Responses of leaf respiration to heatwaves.
heat stress
high temperature
leaf respiration
mitochondria
thermal acclimation
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
21
01
2021
received:
21
12
2020
accepted:
23
01
2021
pubmed:
4
2
2021
medline:
15
12
2021
entrez:
3
2
2021
Statut:
ppublish
Résumé
Mitochondrial respiration (R) is central to plant physiology and responds dynamically to daily short-term temperature changes. In the longer-term, changes in energy demand and membrane fluidity can decrease leaf R at a common temperature and increase the temperature at which leaf R peaks (T
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2090-2101Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Alexander, L. V., Zhang, X., Peterson, T. C., Caesar, J., Gleason, B., Klein Tank, A. M. G., … Vazquez-Aguirre, J. L. (2006). Global observed changes in daily climate extremes of temperature and precipitation. Journal of Geophysical Research-Atmospheres, 111(D5), D05109.
Allakhverdiev, S., Kreslavski, V., Klimov, V., Los, D., Carpentier, R., & Mohanty, P. (2008). Heat stress: An overview of molecular responses in photosynthesis. Photosynthesis Research, 98(1), 541-550.
Almeselmani, M., Deshmukh, P. S., Sairam, R. K., Kushwaha, S. R., & Singh, T. P. (2006). Protective role of antioxidant enzymes under high temperature stress. Plant Science, 171(3), 382-388.
Amthor, J. S. (2000). The McCree-de wit-penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany, 86(1), 1-20.
Anderegg, W. R. L., Ballantyne, A. P., Smith, W. K., Majkut, J., Rabin, S., Beaulieu, C., … Pacala, S. W. (2015). Tropical nighttime warming as a dominant driver of variability in the terrestrial carbon sink. Proceedings of the National Academy of Sciences, 112(51), 15591-15596.
Araújo, W. L., Tohge, T., Ishizaki, K., Leaver, C. J., & Fernie, A. R. (2011). Protein degradation - An alternative respiratory substrate for stressed plants. Trends in Plant Science, 16(9), 489-498.
Arthur, H., & Watson, K. (1976). Thermal adaptation in yeast: Growth temperatures, membrane lipid, and cytochrome composition of psychrophilic, mesophilic, and thermophilic yeasts. Journal of Bacteriology, 128, 56-68.
Atkin, O. K., Evans, J. R., Ball, M. C., Lambers, H., & Pons, T. L. (2000). Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiology, 122(3), 915-923.
Atkin, O. K., & Macherel, D. (2009). The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany, 103(4), 581-597.
Atkin, O. K., Millar, A. H., Gardeström, P., & Day, D. A. (2000). Photosynthesis, carbohydrate metabolism and respiration in leaves of higher plants. In R. C. Leegood, T. D. Sharkey, & S. von Caemmerer (Eds.), Photosynthesis. Advances in photosynthesis and respiration (Vol. 9, pp. 153-175). Dordrecht, the Netherlands: Springer.
Atkin, O. K., Scheurwater, I., & Pons, T. L. (2006). High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Global Change Biology, 12(3), 500-515.
Atkin, O. K., & Tjoelker, M. G. (2003). Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science, 8(7), 343-351.
Banzet, N., Richaud, C., Deveaux, Y., Kazmaier, M., Gagnon, J., & Triantaphylidès, C. (1998). Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. The Plant Journal, 13(4), 519-527.
Berry, J., & Björkman, O. (1980). Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31(1), 491-543.
Blonder, B., & Michaletz, S. T. (2018). A model for leaf temperature decoupling from air temperature. Agricultural and Forest Meteorology, 262, 354-360.
Borovik, O. A., & Grabelnych, O. I. (2018). Mitochondrial alternative cyanide-resistant oxidase is involved in an increase of heat stress tolerance in spring wheat. Journal of Plant Physiology, 231, 310-317.
Bouma, T. J., De Visser, R., Van Leeuwen, P. H., De Kock, M. J., & Lambers, H. (1995). The respiratory energy requirements involved in nocturnal carbohydrate export from starch-storing mature source leaves and their contribution to leaf dark respiration. Journal of Experimental Botany, 46(9), 1185-1194.
Brookes, P. S. (2005). Mitochondrial H+ leak and ROS generation: An odd couple. Free Radical Biology and Medicine, 38(1), 12-23.
Buchert, F., Schober, Y., Römpp, A., Richter, M. L., & Forreiter, C. (2012). Reactive oxygen species affect ATP hydrolysis by targeting a highly conserved amino acid cluster in the thylakoid ATP synthase γ subunit. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1817(11), 2038-2048.
Bunce, J. A. (2005). Response of respiration of soybean leaves grown at ambient and elevated carbon dioxide concentrations to day-to-day variation in light and temperature under field conditions. Annals of Botany, 95(6), 1059-1066.
Busch, F. A., & Sage, R. F. (2017). The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytologist, 213(3), 1036-1051.
Davidson, J. F., & Schiestl, R. H. (2001). Mitochondrial respiratory electron carriers are involved in oxidative stress during heat stress in Saccharomyces cerevisiae. Molecular and Cellular Biology, 21(24), 8483-8489.
Davidson, R. L. (1969). Effect of root/leaf temperature differentials on root/shoot ratios in some pasture grasses and clover. Annals of Botany, 33(3), 561-569.
De Vries, F. W. T. P., Brunsting, A. H. M., & Van Laar, H. H. (1974). Products, requirements and efficiency of biosynthesis a quantitative approach. Journal of Theoretical Biology, 45(2), 339-377.
Degen, G. E., Orr, D. J., & Carmo-Silva, E. (2020). Heat-induced changes in the abundance of wheat Rubisco activase isoforms. New Phytologist, 229(3), 1298-1311.
Del-Saz, N. F., Ribas-Carbo, M., McDonald, A. E., Lambers, H., Fernie, A. R., & Florez-Sarasa, I. (2018). An in vivo perspective of the role(s) of the alternative oxidase pathway. Trends in Plant Science, 23(3), 206-219.
Downs, C. A., & Heckathorn, S. A. (1998). The mitochondrial small heat-shock protein protects NADH:Ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Letters, 430(3), 246-250.
Drake, J. E., Tjoelker, M. G., Vårhammar, A., Medlyn, B. E., Reich, P. B., Leigh, A., … Barton, C. V. M. (2018). Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance. Global Change Biology, 24(6), 2390-2402.
Dry, I. B., Bryce, J. H., Wiskich, J. T., & Davies, D. D. (1987). Regulation of mitochondrial respiration. In P. K. Stumpf & E. E. Conn (Eds.), The biochemistry of plants (pp. 213-252). San Diego, CA: Academic Press.
Eamus, D., Taylor, D. T., Macinnis-Ng, C. M. O., Shanahan, S., & De Silva, L. (2008). Comparing model predictions and experimental data for the response of stomatal conductance and guard cell turgor to manipulations of cuticular conductance, leaf-to-air vapour pressure difference and temperature: Feedback mechanisms are able to account for all observations. Plant, Cell & Environment, 31(3), 269-277.
Edwards, J. M., Roberts, T. H., & Atwell, B. J. (2012). Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. Journal of Experimental Botany, 63(12), 4389-4402.
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases. I. Occurrence in higher plants. Plant Physiology, 59(2), 309-314.
Grossiord, C., Buckley, T. N., Cernusak, L. A., Novick, K. A., Poulter, B., Siegwolf, R. T. W., … McDowell, N. G. (2020). Plant responses to rising vapor pressure deficit. New Phytologist, 226(6), 1550-1566.
Hartl, F. U. (1996). Molecular chaperones in cellular protein folding. Nature, 381(6583), 571-580.
Hazel, J. R. (1995). Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annual Review of Physiology, 57(1), 19-42.
Heskel, M. A., O'Sullivan, O. S., Reich, P. B., Tjoelker, M. G., Weerasinghe, L. K., Penillard, A., … Atkin, O. K. (2016). Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proceedings of the National Academy of Sciences of the United States of America, 113(14), 3832-3837.
Hüve, K., Bichele, I., Ivanova, H., Keerberg, O., Pärnik, T., Rasulov, B., … Niinemets, Ü. (2012). Temperature responses of dark respiration in relation to leaf sugar concentration. Physiologia Plantarum, 144(4), 320-334.
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(1), 113-126.
Impa, S. M., Sunoj, V. S. J., Krassovskaya, I., Bheemanahalli, R., Obata, T., & Jagadish, S. V. K. (2019). Carbon balance and source-sink metabolic changes in winter wheat exposed to high night-time temperature. Plant, Cell & Environment, 42(4), 1233-1246.
Ishihara, H., Moraes, T. A., Pyl, E.-T., Schulze, W. X., Obata, T., Scheffel, A., … Stitt, M. (2017). Growth rate correlates negatively with protein turnover in Arabidopsis accessions. The Plant Journal, 91(3), 416-429.
Jaindl, M., & Popp, M. (2006). Cyclitols protect glutamine synthetase and malate dehydrogenase against heat induced deactivation and thermal denaturation. Biochemical and Biophysical Research Communications, 345(2), 761-765.
Julius, B. T., Leach, K. A., Tran, T. M., Mertz, R. A., & Braun, D. M. (2017). Sugar transporters in plants: New insights and discoveries. Plant and Cell Physiology, 58(9), 1442-1460.
Kaushal, N., Awasthi, R., Gupta, K., Gaur, P., Siddique, K. H. M., & Nayyar, H. (2013). Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Functional Plant Biology, 40(12), 1334-1349.
Krömer, S. (1995). Respiration during photosynthesis. Annual Review of Plant Biology, 46(1), 45-70.
Lambers, H., & Ribas-Carbo, M. (2005). Plant respiration: From cell to ecosystem. Dordrecht, the Netherlands: Springer.
Larkindale, J., & Huang, B. (2004). Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environmental and Experimental Botany, 51(1), 57-67.
Law, R. D., & Crafts-Brandner, S. J. (1999). Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology, 120(1), 173-182.
Li, L., Nelson, C. J., Trosch, J., Castleden, I., Huang, S., & Millar, A. H. (2017). Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell, 29(2), 207-228.
Lin, T.-Y., & Markhart, A. H. (1990). Temperature effects on mitochondrial respiration in Phaseolus acutifolius a. gray and Phaseolus vulgaris L. Plant Physiology, 94(1), 54-58.
Los, D. A., & Murata, N. (2004). Membrane fluidity and its roles in the perception of environmental signals. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1666(1), 142-157.
Lund, A. A., Rhoads, D. M., Lund, A. L., Cerny, R. L., & Elthon, T. E. (2001). In vivo modifications of the maize mitochondrial small heat stress protein, HSP22. Journal of Biological Chemistry, 276(32), 29924-29929.
McLaughlin, B. C., Xu, C.-Y., Rastetter, E. B., & Griffin, K. L. (2014). Predicting ecosystem carbon balance in a warming Arctic: The importance of long-term thermal acclimation potential and inhibitory effects of light on respiration. Global Change Biology, 20(6), 1901-1912.
Millar, A. H., Whelan, J., Soole, K. L., & Day, D. A. (2011). Organization and regulation of mitochondrial respiration in plants. Annual Review of Plant Biology, 62, 79-104.
Millenaar, F. F., & Lambers, H. (2003). The alternative oxidase: In vivo regulation and function. Plant Biology, 5(1), 2-15.
Møller, I. M. (2001). Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology, 52(1), 561-591.
Morita, S., & Nakano, H. (2011). Nonstructural carbohydrate content in the stem at full heading contributes to high performance of ripening in heat-tolerant rice cultivar Nikomaru. Crop Science, 51(2), 818-828.
Murakami, Y., & Toriyama, K. (2008). Enhanced high temperature tolerance in transgenic rice seedlings with elevated levels of alternative oxidase, OsAOX1a. Plant Biotechnology, 25(4), 361-364.
Niu, Y., & Xiang, Y. (2018). An overview of biomembrane functions in plant responses to high-temperature stress. Frontiers in Plant Science, 9, 915.
O'Leary, B. M., Asao, S., Millar, A. H., & Atkin, O. K. (2019). Core principles which explain variation in respiration across biological scales. New Phytologist, 222, 670-686.
O'Leary, B. M., Lee, C. P., Atkin, O. K., Cheng, R., Brown, T. B., & Millar, A. H. (2017). Variation in leaf respiration rates at night correlates with carbohydrate and amino acid supply. Plant Physiology, 174(4), 2261-2273.
O'Sullivan, O. S., Heskel, M. A., Reich, P. B., Tjoelker, M. G., Weerasinghe, L. K., Penillard, A., … Atkin, O. K. (2017). Thermal limits of leaf metabolism across biomes. Global Change Biology, 23(1), 209-223.
O'Sullivan, O. S., Weerasinghe, K. W. L. K., Evans, J. R., Egerton, J. J. G., Tjoelker, M. G., & Atkin, O. K. (2013). High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant, Cell & Environment, 36(7), 1268-1284.
Pan, R., Jones, A. D., & Hu, J. (2014). Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis. The Plant Cell, 26(1), 391-409.
Paradies, G., Ruggiero, F. M., Petrosillo, G., & Quagliariello, E. (1998). Peroxidative damage to cardiac mitochondria: Cytochrome oxidase and cardiolipin alterations. FEBS Letters, 424(3), 155-158.
Perkins-Kirkpatrick, S. E., & Lewis, S. C. (2020). Increasing trends in regional heatwaves. Nature Communications, 11(1), 3357.
Plaxton, W. C., & Podestá, F. E. (2006). The functional organization and control of plant respiration. Critical Reviews in Plant Sciences, 25(2), 159-198.
Poorter, H., Remkes, C., & Lambers, H. (1990). Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology, 94(2), 621-627.
Rashid, F. A. A., Crisp, P. A., Zhang, Y., Berkowitz, O., Pogson, B. J., Day, D. A., … Scafaro, A. P. (2020). Molecular and physiological responses during thermal acclimation of leaf photosynthesis and respiration in rice. Plant, Cell & Environment, 43(3), 594-610.
Rashid, F. A. A., Scafaro, A. P., Asao, S., Fenske, R., Dewar, R. C., Masle, J., … Atkin, O. K. (2020). Diel- and temperature-driven variation of leaf dark respiration rates and metabolite levels in rice. New Phytologist, 228(1), 56-69.
Rezende, E. L., Bozinovic, F., Szilágyi, A., & Santos, M. (2020). Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242-1245.
Rhoads, D. M., Umbach, A. L., Subbaiah, C. C., & Siedow, J. N. (2006). Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiology, 141(2), 357-366.
Rodríguez-Calcerrada, J., Rodrigues, A. M., Perdiguero, P., António, C., Atkin, O. K., Li, M., … Gil, L. (2018). A molecular approach to drought-induced reduction in leaf CO2 exchange in drought-resistant Quercus ilex. Physiologia Plantarum, 162(4), 394-408.
Sadok, W., & Jagadish, S. V. K. (2020). The hidden costs of nighttime warming on yields. Trends in Plant Science, 25(7), 644-651.
Sadok, W., Lopez, J. R., & Smith, K. P. (2020). Transpiration increases under high temperature stress: Potential mechanisms, trade-offs and prospects for crop resilience in a warming world. Plant, Cell & Environment, 2020, 1-15. https://doi.org/10.1111/pce.13970
Saha, B., Borovskii, G., & Panda, S. K. (2016). Alternative oxidase and plant stress tolerance. Plant Signaling & Behavior, 11(12), e1256530.
Salvucci, M. E., & Crafts-Brandner, S. J. (2004). Mechanism for deactivation of Rubisco under moderate heat stress. Physiologia Plantarum, 122(4), 513-519.
Santhanagopalan, I., Basha, E., Ballard, K. N., Bopp, N. E., & Vierling, E. (2015). Model chaperones: Small heat shock proteins from plants. In R. M. Tanguay & L. E. Hightower (Eds.), The big book on small heat shock proteins, heat shock proteins (Vol. 8, pp. 119-153). Switzerland: Springer International Publishing.
Senisterra, G. A., Soo Hong, B., Park, H.-W., & Vedadi, M. (2008). Application of high-throughput isothermal denaturation to assess protein stability and screen for ligands. Journal of Biomolecular Screening, 13(5), 337-342.
Shameer, S., Ratcliffe, R. G., & Sweetlove, L. J. (2019). Leaf energy balance requires mitochondrial respiration and export of chloroplast NADPH in the light. Plant Physiology, 180(4), 1947-1961.
Simon, J.-P. (1979). Differences in thermal properties of NAD malate dehydrogenase in genotypes of Lathyrus japonicus Willd (Leguminosae) from maritime and continental sites. Plant, Cell & Environment, 2(1), 23-33.
Simon, J. P., Potvin, C., & Blanchard, M. H. (1983). Thermal adaptation and acclimation of higher plants at the enzyme level: Kinetic properties of NAD malate dehydrogenase and glutamate oxaloacetate transaminase in two genotypes of Arabidopsis thaliana (Brassicaceae). Oecologia, 60, 143-148.
Slot, M., Zaragoza-Castells, J., & Atkin, O. K. (2008). Transient shade and drought have divergent impacts on the temperature sensetivity of dark respiration in leaves of Geum urbanum. Functional Plant Biology, 35(11), 1135-1146.
Smith, A. M., & Stitt, M. (2007). Coordination of carbon supply and plant growth. Plant, Cell & Environment, 30(9), 1126-1149.
Smith, N. G., & Dukes, J. S. (2018). Drivers of leaf carbon exchange capacity across biomes at the continental scale. Ecology, 99(7), 1610-1620.
Smith, N. G., Li, G., & Dukes, J. S. (2019). Short-term thermal acclimation of dark respiration is greater in non-photosynthetic than in photosynthetic tissues. AoB Plants, 11(6), plz064.
Somero, G. N. (1995). Proteins and temperature. Annual Review of Physiology, 57, 43-68.
Suzuki, N., Koussevitzky, S., Mittler, R. O. N., & Miller, G. A. D. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment, 35(2), 259-270.
Suzuki, N., & Mittler, R. (2006). Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiologia Plantarum, 126(1), 45-51.
Sweetlove, L. J., Heazlewood, J. L., Herald, V., Holtzapffel, R., Day, D. A., Leaver, C. J., & Millar, A. H. (2002). The impact of oxidative stress on Arabidopsis mitochondria. The Plant Journal, 32(6), 891-904.
Takahashi, S., & Badger, M. R. (2011). Photoprotection in plants: A new light on photosystem II damage. Trends in Plant Science, 16(1), 53-60.
Tcherkez, G., Gauthier, P., Buckley, T. N., Busch, F. A., Barbour, M. M., Bruhn, D., … Cornic, G. (2017). Leaf day respiration: Low CO2 flux but high significance for metabolism and carbon balance. New Phytologist, 216(4), 986-1001.
Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., McGuire, M. A., & Steppe, K. (2014). Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment, 38(9), 1699-1712.
Turnbull, M. H., Murthy, R., & Griffin, K. L. (2002). The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides. Plant, Cell & Environment, 25(12), 1729-1737.
Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. The Journal of Physiology, 552(2), 335-344.
Walker, B., Ariza, L. S., Kaines, S., Badger, M. R., & Cousins, A. B. (2013). Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: Comparisons to Nicotiana tabacum. Plant, Cell & Environment, 36(12), 2108-2119.
Wang, H., Atkin, O. K., Keenan, T. F., Smith, N. G., Wright, I. J., Bloomfield, K. J., … Prentice, I. C. (2020). Acclimation of leaf respiration consistent with optimal photosynthetic capacity. Global Change Biology, 26(4), 2573-2583.
Wang, W., Vinocur, B., Shoseyov, O., & Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science, 9(5), 244-252.
Wardlaw, I. F., Moncur, L., & Patrick, J. W. (1995). The response of wheat to high temperature following anthesis. II. Sucrose accumulation and metabolism by isolated kernels. Functional Plant Biology, 22(3), 399-407.
Way, D., & Yamori, W. (2014). Thermal acclimation of photosynthesis: On the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynthesis Research, 119, 89-100.
Way, D. A., Aspinwall, M. J., Drake, J. E., Crous, K. Y., Campany, C. E., Ghannoum, O., … Tjoelker, M. G. (2019). Responses of respiration in the light to warming in field-grown trees: A comparison of the thermal sensitivity of the Kok and Laisk methods. New Phytologist, 222(1), 132-143.
Wei, S.-S., Niu, W.-T., Zhai, X.-T., Liang, W.-Q., Xu, M., Fan, X., … Li, B. (2019). Arabidopsis mtHSC70-1 plays important roles in the establishment of COX-dependent respiration and redox homeostasis. Journal of Experimental Botany, 70(20), 5575-5590.
Yamori, W., Hikosaka, K., & Way, D. A. (2014). Temperature response of photosynthesis in C3, C4, and CAM plants: Temperature acclimation and temperature adaptation. Photosynthesis Research, 119(1-2), 101-117.
Yoshioka, M., Uchida, S., Mori, H., Komayama, K., Ohira, S., Morita, N., … Yamamoto, Y. (2006). Quality control of photosystem II: Cleavage of reaction center D1 protein in spinach thylakoids by ftsh protease under moderate heat stress. Journal of Biological Chemistry, 281(31), 21660-21669.
Zhu, L., Bloomfield, K. J., Hocart, C. H., Egerton, J. J. G., O'Sullivan, O. S., Penillard, A., … Atkin, O. K. (2018). Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. Plant, Cell & Environment, 41(6), 1251-1262.
Zhu, L. L., Bloomfield, K. J., Asao, S., Tjoelker, M. G., Egerton, J. J. G., Hayes, L., … Atkin, O. K. (2020). Acclimation of leaf respiration temperature responses across thermally contrasting biomes. New Phytologist, 229(3), 1312-1325.