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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

Consistently high heat tolerance acclimation in response to a simulated heatwave across species from the broadly distributed Acacia genus

Samuel C. Andrew https://orcid.org/0000-0003-4589-2746 A § * , Pieter A. Arnold https://orcid.org/0000-0002-6158-7752 B § * , Anna K. Simonsen C D and Verónica F. Briceño B
+ Author Affiliations
- Author Affiliations

A CSIRO Land and Water, Canberra, ACT 2600, Australia.

B Division of Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2600, Australia.

C Department of Biological Sciences, Florida International University, Miami, FL 33199, USA.

D Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 2600, Australia.


Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 50(1) 71-83 https://doi.org/10.1071/FP22173
Submitted: 11 May 2022  Accepted: 18 September 2022   Published: 10 October 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

When leaves exceed their thermal threshold during heatwaves, irreversible damage to the leaf can accumulate. However, few studies have explored short-term acclimation of leaves to heatwaves that could help plants to prevent heat damage with increasing heatwave intensity. Here, we studied the heat tolerance of PSII (PHT) in response to a heatwave in Acacia species from across a strong environmental gradient in Australia. We compared PHT metrics derived from temperature-dependent chlorophyll fluorescence response curves (T–F0) before and during a 4-day 38°C heatwave in a controlled glasshouse experiment. We found that the 15 Acacia species displayed surprisingly large and consistent PHT acclimation responses with a mean tolerance increase of 12°C (range, 7.7–19.1°C). Despite species originating from diverse climatic regions, neither maximum temperature of the warmest month nor mean annual precipitation at origin were clear predictors of PHT. To our knowledge, these are some of the largest measured acclimation responses of PHT from a controlled heatwave experiment. This remarkable capacity could partially explain why this genus has become more diverse and common as the Australian continent became more arid and suggests that the presence of Acacia in Australian ecosystems will remain ubiquitous with climate change.

Keywords: Acacia, Australian plants, climate change, heat tolerance, leaf physiology, photosystem II, plasticity, Tcrit, thermal safety margin.


References

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 114, 1212–1225.
Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins.Crossref | GoogleScholarGoogle Scholar |

Arnold PA, Briceño VF, Gowland KM, Catling AA, Bravo LA, Nicotra AB (2021) A high-throughput method for measuring critical thermal limits of leaves by chlorophyll imaging fluorescence. Functional Plant Biology 48, 634–646.
A high-throughput method for measuring critical thermal limits of leaves by chlorophyll imaging fluorescence.Crossref | GoogleScholarGoogle Scholar |

Arnold PA, Wang S, Catling AA, Kruuk LEB, Nicotra AB (2022) Patterns of phenotypic plasticity along a thermal gradient differ by trait type in an alpine plant. Functional Ecology 36, 2412–2428.
Patterns of phenotypic plasticity along a thermal gradient differ by trait type in an alpine plant.Crossref | GoogleScholarGoogle Scholar |

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Bilger H-W, Schreiber U, Lange OL (1984) Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods. Oecologia 63, 256–262.
Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods.Crossref | GoogleScholarGoogle Scholar |

Breshears DD, Fontaine JB, Ruthrof KX, Field JP, Feng X, Burger JR, Law DJ, Kala J, Hardy GESJ (2021) Underappreciated plant vulnerabilities to heat waves. New Phytologist 231, 32–39.
Underappreciated plant vulnerabilities to heat waves.Crossref | GoogleScholarGoogle Scholar |

Brestic M, Zivcak M, Hauptvogel P, Misheva S, Kocheva K, Yang X, Li X, Allakhverdiev SI (2018) Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynthesis Research 136, 245–255.
Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions.Crossref | GoogleScholarGoogle Scholar |

Buchner O, Stoll M, Karadar M, Kranner I, Neuner G (2015) Application of heat stress in situ demonstrates a protective role of irradiation on photosynthetic performance in alpine plants. Plant, Cell & Environment 38, 812–826.
Application of heat stress in situ demonstrates a protective role of irradiation on photosynthetic performance in alpine plants.Crossref | GoogleScholarGoogle Scholar |

Buchner O, Roach T, Gertzen J, Schenk S, Karadar M, Stöggl W, Miller R, Bertel C, Neuner G, Kranner I (2017) Drought affects the heat-hardening capacity of alpine plants as indicated by changes in xanthophyll cycle pigments, singlet oxygen scavenging, α-tocopherol and plant hormones. Environmental and Experimental Botany 133, 159–175.
Drought affects the heat-hardening capacity of alpine plants as indicated by changes in xanthophyll cycle pigments, singlet oxygen scavenging, α-tocopherol and plant hormones.Crossref | GoogleScholarGoogle Scholar |

Coast O, Posch BC, Rognoni BG, Bramley H, Gaju O, Mackenzie J, Pickles C, Kelly AM, Lu M, Ruan Y-L, Trethowan R, Atkin OK (2022) Wheat photosystem II heat tolerance: evidence for genotype-by-environment interactions. The Plant Journal 111, 1368–1382.
Wheat photosystem II heat tolerance: evidence for genotype-by-environment interactions.Crossref | GoogleScholarGoogle Scholar |

Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences of the United States of America 97, 13430–13435.
| Crossref |

Curtis EM, Gollan J, Murray BR, Leigh A (2016) Native microhabitats better predict tolerance to warming than latitudinal macro-climatic variables in arid-zone plants. Journal of Biogeography 43, 1156–1165.
Native microhabitats better predict tolerance to warming than latitudinal macro-climatic variables in arid-zone plants.Crossref | GoogleScholarGoogle Scholar |

Dale EE, Larcombe MJ, Lee WG, Higgins SI (2020) Diversification is decoupled from biome fidelity: Acacia – a case study. Journal of Biogeography 47, 538–552.
Diversification is decoupled from biome fidelity: Acacia – a case study.Crossref | GoogleScholarGoogle Scholar |

Downton WJS, Berry JA, Seemann JR (1984) Tolerance of photosynthesis to high temperature in desert plants. Plant Physiology 74, 786–790.
Tolerance of photosynthesis to high temperature in desert plants.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 |

Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37, 4302–4315.
WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |

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 |

Frolec J, Ilík P, Krchňák P, Sušila P, Nauš J (2008) Irreversible changes in barley leaf chlorophyll fluorescence detected by the fluorescence temperature curve in a linear heating/cooling regime. Photosynthetica 46, 537–546.
Irreversible changes in barley leaf chlorophyll fluorescence detected by the fluorescence temperature curve in a linear heating/cooling regime.Crossref | GoogleScholarGoogle Scholar |

Gallagher RV, Leishman MR, Miller JT, Hui C, Richardson DM, Suda J, Trávníček P (2011) Invasiveness in introduced Australian acacias: the role of species traits and genome size. Diversity and Distributions 17, 884–897.
Invasiveness in introduced Australian acacias: the role of species traits and genome size.Crossref | GoogleScholarGoogle Scholar |

Gallien L, Thornhill AH, Zurell D, Miller JT, Richardson DM (2019) Global predictors of alien plant establishment success: combining niche and trait proxies. Proceedings of the Royal Society B: Biological Sciences 286, 20182477
Global predictors of alien plant establishment success: combining niche and trait proxies.Crossref | GoogleScholarGoogle Scholar |

Geange SR, Arnold PA, Catling AA, Coast O, Cook AM, Gowland KM, Leigh A, Notarnicola RF, Posch BC, Venn SE, Zhu L, Nicotra AB (2021) The thermal tolerance of photosynthetic tissues: a global systematic review and agenda for future research. New Phytologist 229, 2497–2513.
The thermal tolerance of photosynthetic tissues: a global systematic review and agenda for future research.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, Greppin H, Strasser RJ (1991) Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186, 88–98.
Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light.Crossref | GoogleScholarGoogle Scholar |

Hüve K, Bichele I, Tobias M, Niinemets Ü (2006) Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential. Plant, Cell & Environment 29, 212–228.
Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential.Crossref | GoogleScholarGoogle Scholar |

Hüve K, Bichele I, Rasulov B, Niinemets Ü (2011) When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant, Cell & Environment 34, 113–126.
When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation.Crossref | GoogleScholarGoogle Scholar |

Ilík P, Kouřil R, Kruk J, Myśliwa-Kurdziel B, Popelková H, Strzałka K, Nauš J (2003) Origin of chlorophyll fluorescence in plants at 55–75°C. Photochemistry and Photobiology 77, 68–76.
Origin of chlorophyll fluorescence in plants at 55–75°C.Crossref | GoogleScholarGoogle Scholar |

Jajoo A, Allakhverdiev SI (2017) High-temperature stress in plants: consequences and strategies for protecting photosynthetic machinery. In ‘Plant stress physiology’. (Ed. S. Shabala) pp. 138–154. (CABI Books, CABI International)

Johnson PCD (2014) Extension of Nakagawa & Schielzeth’s R2GLMM to random slopes models. Methods in Ecology and Evolution 5, 944–946.
Extension of Nakagawa & Schielzeth’s R2GLMM to random slopes models.Crossref | GoogleScholarGoogle Scholar |

Karadar M, Neuner G, Kranner I, Holzinger A, Buchner O (2018) Solar irradiation levels during simulated long- and short-term heat waves significantly influence heat survival, pigment and ascorbate composition, and free radical scavenging activity in alpine Vaccinium gaultherioides. Physiologia Plantarum 163, 211–230.
Solar irradiation levels during simulated long- and short-term heat waves significantly influence heat survival, pigment and ascorbate composition, and free radical scavenging activity in alpine Vaccinium gaultherioides.Crossref | GoogleScholarGoogle Scholar |

Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, Zimmermann NE, Linder HP, Kessler M (2017) Climatologies at high resolution for the earth’s land surface areas. Scientific Data 4, 170122
Climatologies at high resolution for the earth’s land surface areas.Crossref | GoogleScholarGoogle Scholar |

Knight CA, Ackerly DD (2002) An ecological and evolutionary analysis of photosynthetic thermotolerance using the temperature-dependent increase in fluorescence. Oecologia 130, 505–514.
An ecological and evolutionary analysis of photosynthetic thermotolerance using the temperature-dependent increase in fluorescence.Crossref | GoogleScholarGoogle Scholar |

Knight CA, Ackerly DD (2003) Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments. New Phytologist 160, 337–347.
Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments.Crossref | GoogleScholarGoogle Scholar |

Krause GH, Winter K, Krause B, Virgo A (2015) Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium. Functional Plant Biology 42, 42–51.
Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium.Crossref | GoogleScholarGoogle Scholar |

Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest Package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.
lmerTest Package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |

Lancaster LT, Humphreys AM (2020) Global variation in the thermal tolerances of plants. Proceedings of the National Academy of Sciences of the United States of America 117, 13580–13587.
Global variation in the thermal tolerances of plants.Crossref | GoogleScholarGoogle Scholar |

Leon-Garcia IV, Lasso E (2019) High heat tolerance in plants from the Andean highlands: implications for Paramos in a warmer world. PLoS ONE 14, e0224218
High heat tolerance in plants from the Andean highlands: implications for Paramos in a warmer world.Crossref | GoogleScholarGoogle Scholar |

Li X, Kristiansen K, Rosenqvist E, Liu F (2019) Elevated CO2 modulates the effects of drought and heat stress on plant water relations and grain yield in wheat. Journal of Agronomy and Crop Science 205, 362–371.
Elevated CO2 modulates the effects of drought and heat stress on plant water relations and grain yield in wheat.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 |

Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. Journal of Photochemistry and Photobiology B: Biology 137, 116–126.
Photosynthesis: response to high temperature stress.Crossref | GoogleScholarGoogle Scholar |

McKnight T (1949) Efficiency of isolates of Rhizobium in the cowpea group, with proposed additions to this group. Queensland Journal of Agricultural Science 6, 61–76.

Muggeo VMR (2017) Interval estimation for the breakpoint in segmented regression: a smoothed score-based approach. Australian & New Zealand Journal of Statistics 59, 311–322.
Interval estimation for the breakpoint in segmented regression: a smoothed score-based approach.Crossref | GoogleScholarGoogle Scholar |

Neuner G, Pramsohler M (2006) Freezing and high temperature thresholds of photosystem 2 compared to ice nucleation, frost and heat damage in evergreen subalpine plants. Physiologia Plantarum 126, 196–204.
Freezing and high temperature thresholds of photosystem 2 compared to ice nucleation, frost and heat damage in evergreen subalpine plants.Crossref | GoogleScholarGoogle Scholar |

Nievola CC, Carvalho CP, Carvalho V, Rodrigues E (2017) Rapid responses of plants to temperature changes. Temperature 4, 371–405.
Rapid responses of plants to temperature changes.Crossref | GoogleScholarGoogle Scholar |

Notarnicola RF, Nicotra AB, Kruuk LEB, Arnold PA (2021) Tolerance of warmer temperatures does not confer resilience to heatwaves in an alpine herb. Frontiers in Ecology and Evolution 9, 615119
Tolerance of warmer temperatures does not confer resilience to heatwaves in an alpine herb.Crossref | GoogleScholarGoogle Scholar |

O’Sullivan OS, Heskel MA, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A, Zhu L, Egerton JJG, Bloomfield KJ, Creek D, Bahar NHA, Griffin KL, Hurry V, Meir P, Turnbull MH, Atkin OK (2017) Thermal limits of leaf metabolism across biomes. Global Change Biology 23, 209–223.
Thermal limits of leaf metabolism across biomes.Crossref | GoogleScholarGoogle Scholar |

Perez TM, Feeley KJ (2020) Photosynthetic heat tolerances and extreme leaf temperatures. Functional Ecology 34, 2236–2245.
Photosynthetic heat tolerances and extreme leaf temperatures.Crossref | GoogleScholarGoogle Scholar |

Perez TM, Feeley KJ (2021) Weak phylogenetic and climatic signals in plant heat tolerance. Journal of Biogeography 48, 91–100.
Weak phylogenetic and climatic signals in plant heat tolerance.Crossref | GoogleScholarGoogle Scholar |

Perez TM, Feeley KJ, Michaletz ST, Slot M (2021a) Methods matter for assessing global variation in plant thermal tolerance. Proceedings of the National Academy of Sciences of the United States of America 118, e2024636118
Methods matter for assessing global variation in plant thermal tolerance.Crossref | GoogleScholarGoogle Scholar |

Perez TM, Socha A, Tserej O, Feeley KJ (2021b) Photosystem II heat tolerances characterize thermal generalists and the upper limit of carbon assimilation. Plant, Cell & Environment 44, 2321–2330.
Photosystem II heat tolerances characterize thermal generalists and the upper limit of carbon assimilation.Crossref | GoogleScholarGoogle Scholar |

Perkins SE, Alexander LV (2013) On the measurement of heat waves. Journal of Climate 26, 4500–4517.
On the measurement of heat waves.Crossref | GoogleScholarGoogle Scholar |

Perkins-Kirkpatrick SE, Gibson PB (2017) Changes in regional heatwave characteristics as a function of increasing global temperature. Scientific Reports 7, 12256
Changes in regional heatwave characteristics as a function of increasing global temperature.Crossref | GoogleScholarGoogle Scholar |

Perkins-Kirkpatrick SE, Lewis SC (2020) Increasing trends in regional heatwaves. Nature Communications 11, 3357
Increasing trends in regional heatwaves.Crossref | GoogleScholarGoogle Scholar |

Posch BC, Hammer J, Atkin OK, Bramley H, Ruan Y-L, Trethowan R, Coast O (2022) Wheat photosystem II heat tolerance responds dynamically to short- and long-term warming. Journal of Experimental Botany 73, 3268–3282.
Wheat photosystem II heat tolerance responds dynamically to short- and long-term warming.Crossref | GoogleScholarGoogle Scholar |

Rashid FAA, Crisp PA, Zhang Y, Berkowitz O, Pogson BJ, Day DA, Masle J, Dewar RC, Whelan J, Atkin OK, Scafaro AP (2020) Molecular and physiological responses during thermal acclimation of leaf photosynthesis and respiration in rice. Plant, Cell & Environment 43, 594–610.
Molecular and physiological responses during thermal acclimation of leaf photosynthesis and respiration in rice.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Renner MAM, Foster CSP, Miller JT, Murphy DJ (2020) Increased diversification rates are coupled with higher rates of climate space exploration in Australian Acacia (Caesalpinioideae). New Phytologist 226, 609–622.
Increased diversification rates are coupled with higher rates of climate space exploration in Australian Acacia (Caesalpinioideae).Crossref | GoogleScholarGoogle Scholar |

Sastry A, Barua D (2017) Leaf thermotolerance in tropical trees from a seasonally dry climate varies along the slow-fast resource acquisition spectrum. Scientific Reports 7, 11246
Leaf thermotolerance in tropical trees from a seasonally dry climate varies along the slow-fast resource acquisition spectrum.Crossref | GoogleScholarGoogle Scholar |

Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution 1, 103–113.
Simple means to improve the interpretability of regression coefficients.Crossref | GoogleScholarGoogle Scholar |

Schreiber U, Berry JA (1977) Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. Planta 136, 233–238.
Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |

Seemann JR, Berry JA, Downton WJS (1984) Photosynthetic response and adaptation to high temperature in desert plants. Plant Physiology 75, 364–368.
Photosynthetic response and adaptation to high temperature in desert plants.Crossref | GoogleScholarGoogle Scholar |

Sgrò CM, Overgaard J, Kristensen TN, Mitchell KA, Cockerell FE, Hoffmann AA (2010) A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia. Journal of Evolutionary Biology 23, 2484–2493.
A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2012) Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence. Functional Plant Biology 39, 936–947.
Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence.Crossref | GoogleScholarGoogle Scholar |

Slot M, Cala D, Aranda J, Virgo A, Michaletz ST, Winter K (2021) Leaf heat tolerance of 147 tropical forest species varies with elevation and leaf functional traits, but not with phylogeny. Plant, Cell & Environment 44, 2414–2427.
Leaf heat tolerance of 147 tropical forest species varies with elevation and leaf functional traits, but not with phylogeny.Crossref | GoogleScholarGoogle Scholar |

Smillie RM, Nott R (1979) Heat injury in leaves of alpine, temperate and tropical plants. Functional Plant Biology 6, 135–141.
Heat injury in leaves of alpine, temperate and tropical plants.Crossref | GoogleScholarGoogle Scholar |

Tabassum S, Manea A, Ossola A, Thomy B, Blackham D, Leishman MR (2021) The angriest summer on record: assessing canopy damage and economic costs of an extreme climatic event. Urban Forestry & Urban Greening 63, 127221
The angriest summer on record: assessing canopy damage and economic costs of an extreme climatic event.Crossref | GoogleScholarGoogle Scholar |

Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16, 53–60.
Photoprotection in plants: a new light on photosystem II damage.Crossref | GoogleScholarGoogle Scholar |

Terzaghi WB, Fork DC, Berry JA, Field CB (1989) Low and high temperature limits to PSII. Plant Physiology 91, 1494–1500.
Low and high temperature limits to PSII.Crossref | GoogleScholarGoogle Scholar |

Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
Heat tolerance in plants: an overview.Crossref | GoogleScholarGoogle Scholar |

Weis E (1982) Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Plant Physiology 70, 1530–1534.
Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. Journal of Plant Physiology 167, 959–966.
Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves.Crossref | GoogleScholarGoogle Scholar |

Zhu L, Bloomfield KJ, Hocart CH, Egerton JJG, O’Sullivan OS, Penillard A, Weerasinghe LK, Atkin OK (2018) Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. Plant, Cell & Environment 41, 1251–1262.
Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes.Crossref | GoogleScholarGoogle Scholar |