/10.1111/ppl.12540

Zang X, Geng X, He K, Wang F, Tian X, Xin M, Yao Y, Hu Z, Ni Z, Sun Q, Peng H (2018) Overexpression of the wheat (Triticum aestivum L.) TaPEPKR2 gene enhances heat and dehydration tolerance in both wheat and Arabidopsis. Front Plant Sci 9:1710

Zhang B, Liu W, Chang SX, Anyia AO (2010) Water-deficit and high temperature affected water use efficiency and arabinoxylan concentration in spring wheat. J Cereal Sci 52:263–269. https://doi.org/10.1016/j.jcs.2010.05.014

Zhao F, Zhang D, Zhao Y et al (2016) The difference of physiological and proteomic changes in maize leaves adaptation to drought, heat, and combined both stresses. Front Plant Sci 7:1471

Zheng, Y, Xia Z, Ma H, Yu Z (2019) The combined effects of water deficit and heat stress on physiological characteristics of endangered Nouelia insignis. Acta Physiol Plant 41:1–14. https://doi.org/10.1007/s11738-019-2955-1

Zhou B, Zhang L, Ullah A, Jin X, Yang XY, Zhang XL (2016) Identification of multiple stress responsive genes by sequencing a normalized cDNA library from sea-land cotton (Gossypium barbadense L.). PLoS ONE 11:e0152927. https://doi.org/10.1371/journal.pone.0152927

Zhou R, Yu X, Ottosen CO, Rosenqvist E, Zhao L, Wang Y, Wu Z (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol 17:1–13. https://doi.org/10.1186/s12870-017-0974-x

Zhou R, Kong L, Wu Z, Rosenqvist E, Wang Y, Zhao L, Ottosen CO (2019) Physiological response of tomatoes at drought, heat and their combination followed by recovery. Physiol Plant 165(2):144–154. https://doi.org/10.1111/ppl.12764

Zhou R, Yu X, Ottosen CO, Zhang T, Wu Z, Zhao T (2020) Unique miRNAs and their targets in tomato leaf responding to combined drought and heat stress. BMC Plant Biol 20:1

Zhu JK (2001) Cell signaling under salt, water and cold stresses Curr Opin Plant Biol 4:401–406. https://doi.org/10.1016/S1369-5266(00)00192-8

Zinselmeier C, Jeong BR, Boyer JS (1999) Starch and the control of kernel number in maize at low water potentials. Plant Physiol 121:25–36. https://doi.org/10.1104/pp.121.1.25

Zinta G, AbdElgawad H, Domagalska MA, Vergauwen L, Knapen D, Nijs I, Asard H (2014) Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Global Change Biol 20:3670–3685. https://doi.org/10.1111/gcb.12626

Zinta G, AbdElgawad H, Peshev D, Weedon JT, Van den Ende W, Nijs I, Janssens IA, Beemster GT, Asard H (2018) Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2. J Exp Bot 69:2159–2170