Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium
G. Heinrich Krause A B C , Klaus Winter A , Barbara Krause A and Aurelio Virgo AA Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panama City, Republic of Panama.
B Institute of Plant Biochemistry, Heinrich Heine University Düsseldorf, Universitätsstraße 1, 40225 Düsseldorf, Germany.
C Corresponding author. Email: ghkrause@uni-duesseldorf.de
Functional Plant Biology 42(1) 42-51 https://doi.org/10.1071/FP14095
Submitted: 27 March 2014 Accepted: 25 June 2014 Published: 20 August 2014
Abstract
Previous heat tolerance tests of higher plants have been mostly performed with darkened leaves. However, under natural conditions, high leaf temperatures usually occur during periods of high solar radiation. In this study, we demonstrate small but significant increases in the heat tolerance of illuminated leaves. Leaf disks of mature sun leaves from two neotropical tree species, Ficus insipida Willd. and Calophyllum longifolium Willd., were subjected to 15 min of heat treatment in the light (500 µmol photons m–2 s–1) and in the dark. Tissue temperatures were controlled by floating the disks on the surface of a water bath. PSII activity was determined 24 h and 48 h after heating using chlorophyll a fluorescence. Permanent tissue damage was assessed visually during long-term storage of leaf sections under dim light. In comparison to heat treatments in the dark, the critical temperature (T50) causing a 50% decline of the fluorescence ratio Fv/Fm was increased by ~1°C (from ~52.5°C to ~53.5°C) in the light. Moreover, illumination reduced the decline of Fv/Fm as temperatures approached T50. Visible tissue damage was reduced following heat treatment in the light. Experiments with attached leaves of seedlings exposed to increasing temperatures in a gas exchange cuvette also showed a positive effect of light on heat tolerance.
Additional keywords: carbon dioxide assimilation, dark respiration, global warming, necrosis, transpiration.
References
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541–550.| Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOgt7bF&md5=2dd294b9dfea2e1b31878a6900db7c5dCAS | 18649006PubMed |
Barua D, Heckathorn SA (2006) The interactive effects of light and temperature on heat-shock protein accumulation in Solidago altissima (Asteraceae) in the field and laboratory. American Journal of Botany 93, 102–109.
| The interactive effects of light and temperature on heat-shock protein accumulation in Solidago altissima (Asteraceae) in the field and laboratory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1Cqtw%3D%3D&md5=7205805c8c1a6490abc773dd56ea36f0CAS |
Bigras FJ (2000) Selection of white spruce families in the context of climate change: heat tolerance. Tree Physiology 20, 1227–1234.
| Selection of white spruce families in the context of climate change: heat tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovVGgs7o%3D&md5=cedbc0a890568e55e76dd33640822797CAS | 12651485PubMed |
Buchner O, Karadar M, Bauer I, Neuner G (2013) A novel system for in situ determination of heat tolerance of plants: first results on alpine dwarf shrubs. Plant Methods 9, 7
| A novel system for in situ determination of heat tolerance of plants: first results on alpine dwarf shrubs.Crossref | GoogleScholarGoogle Scholar | 23497517PubMed |
Cheesman AW, Winter K (2013a) Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species. New Phytologist 197, 1185–1192.
| Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOju7g%3D&md5=4248669d77227c1ffbe3ffc06b0824c0CAS | 23278464PubMed |
Cheesman AW, Winter K (2013b) Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings. Journal of Experimental Botany 64, 3817–3828.
| Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yrsr3E&md5=8156be7c582b0e9093f7b2a944b16b51CAS | 23873999PubMed |
Cramer W, Bondeau A, Schaphoff S, Lucht W, Smith B, Sitch S (2004) Tropical forests and global carbon cycle: impacts of atmospheric carbon dioxide, climate change and rate of deforestation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 331–343.
| Tropical forests and global carbon cycle: impacts of atmospheric carbon dioxide, climate change and rate of deforestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1SjsrY%3D&md5=fa69af509fc0e2833a2546f456f11e39CAS | 15212088PubMed |
Cunningham SC, Read J (2003) Do temperate rainforest trees have a greater ability to acclimate to changing temperatures than tropical rainforest trees? New Phytologist 157, 55–64.
| Do temperate rainforest trees have a greater ability to acclimate to changing temperatures than tropical rainforest trees?Crossref | GoogleScholarGoogle Scholar |
Cunningham SC, Read J (2006) Foliar temperature tolerance of temperate and tropical evergreen rain forest trees of Australia. Tree Physiology 26, 1435–1443.
| Foliar temperature tolerance of temperate and tropical evergreen rain forest trees of Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vlsVCktw%3D%3D&md5=eae845f03854ac6a4873a5357011b06bCAS | 16877328PubMed |
Debel K, Knack G, Kloppstech K (1994) Accumulation of plastid HSP 23 of Chenopodium rubrum is controlled post-translationally by light. The Plant Journal 6, 79–85.
| Accumulation of plastid HSP 23 of Chenopodium rubrum is controlled post-translationally by light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1Kmsrk%3D&md5=cd75d1b1db8b0bbe45ac4ab4ce4ada62CAS |
Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiology 84, 218–224.
| Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXkslCmsLc%3D&md5=f9288636643062d5d275a890a736ddf3CAS | 16665420PubMed |
Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant & Cell Physiology 39, 474–482.
| Survey of thermal energy dissipation and pigment composition in sun and shade leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsFSmtrY%3D&md5=3432d97d62ab92a0146100cd91f9fc9aCAS |
Diffenbaugh NS, Scherer M (2011) Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries. Climatic Change 107, 615–624.
| Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries.Crossref | GoogleScholarGoogle Scholar | 22707810PubMed |
Dongsansuk A, Lütz C, Neuner G (2013) Effects of temperature and irradiance on quantum yield of PSII photochemistry and xanthophyll cycle in a tropical and a temperate species. Photosynthetica 51, 13–21.
| Effects of temperature and irradiance on quantum yield of PSII photochemistry and xanthophyll cycle in a tropical and a temperate species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivFCgsL4%3D&md5=d3a6ad5c4cf7bb41c75254884acedff9CAS |
Ducruet J-M, Peeva V, Havaux M (2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynthesis Research 93, 159–171.
| Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlKgt70%3D&md5=cf2705b97a0897e2e552cff608971395CAS | 17279439PubMed |
Gamon JA, Pearcy RW (1990) Photoinhibition in Vitis californica. The role of temperature during high-light treatment. Plant Physiology 92, 487–494.
| Photoinhibition in Vitis californica. The role of temperature during high-light treatment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhvFCmsA%3D%3D&md5=73df3f46894264b04e4ee58581c750b3CAS | 16667302PubMed |
Hamerlynck EP, Knapp AK (1994) Leaf-level responses to light and temperature in two co-occurring Quercus (Fagaceae) species: implications for tree distribution patterns. Forest Ecology and Management 68, 149–159.
| Leaf-level responses to light and temperature in two co-occurring Quercus (Fagaceae) species: implications for tree distribution patterns.Crossref | GoogleScholarGoogle Scholar |
Havaux M (1992) Stress tolerance of photosystem II in vivo. Antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiology 100, 424–432.
| Stress tolerance of photosystem II in vivo. Antagonistic effects of water, heat, and photoinhibition stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgsbw%3D&md5=500ab1dc23af326376d0aa288db5b1f0CAS | 16652979PubMed |
Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences of the United States of America 96, 8762–8767.
| The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOkur4%3D&md5=a42ed184d90e01393d0c2bee996024a3CAS | 10411949PubMed | 10411949PubMed |
Havaux M, Strasser RJ (1990) Protection of photosystem II by light in heat-stressed pea leaves. Zeitschrift für Naturforschung 45c, 1133–1141.
Havaux M, Tardy F (1996) Temperature-dependent adjustment of thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198, 324–333.
| Temperature-dependent adjustment of thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvVertA%3D%3D&md5=c385f6e6764f365f23b0a2d9ea72009aCAS |
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: Analysis using in-vivo fluorescence, absorbance, oxygen and photoacoustic measurements. Planta 186, 88–98.
| Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light: Analysis using in-vivo fluorescence, absorbance, oxygen and photoacoustic measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFOltw%3D%3D&md5=16c7feac428335855ec7c5a90f25f3ecCAS | 24186579PubMed | 24186579PubMed |
Holtum JAM, Winter K (2003) Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentration of CO2. Planta 218, 152–158.
| Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentration of CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovV2ltLg%3D&md5=80ae92d7bd170ab93da4ada61c189331CAS |
Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 655–684.
| Regulation of light harvesting in green plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgt70%3D&md5=6a16ea14be5baac43826fcf35cb18fc3CAS | 15012304PubMed | 15012304PubMed |
Jentsch A, Beierkuhnlein C (2008) Research frontiers in climate change: effects of extreme meteorological events on ecosystems. Comptes Rendus Geoscience 340, 621–628.
| Research frontiers in climate change: effects of extreme meteorological events on ecosystems.Crossref | GoogleScholarGoogle Scholar |
Johnson MP, Havaux M, Triantaphylidès C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. The Journal of Biological Chemistry 282, 22 605–22 618.
| Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1WjtLk%3D&md5=0cb6e22da18669a3888f222bb05c242dCAS |
Kislyuk IM, Bubolo LS, Bykov OD, Kamentseva IE, Sherstneva OA (2008) Protective and injuring action of visible light on photosynthetic apparatus in wheat plants during hyperthermia treatment. Russian Journal of Plant Physiology 55, 613–620.
| Protective and injuring action of visible light on photosynthetic apparatus in wheat plants during hyperthermia treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGgt73L&md5=b153964e8cb002c248b49bd4af9cd39aCAS |
Kitao M, Lei TT, Koike T, Tobita H, Maruyama Y, Matsumoto Y, Ang LH (2000) Temperature response and photoinhibition investigated by chlorophyll fluorescence measurements for four distinct species of dipterocarp trees. Physiologia Plantarum 109, 284–290.
| Temperature response and photoinhibition investigated by chlorophyll fluorescence measurements for four distinct species of dipterocarp trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvFCru7s%3D&md5=9d8c585739ae4fcf1bef3fa97a2dee6bCAS |
Königer M, Harris GC, Pearcy RW (1998) Interaction between photon flux density and elevated temperatures on photoinhibition in Alocasia macrorrhiza. Planta 205, 214–222.
| Interaction between photon flux density and elevated temperatures on photoinhibition in Alocasia macrorrhiza.Crossref | GoogleScholarGoogle Scholar |
Kouřil R, Lazár D, Ilík P, Skotnica J, Krchňák P, Nauš J (2004) High-temperature induced chlorophyll fluorescence rise in plants at 40−50°C: experimental and theoretical approach. Photosynthesis Research 81, 49–66.
| High-temperature induced chlorophyll fluorescence rise in plants at 40−50°C: experimental and theoretical approach.Crossref | GoogleScholarGoogle Scholar | 16328847PubMed | 16328847PubMed |
Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 463–495. (Springer: Dordrecht).
Krause GH, Gallé A, Virgo A, García M, Bucic P, Jahns P, Winter K (2006) High-light stress does not impair biomass accumulation of sun-acclimated tropical tree seedlings (Calophyllum longifolium Willd. and Tectona grandis L.f.). Plant Biology 8, 31–41.
| High-light stress does not impair biomass accumulation of sun-acclimated tropical tree seedlings (Calophyllum longifolium Willd. and Tectona grandis L.f.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtlWksLk%3D&md5=0d719ea3c832ca0fa738f919286184f3CAS | 16435267PubMed | 16435267PubMed |
Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, Virgo A (2010) High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations. Functional Plant Biology 37, 890–900.
| High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations.Crossref | GoogleScholarGoogle Scholar |
Krause GH, Cheesman AW, Winter K, Krause B, Virgo A (2013) Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures. Journal of Plant Physiology 170, 822–827.
| Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit12jtrs%3D&md5=1d06915cc7f6000aaac6ab0aede1c19eCAS | 23399405PubMed | 23399405PubMed |
Lintner BR, Biasutti M, Diffenbaugh NS, Lee JE, Niznik MJ, Findell KL (2012) Amplification of wet and dry month occurrence over tropical land regions in response to global warming. Journal of Geophysical Research, D, Atmospheres 117, D11106
| Amplification of wet and dry month occurrence over tropical land regions in response to global warming.Crossref | GoogleScholarGoogle Scholar |
Lu CM, Zhang JH (2000) Heat-induced multiple effects on PSII in wheat plants. Journal of Plant Physiology 156, 259–265.
| Heat-induced multiple effects on PSII in wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1yitLY%3D&md5=40e3866ecf9bb066af87d7eb1eeabacaCAS |
Malhi Y, Wright J (2004) Spatial patterns and recent trends in the climate of tropical rainforest regions. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 311–329.
| Spatial patterns and recent trends in the climate of tropical rainforest regions.Crossref | GoogleScholarGoogle Scholar | 15212087PubMed | 15212087PubMed |
Marutani Y, Yamauchi Y, Kimura Y, Mizutani M, Sugimoto Y (2012) Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta 236, 753–761.
| Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyks7jL&md5=1998bd2cb518854c01e508a1d3e82122CAS | 22526503PubMed | 22526503PubMed |
Méthy M, Gillon D, Houssard C (1997) Temperature-induced changes of photosystem II activity in Quercus ilex and Pinus halepensis. Canadian Journal of Forest Research 27, 31–38.
| Temperature-induced changes of photosystem II activity in Quercus ilex and Pinus halepensis.Crossref | GoogleScholarGoogle Scholar |
Munasinghe L, Jun T, Rind DH (2012) Climate change: a new metric to measure changes in the frequency of extreme temperatures using record data. Climatic Change 113, 1001–1024.
| Climate change: a new metric to measure changes in the frequency of extreme temperatures using record data.Crossref | GoogleScholarGoogle Scholar |
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767, 414–421.
| Photoinhibition of photosystem II under environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1ygsLw%3D&md5=ade4b1efca3c2d7f102c14bb4ed7c4dfCAS | 17207454PubMed | 17207454PubMed |
Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochimica et Biophysica Acta 1817, 1127–1133.
| The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xkt1Ghsbg%3D&md5=bfdc0a8d7c68cfc99351546eb0d3a796CAS | 22387427PubMed | 22387427PubMed |
Ohira S, Morita N, Suh H-J, Jung J, Yamamoto Y (2005) Quality control of photosystem II under light stress – turnover of aggregates of the D1 protein in vivo. Photosynthesis Research 84, 29–33.
| Quality control of photosystem II under light stress – turnover of aggregates of the D1 protein in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yitb0%3D&md5=675591dd71d98f3a61bb2186434e67f8CAS | 16049751PubMed | 16049751PubMed |
Öquist G, Chow WS, Anderson JM (1992) Photoinhibtion of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186, 450–460.
| Photoinhibtion of photosynthesis represents a mechanism for the long-term regulation of photosystem II.Crossref | GoogleScholarGoogle Scholar | 24186743PubMed | 24186743PubMed |
Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiology 130, 1109–1120.
| Global changes in gene expression in response to high light in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOnu7g%3D&md5=584d546fbf5122ceb99f71c7b2d294e0CAS | 12427978PubMed | 12427978PubMed |
Sachs J (1864) Ueber die obere Temperaturgränze der Vegetation. Flora 47, 5–65–75.
Schreiber U, Berry JH (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 | 1:CAS:528:DyaE2sXlvVSqs7w%3D&md5=a88aec02cee3c5e1cef054e74c3cede8CAS | 24420396PubMed | 24420396PubMed |
Slot M, Rey-Sánchez C, Gerber S, Lichstein JW, Winter K, Kitajima K (2014) Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical carbon balance. Global Change Biology 20, 2915–2926.
| Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical carbon balance.Crossref | GoogleScholarGoogle Scholar | 24604769PubMed | 24604769PubMed |
Smillie RM, Nott R (1979) Heat injury in leaves of alpine, temperate and tropical plants. Australian Journal of Plant Physiology 6, 135–141.
| Heat injury in leaves of alpine, temperate and tropical plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXitVSlsb0%3D&md5=c37b59f8cfd8ab91178a77b4d0acfab8CAS |
Stapel D, Kruse E, Kloppstech K (1993) The protective effect of heat shock proteins against photoinhibition under heat shock in barley (Hordeum vulgare). Journal of Photochemistry and Photobiology. B, Biology 21, 211–218.
| The protective effect of heat shock proteins against photoinhibition under heat shock in barley (Hordeum vulgare).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVCntA%3D%3D&md5=bce1bf0563757528189da7bbbdf4277eCAS |
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 | 1:CAS:528:DC%2BC3MXjvFOgtw%3D%3D&md5=e86a07a0f00f7464ff6935885c141a60CAS | 21050798PubMed | 21050798PubMed |
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 | 1:CAS:528:DC%2BD2sXhvFWnsLg%3D&md5=2fca60efbdcb2b20e78cad4b98c47a7dCAS | 17142484PubMed | 17142484PubMed |
Weng J-H, Lai M-F (2005) Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. Photosynthetica 43, 439–444.
| Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVylu7zO&md5=11ea083ff18c8ad13f57314b42a417c4CAS |
Zotz G, Harris G, Königer M, Winter K (1995) High rates of photosynthesis in the tropical pioneer tree, Ficus insipida Willd. Flora 190, 265–272.