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The Photosynthetic System in Tropical Plants Under High Irradiance and Temperature Stress

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Progress in Botany Vol. 82

Part of the book series: Progress in Botany ((BOTANY,volume 82))

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Abstract

Plants in the tropics frequently experience stressful environmental conditions such as excessive sunlight including solar ultraviolet (UV) radiation or high leaf temperatures. In view of progressing climate change, the combination of various stress factors, particularly during extreme drought periods and heat waves, may cause damage to the photosynthetic system followed by cell death in leaves, resulting in reduction of total photosynthetic productivity. The present article reviews a series of investigations on tropical forest species in Panama. Recording of chlorophyll a (Chl a) fluorescence parameters served as a versatile method to assess the degree of damage and acclimation in chloroplasts. Analysis of chloroplast pigments and antioxidative cell constituents provided valuable information on the acclimation state of leaves. The studies indicate that tropical plants are capable of adjusting to potentially harmful conditions in their respective habitats. One important way of protecting photosystem II is the operation of the violaxanthin cycle and, in certain species, the lutein epoxide cycle. Responses to excess solar radiation in young and mature canopy sun leaves, in leaves of plants growing in treefall gaps and understory of the tropical forest are highlighted. The response of photosystem I to excessive visible light, as well as damaging and acclimatory processes induced by solar UV radiation in photosystems I and II, has been investigated. A reassessed method of Chl a fluorescence measurements was used to determine the limits of heat tolerance in sun and shade leaves of C3 species and in sun leaves of species exhibiting crassulacean acid metabolism (CAM).

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References

  • Allen JF (2003) State transitions – a question of balance. Science 299:1530–1532

    CAS  PubMed  Google Scholar 

  • Allen DJ, McKee IF, Farage PK, Baker NR (1997) Analysis of limitations to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640

    CAS  Google Scholar 

  • Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Ǻ resolution. Nature 447:58–63

    CAS  PubMed  Google Scholar 

  • Anderson JM, Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition, Topics in photosynthesis, vol 9. Elsevier, Amsterdam, pp 1–38

    Google Scholar 

  • Aro EM, McCaffery S, Anderson JM (1993a) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103:835–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993b) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    CAS  PubMed  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplast: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    CAS  PubMed  Google Scholar 

  • Asner GB, Scurlock JM, Hicke JA (2003) Global synthesis of leaf area index observations: implications for ecological and remote sensing studies. Glob Ecol Biogeogr 12:191–205

    Google Scholar 

  • Barnes PW, Flint SD, Ryel RJ, Tobler MA, Barkley AE, Wargent JJ (2015) Rediscovering leaf optical properties: new insights into plant acclimation to solar UV radiation. Plant Physiol Biochem 93:94–100

    CAS  PubMed  Google Scholar 

  • Barth C, Krause GH (1999) Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch 54c:645–657

    Google Scholar 

  • Barth C, Krause GH (2002) Study of tobacco transformants to assess the role of chloroplastic NAD(P)H dehydrogenase in photoprotection of photosystems I and II. Planta 216:273–279

    CAS  PubMed  Google Scholar 

  • Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Envir 24:163–176

    CAS  Google Scholar 

  • Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron-transport. Biochim Biophys Acta 1229:23–38

    Google Scholar 

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

    Google 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

    Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. Planta 179:489–504

    Google Scholar 

  • Bornman JF, Barnes PW, Robson TM, Robinson SA, Jansen MAK, Ballaré CL, Flint SD (2019) Linkages between stratospheric ozone, UV radiation and climate change and their implications for terrestrial ecosystems. Photochem Photobiol Sci 18:681–716

    CAS  PubMed  Google Scholar 

  • Boyer JS (2017) Plant water relations: a whirlwind of change. Progr Bot 79:1–31

    Google Scholar 

  • Braun V, Buchner O, Neuner G (2002) Thermotolerance of photosystem II of three alpine plant species under field conditions. Photosynthetica 40:587–595

    CAS  Google Scholar 

  • Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318:322–373

    CAS  Google 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 Envir 38:812–826

    CAS  Google Scholar 

  • Burchard P, Bilger B, Weissenböck G (2000) Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant Cell Environ 23:1373–1380

    CAS  Google Scholar 

  • Butler WJ (1978) Energy distribution in the photosynthetic apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378

    CAS  Google Scholar 

  • Camus GC, Went FW (1952) Thermoperiodicity of three varieties of Nicotiana tabacum. Amer J Bot 38:521–528

    Google Scholar 

  • Cernusak LA, Mejia-Chang M, Winter K, Griffith H (2008) Oxygen isotope composition of CAM and C3 Clusia species: non-steady-state dynamics control leaf water 18O enrichment in succulent leaves. Plant Cell Envir 31:1644–1662

    CAS  Google Scholar 

  • Chaves CJN, Santos Leal BS, de Lemos-Filho JP (2015) Temperature modulation of thermal tolerance of a CAM-tank bromeliad and the relationship with acid accumulation in different leaf regions. Physiol Plant 154:500–510

    CAS  PubMed  Google Scholar 

  • Cheesman AW, Winter K (2013a) Elevated night-time temperatures increase growth in seedlings of two tropical pioneer species. New Phytol 197:1185–1192

    CAS  PubMed  Google Scholar 

  • Cheesman AW, Winter K (2013b) Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings. J Exp Bot 64:3817–3828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BL (2018) Triggers of tree mortality under drought. Nature 558:531–539

    CAS  PubMed  Google Scholar 

  • Clark DB, Olivas PC, Oberbauer SF, Clark DA, Ryan MG (2008) First direct landscape-scale measurement of tropical rain forest leaf area index, a key driver of global primary productivity. Ecol Lett 11:163–172

    PubMed  Google Scholar 

  • Clark DB, Clark DA, Oberbauer SF (2010) Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO2. Glob Change Biol 16:747–759

    Google Scholar 

  • Correa Galvis V, Poschmann G, Melzer M, Stühler K, Jahns P (2016) PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nature Plants 2:15225

    CAS  PubMed  Google Scholar 

  • Cunningham SC, Read J (2003) Do temperate rainforest trees have a greater ability to acclimate to changing temperatures than tropical rainforest trees? New Phytol 157:55–64

    Google Scholar 

  • Cunningham SC, Read J (2006) Foliar temperature tolerance of temperate and tropical evergreen rain forests in Australia. Tree Physiol 26:1435–1443

    CAS  PubMed  Google Scholar 

  • 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 Physiol 84:599–626

    Google Scholar 

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482

    CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Winkelmann E, Krüger A, Czygan F-C (1989) Photosynthetic characteristics and the ratios of chlorophyll, β-carotene, and the components of the xanthophyll cycle upon a sudden increase in growth light regime in several plant species. Plant Biol (formerly Bot Acta) 102:319–325

    CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–260

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google 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, DeKauwe 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. Glob Change Biol 24:2390–2402

    Google Scholar 

  • Ducruet J-M, Peeva V, Havaux M (2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynth Res 93:159–171

    CAS  PubMed  Google Scholar 

  • Duke NC, Kovacs JM, Griffith AD, Preece L, Hill DJE, van Oosterzee P, Mackenzie J, Morning HS, Burrows D (2017) Large-scale dieback of mangroves in Australia’s Gulf of Carpentaria: a severe ecosystem response, coincidental with an unusually extreme weather event. Mar Freshw Res 68:1816–1829

    Google Scholar 

  • Edge R, McGarvey DJ, Truscott TG (1997) The carotenoids as anti-oxidants – a review. J Photochem Photobiol B Biol 41:189–200

    CAS  Google Scholar 

  • Endo T, Shikanai T, Takabayashi A, Asada K, Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457:5–8

    CAS  PubMed  Google Scholar 

  • Esteban R, Jiménez ET, Jiménez MS, Morales D, Hormaetxe K, Becerril JM, García-Plazaola JI (2007) Dynamics of violaxanthin and lutein epoxide xanthophyll cycles in Lauraceae tree species under field conditions. Tree Physiol 27:1407–1414

    CAS  PubMed  Google Scholar 

  • Esteban R, Jiménez MS, Morales D, Jiménez ET, Hormaetxe K, Becerril JM, Osmond B, García-Plazaola JI (2008) Short- and long-term modulation of the lutein epoxide and violaxanthin cycle in two species of the Lauraceae: sweet bay laurel (Laurus nobilis L.) and avocado (Persea americana Mill.). Plant Biol 10:288–297

    CAS  PubMed  Google Scholar 

  • Färber A, Young AJ, Ruban AV, Horton P, Jahns P (1997) Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants. Plant Physiol 115:1609–1618

    PubMed  PubMed Central  Google Scholar 

  • Fioletov VE, Bodeker GE, Miller AJ, McPeters RD, Stolarski R (2002) Global and zonal total ozone variations estimated from ground-based and satellite measurements: 1964-2000. J Geophys Res-Atmos 107(D22):4647

    Google Scholar 

  • Fork DC, Herbert SK (1993) Electron-transport and photophosphorylation by photosystem-I in vivo in plants and cyanobacteria. Photosynth Res 36:149–168

    CAS  PubMed  Google Scholar 

  • Förster B, Osmond CB, Pogson BJ (2009) De novo synthesis and degradation of Lx and V cycle pigments during shade and sun acclimation in avocado leaves. Plant Physiol 149:1179–1195

    PubMed  PubMed Central  Google Scholar 

  • Franco AC, Lüttge U (2002) Midday depression in savanna trees: coordinated adjustments in photosynthetic efficiency, photorespiration, CO2 assimilation and water use efficiency. Oecologia 131:356–365

    CAS  PubMed  Google Scholar 

  • Friso G, Barbato R, Giacometti GM, Barber J (1994) Degradation of the D1 protein due to UV-B irradiation of the reaction centre of photosystem II. FEBS Lett 339:217–221

    CAS  PubMed  Google Scholar 

  • Fryer MJ (1992) The antioxidative effect of thylakoid Vitamin E (α-tocopherol). Plant Cell Environ 15:381–392

    CAS  Google Scholar 

  • Gamon JA, Pearcy RW (1990) Photoinhibition in Vitis californica. The role of temperature during high-light treatment. Plant Physiol 92:487–494

    CAS  PubMed  PubMed Central  Google Scholar 

  • García-Plazaola JI, Becerril JM, Hernández A, Niinemets U, Kollist H (2004) Acclimation of antioxidant pools to the light environment in a natural forest canopy. New Phytol 163:87–97

    Google Scholar 

  • García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationship to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773

    PubMed  Google Scholar 

  • Gerola AP, Tsubone TM, Santana A, De Oliveira HPM, Hioka N, Caetano W (2011) Properties of chlorophyll and derivatives in homogeneous and microheterogeneous systems. J Phys Chem B 115:7364–7373

    CAS  PubMed  Google Scholar 

  • Harbinson J, Genty B, Baker NR (1989) Relationship between quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol 90:1029–1034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem-II activity. Photosynth Res 40:75–92

    CAS  PubMed  Google 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: analysis using in vivo fluorescence, absorbance, oxygen and photoacoustic measurements. Planta 186:88–98

    CAS  PubMed  Google Scholar 

  • Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    CAS  PubMed  PubMed Central  Google Scholar 

  • Havaux M, Dall’Ostro L, Bassi R (2007) Zeaxanthin has enhanced antioxidative capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron-transport in leaves. Plant Physiol 100:1621–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hernández GG, Winter K, Slot M (2020) Similar temperature dependence of photosynthetic parameters in sun and shade leaves of three tropical tree species. Tree Physiol 40:637–651

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. IPCC, Geneva, Switzerland, p 151

    Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    CAS  PubMed  Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    CAS  PubMed  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135

    Google Scholar 

  • Joet T, Cournac L, Horvath EM, Medgyesy P, Peltier G (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol 125:1919–1929

    CAS  PubMed  PubMed Central  Google 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. J Biol Chem 282:22605–22618

    CAS  PubMed  Google Scholar 

  • Kaiser E, Correa Galvis V, Armbruster U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast’s perspective. Biochem J 476:2725–2741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    CAS  Google Scholar 

  • Kolb CA, Käser MA, Kopecky J, Zotz G, Riederer M, Pfündel EE (2001) Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves (Vitis vinifera cv. Silvaner). Plant Physiol 127:863–875

    CAS  PubMed  PubMed Central  Google Scholar 

  • Königer M, Winter K (1993) Growth and photosynthesis of Gossypium hirsutum L. at high photon flux densities: effects of soil temperatures and nocturnal air temperatures. Agronomie 13:423–431

    Google Scholar 

  • Königer M, Harris GC, Virgo A, Winter K (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants. Oecologia 104:280–290

    PubMed  Google 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. Photosynth Res 81:49–66

    PubMed  Google Scholar 

  • Kozuleva MA, Ivanov BN (2016) The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol 67:1397–1404

    Google Scholar 

  • Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187

    CAS  Google Scholar 

  • Krause GH, Jahns P (2003) Pulse amplitude modulated chlorophyll fluorometry and its application in plant science. In: Green BR, Parson WW (eds) Light harvesting antennas in photosynthesis, Advances in photosynthesis and respiration, vol 13. Kluwer Academic Publishers, Dordrecht, pp 373–399

    Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching. Characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 14. Springer, Heidelberg, pp 463–495

    Google Scholar 

  • Krause GH, Santarius KA (1975) Relative thermostability of the chloroplast envelope. Planta 127:285–299

    CAS  PubMed  Google Scholar 

  • Krause GH, Winter K (1996) Photoinhibition of photosynthesis in plants growing in natural tropical forest gaps. A chlorophyll fluorescence study. Bot Acta 109:456–462

    CAS  Google Scholar 

  • Krause GH, Virgo A, Winter K (1995) High susceptibility to photoinhibition of young leaves of tropical forest trees. Planta 197:583–591

    CAS  Google Scholar 

  • Krause GH, Schmude C, Garden H, Koroleva OY, Winter K (1999) Effects of solar ultraviolet radiation on the potential efficiency of photosystem II in leaves of tropical plants. Plant Physiol 121:1349–1358

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352

    CAS  Google Scholar 

  • Krause GH, Grube E, Virgo A, Winter K (2003a) Sudden exposure to solar UV-B radiation reduces net CO2 uptake and photosystem I efficiency in shade-acclimated tropical tree seedlings. Plant Physiol 131:745–752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krause GH, Gallé A, Gademann R, Winter K (2003b) Capacity of protection against ultraviolet radiation in sun and shade leaves of tropical forest plants. Funct Plant Biol 30:533–542

    CAS  PubMed  Google Scholar 

  • Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Funct Plant Biol 31:743–756

    PubMed  Google Scholar 

  • 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 Biol 8:31–41

    CAS  PubMed  Google Scholar 

  • Krause GH, Jahns P, Virgo A, García M, Aranda J, Wellmann E, Winter K (2007) Photoprotection, photosynthesis and growth of tropical tree seedlings under near-ambient and strongly reduced solar ultraviolet-B radiation. J Plant Physiol 164:1311–1322

    CAS  PubMed  Google Scholar 

  • 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. Funct Plant Biol 37:890–900

    Google Scholar 

  • Krause GH, Winter K, Matsubara S, Krause B, Jahns P, Virgo A, Aranda J, García M (2012) Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight. Photosynth Res 113:273–285

    CAS  PubMed  Google 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. J Plant Physiol 170:822–827

    CAS  PubMed  Google 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. Funct Plant Biol 42:42–51. https://doi.org/10.1071/FP14095

    Article  CAS  Google Scholar 

  • Krause GH, Winter K, Krause B, Virgo A (2016) Protection by light against heat stress in leaves of tropical crassulacean acid metabolism plants containing high acid levels. Funct Plant Biol 43:1061–1069. https://doi.org/10.1071/FP16093

    Article  CAS  PubMed  Google Scholar 

  • Kress E, Jahns P (2017) The dynamics of energy dissipation and xanthophyll conversion in Arabidopsis indicate an indirect photoprotective role of zeaxanthin in slowly inducible and relaxing components of non-photochemical quenching of excitation energy. Front Plant Sci 8:2094

    PubMed  PubMed Central  Google Scholar 

  • Lehrum W, Kappen L, Lösch R (1987) Zusammenhang zwischen Hitzeresistenz und Säuregehalt in sukkulenten Pflanzen. Verhandlungen Gesellschaft Ökologie 16:207–212

    Google Scholar 

  • Leitsch J, Schnettger B, Critchley C, Krause GH (1994) Two mechanisms of recovery from photoinhibition in vivo: reactivation of photosystem II related and unrelated to D1-prtein turnover. Planta 194:15–21

    CAS  Google Scholar 

  • Li X-P, Gilmore AM, Caffari S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing of the PsbS protein. J Biol Chem 279:22866–22874

    CAS  PubMed  Google Scholar 

  • Lima-Melo Y, Gollan PJ, Tikkanen M, Silveira JAG, Aro EM (2019) Consequences of photosystem-I damage and repair on photosynthesis and carbon use in Arabidopsis thaliana. Plant J 97:1061–1072

    CAS  PubMed  Google Scholar 

  • Liu L-X, Xu S-M, Woo KC (2005) Solar UV-B radiation on growth, photosynthesis and the xanthophyll cycle in tropical acacias and eucalyptus. Environ Exp Bot 54:121–130

    CAS  Google Scholar 

  • Lösch R, Kappen L (1983) Die Temperaturresistenz makaronesischer Sempervivoideae. Verhandlungen Gesellschaft Ökologie 10:521–528

    Google Scholar 

  • Lovelock CE, Jebb M, Osmond CB (1994) Photoinhibition and recovery in tropical plant species: response to disturbance. Oecol 97:297–307

    CAS  Google Scholar 

  • Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin

    Google Scholar 

  • Lüttge U, Smith JAC (1984) Mechanisms of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoë daigremontiana. J Membr Biol 81:149–158

    Google Scholar 

  • Malnoë A (2018) Photoinhibition or photoprotection of photosynthesis? Update of the (newly termed) sustained quenching component qH. Envir Exp Bot 154:123–133

    Google Scholar 

  • Manuel N, Cornic G, Aubert S, Choler P, Bligny R, Heber U (1999) Protection against photoinhibition in the alpine plant Geum montanum. Oecologia 119:149–158

    CAS  PubMed  Google Scholar 

  • Markstädter C, Queck I, Baumeister J, Riederer M, Schreiber U, Bilger W (2001) Epidermal transmittance of leaves of Vicia faba for UV radiation as determined by two different methods. Photosynth Res 67:17–25

    PubMed  Google Scholar 

  • Matsubara S, Gilmore AM, Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii. Aust J Plant Physiol 28:793–800

    CAS  Google Scholar 

  • Matsubara S, Naumann M, Martin R, Nichol C, Rascher U, Morosinotto T, Bassi R, Osmond B (2005) Slowly reversible de-epoxidation of lutein epoxide in deep shade leaves of a tropical tree legume may ‘lock in’ lutein-based photoprotection during acclimation to strong light. J Exper Bot 56:461–468

    CAS  Google Scholar 

  • Matsubara S, Morosinotto T, Osmond B, Bassi R (2007) Short- and long-term operation of the lutein epoxide cycle in light-harvesting antenna complexes. Plant Phsiol 144:926–941

    CAS  Google Scholar 

  • Matsubara S, Krause GH, Seltmann M, Virgo A, Kursar TA, Jahns P, Winter K (2008) Lutein epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga. Plant Cell Environ 31:548–561

    CAS  PubMed  Google Scholar 

  • Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36:20–36. https://doi.org/10.1071/FP08214

    Article  CAS  PubMed  Google Scholar 

  • Mulkey SS, Pearcy RW (1992) Interactions between acclimation and photoinhibition of photosynthesis of a tropical understory herb, Alocasia macrorrhiza, during simulated canopy gap formation. Funct Ecol 6:719–729

    Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    CAS  PubMed  Google Scholar 

  • Muraoka H, Tang Y, Terashima I, Koizumi H, Washitani I (2000) Contributions of diffusional limitation, photoinhibition and photorespiration to midday depression in Arisaema heterophyllum in natural light. Plant Cell Environ 23:235–250

    CAS  Google Scholar 

  • Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwath AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component on non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophy Acta 1797:466–475

    CAS  Google Scholar 

  • Nobel PS (1988) Environmental biology of agaves and cacti. Cambridge University Press, Cambridge

    Google Scholar 

  • O’Sullivan OS, Heskel MA, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A, Zhu L, Egerton JJ, Bloomfield KJ, Creek D, Bahar NH, Griffin KL, Hurry V, Meir P, Turnbull MH, Atkin OK (2017) Thermal limits of leaf metabolism across biomes. Glob Change Biol 23:209–223

    Google Scholar 

  • Phillips OL, Aragao LEOC, Luiz SL et al (2009) Drought sensitivity of the Amazon rainforest. Science 323:1344–1347

    CAS  PubMed  Google Scholar 

  • Polm M, Brettel K (1998) Secondary pair charge recombination in photosystem I under strongly reducing conditions: temperature dependence and suggested mechanism. Biophys J 74:3173–3181

    CAS  PubMed  PubMed Central  Google Scholar 

  • Popp M, Kramer C, Lee H, Diaz M, Ziegler H, Lüttge U (1987) Crassulacean acid metabolism in tropical dicotyledonous trees of the genus Clusia. Trees – Struct Funct 1:238–247

    CAS  Google Scholar 

  • Reuber S, Leitsch J, Krause GH, Weissenböck G (1993) Metabolic reduction of phenylpropanoid compounds in primary leaves of rye (Secale cereale L.) leads to increased UV-B sensitivity of photosynthesis. Z Naturforsch 48c:749–756

    Google Scholar 

  • Reuber S, Bornman JF, Weissenböck G (1996) Phenylpropanoid compounds in primary leaf tissue of rye (Secale cereale): light response of their metabolism and the possible role in UV-B protection. Physiol Plant 97:160–168

    CAS  Google Scholar 

  • Rey-Sánchez AC, Slot M, Posada JM, Kitajima K (2016) Spatial and seasonal variation of leaf temperature within the canopy of a tropical forest. Climate Res 71:75–89

    Google Scholar 

  • Sacharz J, Giovagnetti V, Ungerer P, Mastroianni G, Ruban AV (2017) The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching. Nature Plants 3:16225

    PubMed  Google Scholar 

  • Sachs J (1864) Ueber die obere Temperatur-Gränze der Vegetation. Flora 47:5–12, 24–29, 33–39, 65–75

    Google Scholar 

  • Sastry A, Barua D (2017) Leaf thermotolerance in tropical trees from a seasonally dry climate varies along the slow-fast resource acquisition spectrum. Sci Rep 7:1–11

    CAS  Google Scholar 

  • Scheer H (2003) The pigments. In: Green R, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 29–81

    Google Scholar 

  • Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–272

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    CAS  PubMed  Google Scholar 

  • Schwemmle B, Lange OL (1959) Endogen-tagesperiodische Schwankungen der Hitzeresistenz bei Kalanchoë blossfeldiana. Planta 53:134–144

    Google Scholar 

  • Searles PS, Caldwell MM, Winter K (1995) The response of five tropical dicotyledon species to solar ultraviolet-B radiation. Amer J Bot 82:445–453

    Google Scholar 

  • Slot M, Winter K (2018) High tolerance of tropical sapling growth and gas exchange to moderate warming. Funct Ecol 32:599–611

    Google Scholar 

  • 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 Biol 20:2915–2926

    Google Scholar 

  • Slot M, García MN, Winter K (2016) Temperature responses of CO2 exchange in three tropical tree species. Funct Plant Biol 43:468–478

    CAS  PubMed  Google Scholar 

  • Slot M, Krause GH, Krause B, Hernández GG, Winter K (2019) Photosynthetic heat tolerance of shade and sun leaves of three tropical tree species. Photosynth Res 141:119–130

    CAS  PubMed  Google Scholar 

  • Smillie RM, Nott R (1979) Heat injury in leaves of alpine, temperate and tropical plants. J Plant Physiol 6:135–141

    CAS  Google Scholar 

  • Smith JAC, Ingram J, Tsiantis MS, Barkla BJ, Bartholomew DM, Bettey M, Pantoja O, Pennington AJ (1996) Transport across the vacuolar membrane in CAM plants. In: Winter K, Smith JAC (eds) Ecological studies. Crassulacean acid metabolism, Biochemistry, ecophysiology and evolution, vol 114. Springer, Berlin, pp 53–71

    Google Scholar 

  • Snyder AM, Clark BM, Bungard RA (2005) Light-dependent conversion of carotenoids in the parasitic angiosperm Cuscuta reflexa L. Plant Cell Environ 28:1326–1333

    CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    CAS  PubMed  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transients in plants and cyanobacteria. Photochem Photobiol 61:32–42

    CAS  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    CAS  PubMed  Google Scholar 

  • Teicher HB, Scheller HV (1998) The NAD(P)H dehydrogenase in barley thylakoids is photoactivatable and uses NADPH as well as NADH. Plant Physiol 117:525–532

    CAS  Google Scholar 

  • Teicher HB, Møller BL, Scheller HV (2000) Photoinhibition of photosystem I in field-grown barley (Hordeum vulgare L.): induction, recovery and acclimation. Photosynth Res 64:53–61

    CAS  Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    CAS  Google Scholar 

  • Thayer SS, Björkman O (1992) Carotenoid distribution and de-epoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth Res 33:213–225

    CAS  PubMed  Google Scholar 

  • Thiele A, Schirwitz K, Winter K, Krause GH (1996) Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light. Plant Sci 115:237–250

    CAS  Google Scholar 

  • Thiele A, Winter K, Krause GH (1997) Low inactivation of D1 protein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress. J Plant Physiol 151:286–292

    CAS  Google Scholar 

  • Thiele A, Krause GH, Winter K (1998) In situ study of photoinhibition of photosynthesis and xanthophyll cycle activity in plants growing in natural gaps of the tropical forest. Aust J Plant Physiol 25:189–195

    Google Scholar 

  • Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183

    CAS  PubMed  Google Scholar 

  • Tikkanen M, Grebe S (2018) Switching off photoprotection of photosystem I – a novel tool for gradual PSI photoinhibition. Physiol Plant 162:156–161

    CAS  PubMed  Google Scholar 

  • Tiwari A, Mamedov F, Grieco M, Suorsa M, Jajoo A, Styring S, Tikkanen M, Aro EM (2016) Photodamage of iron-sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nat Plants 2:16035

    CAS  PubMed  Google Scholar 

  • Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764

    CAS  PubMed  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Google Scholar 

  • Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25

    Google Scholar 

  • White RC, Gibbs E, Butler LS (1977) Estimation of copper pheophytins, chlorophylls and pheophytins in mixtures in diethyl ether. J Agric Food Chem 25:143–145

    CAS  Google Scholar 

  • Wilson S, Ruban AV (2019) Quantitative assessment of the high-light tolerance in plants with impaired photosystem II donor side. Biochem J 476:1377–1386

    CAS  PubMed  Google Scholar 

  • Winter K, Holtum JAM (2014) Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis. J. Exp Bot 65:3425–3441

    Google Scholar 

  • Winter K, García M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë and Opuntia. J Exp Bot 59:1829–1840

    CAS  PubMed  Google Scholar 

  • Winter K, García M, Holtum JAM (2014) Nocturnal versus diurnal CO2 uptake: how flexible is Agave angustifolia? J Exp Bot 65:3695–3703

    PubMed  PubMed Central  Google Scholar 

  • Yavitt JB, Battles JJ, Lang GE, Knight DH (1995) The canopy gap regime in a secondary neotropical forest in Panama. J Trop Ecol 11:391–402

    Google Scholar 

  • Yu Z-C, Zheng X-T, Lin W, Cai M-L, Zhang Q-L, Peng C-L (2020) Different photoprotection strategies for mid- and late-successional dominant tree species in a high-light environment in summer. Environ Exp Bot 171:103927

    CAS  Google Scholar 

  • Ziska LH (1996) The potential sensitivity of tropical plants to increased ultraviolet-B radiation. J Plant Physiol 148:35–41

    CAS  Google Scholar 

  • 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

    Google Scholar 

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Acknowledgments

We thank Barbara Krause for competent assistance in preparation of the manuscript, Shizue Matsubara for critical reading of the text, and Aurelio Virgo for preparing the illustrations.

The research was supported by the Deutsche Forschungsgemeinschaft (GHK), the Andrew W. Mellon Foundation (KW), and the Smithsonian Tropical Research Institute (KW).

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Krause, G.H., Winter, K. (2020). The Photosynthetic System in Tropical Plants Under High Irradiance and Temperature Stress. In: Cánovas, F.M., Lüttge, U., Risueño, MC., Pretzsch, H. (eds) Progress in Botany Vol. 82. Progress in Botany, vol 82. Springer, Cham. https://doi.org/10.1007/124_2020_44

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