The effects of spring versus summer heat events on two arid zone plant species under field conditions
K. V. Milner
A * , K. French B , D. W. Krix A , S. M. Valenzuela A and A. Leigh A
+ Author Affiliations
- Author Affiliations
A School of Life Sciences, University of Technology Sydney, Ultimo, NSW 2007, Australia.
B Centre for Sustainable Ecosystem Solutions, School of Earth, Atmospherics and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.
Functional Plant Biology 50(6) 455-469 https://doi.org/10.1071/FP22135
Submitted: 21 September 2021 Accepted: 15 March 2023 Published: 21 April 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Heatwaves are increasingly occurring out-of-season, which may affect plants not primed for the event. Further, heat stress often coincides with water and/or nutrient stress, impairing short-term physiological function and potentially causing downstream effects on reproductive fitness. We investigated the response of water-stressed arid-zone Solanum oligacanthum and Solanum orbiculatum to spring vs summer heat stress under differing nutrient conditions. Heat stress events were imposed in open-topped chambers under in situ desert conditions. To assess short-term impacts, we measured leaf photosystem responses (Fv/Fm) and membrane stability; long-term effects were compared via biomass allocation, visible damage, flowering and fruiting. Plants generally fared more poorly following summer than spring heat stress, with the exception of Fv/Fm. Summer heat stress caused greater membrane damage, reduced growth and survival compared with spring. Nutrient availability had a strong influence on downstream effects of heat stress, including species-specific outcomes for reproductive fitness. Overall, high temperatures during spring posed a lower threat to fitness than in severe arid summer conditions of high temperature and low water availability, which were more detrimental to plants in both the short and longer term. Our study highlights the importance of considering ecologically relevant, multiple-stressor events to understand different species responses to extreme heat.
Keywords: chlorophyll fluorescence (Fv/Fm), desert species, fitness, heat stress, heatwaves, membrane stability, Solanum species, thermal tolerance.
References
Abeli T, Rossi G, Gentili R, Gandini M, Mondoni A, Cristofanelli P (2012) Effect of the extreme summer heat waves on isolated populations of two orophitic plants in the north Apennines (Italy). Nordic Journal of Botany 30, 109–115.| Effect of the extreme summer heat waves on isolated populations of two orophitic plants in the north Apennines (Italy).Crossref | GoogleScholarGoogle Scholar |
Ahrens CW, Challis A, Byrne M, Leigh A, Nicotra AB, Tissue D, Rymer P (2021) Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins. New Phytologist 232, 1212––1225.
| Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins.Crossref | GoogleScholarGoogle Scholar |
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH(Ted), Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660–684.
| A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests.Crossref | GoogleScholarGoogle Scholar |
Aspinwall MJ, Vårhammar A, Blackman CJ, Tjoelker MG, Ahrens C, Byrne M, Tissue DT, Rymer PD (2017) Adaptation and acclimation both influence photosynthetic and respiratory temperature responses in Corymbia calophylla. Tree Physiology 37, 1095–1112.
| Adaptation and acclimation both influence photosynthetic and respiratory temperature responses in Corymbia calophylla.Crossref | GoogleScholarGoogle Scholar |
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
| Thermal acclimation and the dynamic response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar |
Atkin OK, Holly C, Ball MC (2000) Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant, Cell & Environment 23, 15–26.
| Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration.Crossref | GoogleScholarGoogle Scholar |
Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology 32, 87–105.
| The hot and the cold: unravelling the variable response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar |
Bauweraerts I, Ameye M, Wertin TM, McGuire MA, Teskey RO, Steppe K (2014) Water availability is the decisive factor for the growth of two tree species in the occurrence of consecutive heat waves. Agricultural and Forest Meteorology 189–190, 19–29.
| Water availability is the decisive factor for the growth of two tree species in the occurrence of consecutive heat waves.Crossref | GoogleScholarGoogle Scholar |
Bean AR (2004) The taxonomy and ecology of Solanum subg. Leptostemonum (Dunal) Bitter (Solanaceae) in Queensland and far north-eastern New South Wales, Australia. Austrobaileya 6, 639–816.
Begcy K, Weigert A, Egesa AO, Dresselhaus T (2018) Compared to Australian cultivars, European summer wheat (Triticum aestivum) overreacts when moderate heat stress is applied at the pollen development stage. Agronomy-Basel 8, 99
| Compared to Australian cultivars, European summer wheat (Triticum aestivum) overreacts when moderate heat stress is applied at the pollen development stage.Crossref | GoogleScholarGoogle Scholar |
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher-plants. Annual Review of Plant Physiology and Plant Molecular Biology 31, 491–543.
| Photosynthetic response and adaptation to temperature in higher-plants.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2018) Climate data online: Port Augusta Aero 2001–2018. Commonwealth of Australia.
Bureau of Meteorology (2019) Australian climate and weather extremes monitoring system. Commonwealth of Australia.
Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533.
| Europe-wide reduction in primary productivity caused by the heat and drought in 2003.Crossref | GoogleScholarGoogle Scholar |
Cook AM, Berry N, Milner KV, Leigh A (2021) Water availability influences thermal safety margins for leaves. Functional Ecology 35, 2179–2189.
| Water availability influences thermal safety margins for leaves.Crossref | GoogleScholarGoogle Scholar |
Cowan T, Purich A, Perkins S, Pezza A, Boschat G, Sadler K (2014) More frequent, longer, and hotter heat waves for Australia in the twenty-first century. Journal of Climate 27, 5851–5871.
| More frequent, longer, and hotter heat waves for Australia in the twenty-first century.Crossref | GoogleScholarGoogle Scholar |
Crawley MJ (2013) ‘The R book.’ 2nd edn. (John Wiley & Sons, Ltd: Chichester, West Sussex, UK)
Crous KY, Drake JE, Aspinwall MJ, Sharwood RE, Tjoelker MG, Ghannoum O (2018) Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species. Global Change Biology 24, 4626–4644.
| Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species.Crossref | GoogleScholarGoogle Scholar |
Curtis EM, Knight CA, Petrou K, Leigh A (2014) A comparative analysis of photosynthetic recovery from thermal stress: a desert plant case study. Oecologia 175, 1051––1061.
| A comparative analysis of photosynthetic recovery from thermal stress: a desert plant case study.Crossref | GoogleScholarGoogle Scholar |
Daniell JW, Chappell WE, Couch HB (1969) Effect of sublethal and lethal temperature on plant cells. Plant Physiology 44, 1684–1689.
| Effect of sublethal and lethal temperature on plant cells.Crossref | GoogleScholarGoogle Scholar |
Davies M, Ecroyd H, Robinson SA, French K (2018) Stress in native grasses under ecologically relevant heat waves. PLoS ONE 13, e0204906
| Stress in native grasses under ecologically relevant heat waves.Crossref | GoogleScholarGoogle Scholar |
De Boeck HJ, Dreesen FE, Janssens IA, Nijs I (2011) Whole-system responses of experimental plant communities to climate extremes imposed in different seasons. New Phytologist 189, 806–817.
| Whole-system responses of experimental plant communities to climate extremes imposed in different seasons.Crossref | GoogleScholarGoogle Scholar |
De Boeck HJ, De Groote T, Nijs I (2012) Leaf temperatures in glasshouses and open-top chambers. New Phytologist 194, 1155–1164.
| Leaf temperatures in glasshouses and open-top chambers.Crossref | GoogleScholarGoogle Scholar |
Djanaguiraman M, Boyle DL, Welti R, Jagadish SVK, Prasad PVV (2018) Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles. BMC Plant Biology 18, 55
| Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles.Crossref | GoogleScholarGoogle Scholar |
Drake JE, Tjoelker MG, Vårhammar A, Medlyn BE, Reich PB, Leigh A, Pfautsch S, Blackman CJ, López R, Aspinwall MJ, Crous KY, Duursma RA, Kumarathunge D, De Kauwe MG, Jiang M, Nicotra AB, Tissue DT, Choat B, Atkin OK, Barton CVM (2018) Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance. Global Change Biology 24, 2390–2402.
| Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance.Crossref | GoogleScholarGoogle Scholar |
Erskine PD, Stewart GR, Schmidt S, Turnbull MH, Unkovich M, Pate JS (1996) Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid muiga woodlands. Plant, Cell & Environment 19, 1149–1159.
| Water availability – a physiological constraint on nitrate utilization in plants of Australian semi-arid muiga woodlands.Crossref | GoogleScholarGoogle Scholar |
FloraNT (2013) FloraNT – Northern Territory flora online. (Ed. NT Herbarium). Department of Land Resource Management.
Fox J, Weisber S (2011) ‘An R companion to applied regression.’ 2nd edn. (Sage: Thousand Oaks, CA, USA)
French K, Jansens IB, Ashcroft MB, Ecroyd H, Robinson SA (2019) High tolerance of repeated heatwaves in Australian native plants. Austral Ecology 44, 597–608.
| High tolerance of repeated heatwaves in Australian native plants.Crossref | GoogleScholarGoogle Scholar |
Friedman J, Rubin MJ (2015) All in good time: understanding annual and perennial strategies in plants. American Journal of Botany 102, 497–499.
| All in good time: understanding annual and perennial strategies in plants.Crossref | GoogleScholarGoogle Scholar |
Guha A, Han J, Cummings C, McLennan DA, Warren JM (2018) Differential ecophysiological responses and resilience to heat wave events in four co-occurring temperate tree species. Environmental Research Letters 13, 065008
| Differential ecophysiological responses and resilience to heat wave events in four co-occurring temperate tree species.Crossref | GoogleScholarGoogle Scholar |
Handley LL, Austin AT, Stewart GR, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Functional Plant Biology 26, 185–199.
| The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability.Crossref | GoogleScholarGoogle Scholar |
Harris RMB, Beaumont LJ, Vance TR, Tozer CR, Remenyi TA, Perkins-Kirkpatrick SE, Mitchell PJ, Nicotra AB, McGregor S, Andrew NR, Letnic M, Kearney MR, Wernberg T, Hutley LB, Chambers LE, Fletcher M-S, Keatley MR, Woodward CA, Williamson G, Duke NC, Bowman DMJS (2018) Biological responses to the press and pulse of climate trends and extreme events. Nature Climate Change 8, 579–587.
| Biological responses to the press and pulse of climate trends and extreme events.Crossref | GoogleScholarGoogle Scholar |
Havaux M (1993a) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Science 94, 19–33.
| Characterization of thermal damage to the photosynthetic electron transport system in potato leaves.Crossref | GoogleScholarGoogle Scholar |
Havaux M (1993b) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant, Cell & Environment 16, 461–467.
| Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures.Crossref | GoogleScholarGoogle Scholar |
Heckathorn SA, Poeller GJ, Coleman JS, Hallberg RL (1996a) Nitrogen availability alters patterns of accumulation of heat stress-induced proteins in plants. Oecologia 105, 413–418.
| Nitrogen availability alters patterns of accumulation of heat stress-induced proteins in plants.Crossref | GoogleScholarGoogle Scholar |
Heckathorn SA, Poeller GJ, Coleman JS, Hallberg RL (1996b) Nitrogen availability and vegetative development influence the response of ribulose 1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and heat-shock protein content to heat stress in Zea mays L. International Journal of Plant Sciences 157, 546–553.
| Nitrogen availability and vegetative development influence the response of ribulose 1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and heat-shock protein content to heat stress in Zea mays L.Crossref | GoogleScholarGoogle Scholar |
Hoffmann AA, Rymer PD, Byrne M, Ruthrof KX, Whinam J, McGeoch M, Bergstrom DM, Guerin GR, Sparrow B, Joseph L, Hill SJ, Andrew NR, Camac J, Bell N, Riegler M, Gardner JL, Williams SE (2019) Impacts of recent climate change on terrestrial flora and fauna: some emerging Australian examples. Austral Ecology 44, 3–27.
| Impacts of recent climate change on terrestrial flora and fauna: some emerging Australian examples.Crossref | GoogleScholarGoogle Scholar |
Holmgren M, Stapp P, Dickman CR, Gracia C, Graham S, Gutiérrez JR, Hice C, Jaksic F, Kelt DA, Letnic M, Lima M, López BC, Meserve PL, Milstead WB, Polis GA, Previtali MA, Richter M, Sabaté S, Squeo FA (2006) Extreme climatic events shape arid and semiarid ecosystems. Frontiers in Ecology and the Environment 4, 87–95.
| Extreme climatic events shape arid and semiarid ecosystems.Crossref | GoogleScholarGoogle Scholar |
Hovenden MJ, Miglietta F, Zaldei A, Vander Schoor JK, Wills KE, Newton PCD (2006) The TasFACE climate-change impacts experiment: design and performance of combined elevated CO2 and temperature enhancement in a native Tasmanian grassland. Australian Journal of Botany 54, 1–10.
| The TasFACE climate-change impacts experiment: design and performance of combined elevated CO2 and temperature enhancement in a native Tasmanian grassland.Crossref | GoogleScholarGoogle Scholar |
Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Frontiers in Ecology and the Environment 5, 365–374.
| A new generation of climate-change experiments: events, not trends.Crossref | GoogleScholarGoogle Scholar |
Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020.
| Running to stand still: adaptation and the response of plants to rapid climate change.Crossref | GoogleScholarGoogle Scholar |
Jyoteeshkumar Reddy P, Perkins-Kirkpatrick SE, Sharples JJ (2021) Intensifying Australian heatwave trends and their sensitivity to observational data. Earth’s Future 9, e2020EF001924
| Intensifying Australian heatwave trends and their sensitivity to observational data.Crossref | GoogleScholarGoogle Scholar |
Kassas M, Girgis WA (1970) Habitat and plant communities in the Egyptian desert: VII. geographical facies of plant communities. Journal of Ecology 58, 335–350.
| Habitat and plant communities in the Egyptian desert: VII. geographical facies of plant communities.Crossref | GoogleScholarGoogle Scholar |
Kimball BA, Conley MM, Wang S, Lin X, Luo C, Morgan J, Smith D (2008) Infrared heater arrays for warming ecosystem field plots. Global Change Biology 14, 309–320.
| Infrared heater arrays for warming ecosystem field plots.Crossref | GoogleScholarGoogle Scholar |
Langsrud Ø (2003) ANOVA for unbalanced data: use Type II instead of Type III sums of squares. Statistics and Computing 13, 163–167.
| ANOVA for unbalanced data: use Type II instead of Type III sums of squares.Crossref | GoogleScholarGoogle Scholar |
Leigh A, Sevanto S, Ball MC, Close JD, Ellsworth DS, Knight CA, Nicotra AB, Vogel S (2012) Do thick leaves avoid thermal damage in critically low wind speeds? New Phytologist 194, 477–487.
| Do thick leaves avoid thermal damage in critically low wind speeds?Crossref | GoogleScholarGoogle Scholar |
Lenth R (2018) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.1. Available at https://cran.r-project.org/web/packages/emmeans/index.html
Marchand FL, Mertens S, Kockelbergh F, Beyens L, Nijs I (2005) Performance of high Arctic tundra plants improved during but deteriorated after exposure to a simulated extreme temperature event. Global Change Biology 11, 2078–2089.
| Performance of high Arctic tundra plants improved during but deteriorated after exposure to a simulated extreme temperature event.Crossref | GoogleScholarGoogle Scholar |
Marchin RM, Backes D, Ossola A, Leishman MR, Tjoelker MG, Ellsworth DS (2022) Extreme heat increases stomatal conductance and drought-induced mortality risk in vulnerable plant species. Global Change Biology 28, 1133–1146.
| Extreme heat increases stomatal conductance and drought-induced mortality risk in vulnerable plant species.Crossref | GoogleScholarGoogle Scholar |
Milner K (2020) The price of heat stress: functional and resource constraints to thermal tolerance in arid zone plants. PhD Thesis, University of Technology Sydney. Available at https://opus.lib.uts.edu.au/bitstream/10453/142273/2/02whole.pdf
Milner K (2023) The effects of spring versus summer heat events on two arid zone plant species under field conditions. Mendeley Data, V1. Available at https://doi.org/10.17632/54yd5m85fn.1
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends in Biochemical Sciences 37, 118–125.
| How do plants feel the heat?Crossref | GoogleScholarGoogle Scholar |
Nano CEM, Clarke PJ (2011) How do drought and fire influence the patterns of resprouting in Australian deserts? Plant Ecology 212, 2095–2110.
| How do drought and fire influence the patterns of resprouting in Australian deserts?Crossref | GoogleScholarGoogle Scholar |
Nijs I, Kockelbergh F, Teughels H, Blum H, Hendrey G, Impens I (1996) Free Air Temperature Increase (FATI): a new tool to study global warming effects on plants in the field. Plant, Cell & Environment 19, 495–502.
| Free Air Temperature Increase (FATI): a new tool to study global warming effects on plants in the field.Crossref | GoogleScholarGoogle Scholar |
O’Sullivan OS, Weerasinghe KWLK, Evans JR, Egerton JJG, Tjoelker MG, Atkin OK (2013) High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant, Cell & Environment 36, 1268–1284.
Parsons PA (1990) The metabolic cost of multiple environmental stresses: implications for climatic change and conservation. Trends in Ecology & Evolution 5, 315–317.
| The metabolic cost of multiple environmental stresses: implications for climatic change and conservation.Crossref | GoogleScholarGoogle Scholar |
Pate JS, Bell TL (1999) Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agroforestry Systems 45, 303–341.
| Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Rajametov SN, Yang EY, Jeong HB, Cho MC, Chae SY, Paudel N (2021) Heat treatment in two tomato cultivars: a study of the effect on physiological and growth recovery. Horticulturae 7, 119
| Heat treatment in two tomato cultivars: a study of the effect on physiological and growth recovery.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2018) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Reyer CPO, Leuzinger S, Rammig A, Wolf A, Bartholomeus RP, Bonfante A, de Lorenzi F, Dury M, Gloning P, Abou Jaoudé R, Klein T, Kuster TM, Martins M, Niedrist G, Riccardi M, Wohlfahrt G, de Angelis P, de Dato G, François L, Menzel A, Pereira M (2013) A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability. Global Change Biology 19, 75–89.
| A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability.Crossref | GoogleScholarGoogle Scholar |
Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant, Cell & Environment 28, 269–277.
| Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene.Crossref | GoogleScholarGoogle Scholar |
Smith DMS, Morton SR (1990) A framework for the ecology of arid Australia. Journal of Arid Environments 18, 255–278.
| A framework for the ecology of arid Australia.Crossref | GoogleScholarGoogle Scholar |
Steffen W, Hughes L, Perkins S (2014) Heatwaves: hotter, longer, more often. Climate Council of Australia Ltd.
Tang Y, Wen X, Lu Q, Yang Z, Cheng Z, Lu C (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant Physiology 143, 629–638.
| Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants.Crossref | GoogleScholarGoogle Scholar |
Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment 38, 1699–1712.
| Responses of tree species to heat waves and extreme heat events.Crossref | GoogleScholarGoogle Scholar |
Valladares F, Pearcy RW (1997) Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia. Plant, Cell & Environment 20, 25–36.
| Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia.Crossref | GoogleScholarGoogle Scholar |
Vicente-Serrano SM, Lopez-Moreno J-I, Beguería S, Lorenzo-Lacruz J, Sanchez-Lorenzo A, García-Ruiz JM, Azorin-Molina C, Morán-Tejeda E, Revuelto J, Trigo R, Coelho F, Espejo F (2014) Evidence of increasing drought severity caused by temperature rise in southern Europe. Environmental Research Letters 9, 044001
| Evidence of increasing drought severity caused by temperature rise in southern Europe.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Huang B (2004) Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress. Crop Science 44, 1729–1736.
| Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress.Crossref | GoogleScholarGoogle Scholar |
Wang D, Heckathorn SA, Mainali K, Tripathee R (2016) Timing effects of heat-stress on plant ecophysiological characteristics and growth. Frontiers in Plant Science 7, 1629
| Timing effects of heat-stress on plant ecophysiological characteristics and growth.Crossref | GoogleScholarGoogle Scholar |
Ward EJ, Domec J-C, Laviner MA, Fox TR, Sun G, McNulty S, King J, Noormets A (2015) Fertilization intensifies drought stress: water use and stomatal conductance of Pinus taeda in a midrotation fertilization and throughfall reduction experiment. Forest Ecology and Management 355, 72–82.
| Fertilization intensifies drought stress: water use and stomatal conductance of Pinus taeda in a midrotation fertilization and throughfall reduction experiment.Crossref | GoogleScholarGoogle Scholar |
Zhao WY, Xu S, Li JL, Cui LJ, Chen YN, Wang JZ (2008) Effects of foliar application of nitrogen on the photosynthetic performance and growth of two fescue cultivars under heat stress. Biologia Plantarum 52, 113–116.
| Effects of foliar application of nitrogen on the photosynthetic performance and growth of two fescue cultivars under heat stress.Crossref | GoogleScholarGoogle Scholar |
Zscheischler J, Seneviratne SI (2017) Dependence of drivers affects risks associated with compound events. Science Advances 3, e1700263
| Dependence of drivers affects risks associated with compound events.Crossref | GoogleScholarGoogle Scholar |
