Temperature responses of photosynthesis and respiration in a sub-Antarctic megaherb from Heard Island
Marcus Schortemeyer A C , John R. Evans A , Dan Bruhn A D , Dana M. Bergstrom B and Marilyn C. Ball A EA Plant Science Division, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
B Australian Antarctic Division, Department of the Environment, 203 Channel Highway, Kingston, Tas. 7050, Australia.
C Present address: Plant Biosecurity, Department of Agriculture, 7 London Circuit, Canberra, ACT 2601, Australia.
D Present address: Centre for Earth, Planetary, Space and Astronomical Research, The Open University, Milton Keynes MK76AA, UK.
E Corresponding author. Email: marilyn.ball@anu.edu.au
Functional Plant Biology 42(6) 552-564 https://doi.org/10.1071/FP14134
Submitted: 5 May 2014 Accepted: 12 February 2015 Published: 17 April 2015
Abstract
Understanding the response of sub-Antarctic plants to a warming climate requires an understanding of the relationship of carbon gain and loss to temperature. In a field study on Heard Island, we investigated the responses of photosynthesis and respiration of the sub-Antarctic megaherb Pringlea antiscorbutica R. Br. to temperature. This was done by instantaneously manipulating leaf temperature in a gas exchange cuvette on plants adapted to natural temperature variation along an altitudinal gradient. There was little altitudinal variation in the temperature response of photosynthesis. Photosynthesis was much less responsive to temperature than electron transport, suggesting that Rubisco activity was generally the rate-limiting process. The temperature response of leaf respiration rates was greater in cold-grown (high altitude) plants compared with warm-grown (low altitude) plants. This thermal acclimation would enable plants to maintain a positive carbon budget over a greater temperature range.
Additional keywords: acclimation, climate change, Kerguelen cabbage, Pringlea antiscorbutica, nitrogen, warming.
References
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.| Thermal acclimation and the dynamic response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1CjtLk%3D&md5=9f883caac5f5f6b40fa19682d0f826a1CAS | 12878019PubMed |
Aubert S, Assard N, Boutin JP, Frenot Y, Dorne AJ (1999) Carbon metabolism in the sub-Antarctic Kerguelen cabbage Pringlea antiscorbutica R.Br.: environmental controls over carbohydrates and proline contents and relation to phenology. Plant, Cell & Environment 22, 243–254.
| Carbon metabolism in the sub-Antarctic Kerguelen cabbage Pringlea antiscorbutica R.Br.: environmental controls over carbohydrates and proline contents and relation to phenology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Wrurk%3D&md5=93228152b89078defdb77dcb2789a4a3CAS |
Badger MR, Collatz GJ (1977) Studies on the kinetic mechanism of ribulose-1,5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Institute of Washington Year Book 76, 355–361.
Bartish IV, Aïnouche A, Jia D, Bergstrom D, Chown SL, Winkworth RC, Hennion F (2012) Phylogeny and colonization history of Pringlea antiscorbutica (Brassicaceae), an emblematic endemic from the South Indian Ocean Province. Molecular Phylogenetics and Evolution 65, 748–756.
| Phylogeny and colonization history of Pringlea antiscorbutica (Brassicaceae), an emblematic endemic from the South Indian Ocean Province.Crossref | GoogleScholarGoogle Scholar | 22871399PubMed |
Bate GC, Smith VR (1983) Photosynthesis and respiration in the sub-Antarctic tussock grass Poa cookii. New Phytologist 95, 533–543.
| Photosynthesis and respiration in the sub-Antarctic tussock grass Poa cookii.Crossref | GoogleScholarGoogle Scholar |
Bergstrom DM, Chown SL (1999) Life at the front: history, ecology and change on Southern Ocean islands. Trends in Ecology & Evolution 14, 472–477.
| Life at the front: history, ecology and change on Southern Ocean islands.Crossref | GoogleScholarGoogle Scholar |
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24, 253–259.
| Improved temperature response functions for models of Rubisco-limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFGrt7k%3D&md5=a77db99a8d8f6d75b163db60d871247aCAS |
Bernacchi CJ, Pimentel C, Long SP (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant, Cell & Environment 26, 1419–1430.
| In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFyru7o%3D&md5=69c4d76494e42bdd235db63eef3343a0CAS |
Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406.
| Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlyrsLc%3D&md5=87ef81a2b975d3d5159f4be09ccd969bCAS | 24241146PubMed |
Bruhn D, Egerton JJG, Loveys BR, Ball MC (2007) Evergreen leaf respiration acclimates to long-term nocturnal warming under field conditions. Global Change Biology 13, 1216–1223.
| Evergreen leaf respiration acclimates to long-term nocturnal warming under field conditions.Crossref | GoogleScholarGoogle Scholar |
Bruhn D, Schortemeyer M, Edwards EJ, Egerton JJG, Hocart C, Evans JR, Ball MC (2008) The apparent temperature response of leaf respiration depends on the time-scale of measurements: a study of two cold-climate species. Plant Biology 10, 185–193.
| The apparent temperature response of leaf respiration depends on the time-scale of measurements: a study of two cold-climate species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslWqsrY%3D&md5=9d7737b295e6f456f31e1fcfcdffcd9eCAS | 18304192PubMed |
Cabrera HM, Rada F, Cavieres L (1998) Effects of temperature on photosynthesis of two morphologically contrasting plant species along an altitudinal gradient in the tropical high Andes. Oecologia 114, 145–152.
| Effects of temperature on photosynthesis of two morphologically contrasting plant species along an altitudinal gradient in the tropical high Andes.Crossref | GoogleScholarGoogle Scholar |
Chown SL, Gremmen NJM, Gaston KJ (1998) Ecological biogeography of Southern Ocean islands: species-area relationships, human impacts, and conservation. American Naturalist 152, 562–575.
| Ecological biogeography of Southern Ocean islands: species-area relationships, human impacts, and conservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnit1yntg%3D%3D&md5=0e6570e5167fe9fe1f1133b83247fb34CAS | 18811364PubMed |
De Pury DGG, Farquhar GD (1997) Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant, Cell & Environment 20, 537–557.
| Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models.Crossref | GoogleScholarGoogle Scholar |
Ehleringer J, Björkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants. Dependence on temperature, CO2, and O2 concentration. Plant Physiology 59, 86–90.
| Quantum yields for CO2 uptake in C3 and C4 plants. Dependence on temperature, CO2, and O2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhtFOktLc%3D&md5=b49eb3128c6c20e14ac997f4fbcceda1CAS | 16659794PubMed |
Ehleringer J, Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiology 73, 555–559.
| Variation in quantum yield for CO2 uptake among C3 and C4 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVKnsg%3D%3D&md5=33e3351a9454f736bacedeab82d4e7bfCAS | 16663257PubMed |
Erskine PD, Bergstrom DM, Schmidt S, Stewart GR, Tweedie CE, Shaw JD (1998) Subantarctic Macquarie Island – a model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance. Oecologia 117, 187–193.
| Subantarctic Macquarie Island – a model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance.Crossref | GoogleScholarGoogle Scholar |
Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
| On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisFKru7Y%3D&md5=82b58a4e67f359be9ddb6cc51bff01d4CAS |
Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of SLA and nitrogen partitioning in maximising carbon gain. Plant, Cell & Environment 24, 755–767.
| Photosynthetic acclimation of plants to growth irradiance: the relative importance of SLA and nitrogen partitioning in maximising carbon gain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsFCmurk%3D&md5=5f104a739012cb94f02efdff16f8525dCAS |
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=580ad8465ff46edd49bd8f41674c5486CAS | 24306196PubMed |
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
| The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=37e580c0b295f017ee0982c6a1b18ceaCAS |
Gunderson CA, Norby RJ, Wullschleger SD (2000) Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiology 20, 87–96.
| Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence.Crossref | GoogleScholarGoogle Scholar | 12651476PubMed |
Hennion F, Bouchereau A (1998) Accumulation of organic and inorganic solutes in the subantarctic cruciferous species Pringlea antiscorbutica in response to saline and cold stresses. Polar Biology 20, 281–291.
| Accumulation of organic and inorganic solutes in the subantarctic cruciferous species Pringlea antiscorbutica in response to saline and cold stresses.Crossref | GoogleScholarGoogle Scholar |
Hennion F, Frenot Y, Martin-Tanguy J (2006) High flexibility in growth and polyamine composition of the crucifer Pringlea antiscorbutica in relation to environmental conditions. Physiologia Plantarum 127, 212–224.
| High flexibility in growth and polyamine composition of the crucifer Pringlea antiscorbutica in relation to environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtFSku7Y%3D&md5=ea4840404c574a5e30ae73add6a53775CAS |
Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. Journal of Experimental Botany 57, 291–302.
| Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKntw%3D%3D&md5=e32d58aaeb90eafea0ca235592a1de5fCAS | 16364948PubMed |
June T, Evans JR, Farquhar GD (2004) A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. Functional Plant Biology 31, 275–283.
| A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1ejurs%3D&md5=69d74c04e4531bc5d74a0dc0df5d5aafCAS |
Körner C (2007) The use of ‘altitude’ in ecological research. Trends in Ecology & Evolution 22, 569–574.
| The use of ‘altitude’ in ecological research.Crossref | GoogleScholarGoogle Scholar |
Körner C, Diemer M (1987) In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Functional Ecology 1, 179–194.
| In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude.Crossref | GoogleScholarGoogle Scholar |
Körner C, Neumayer M, Peláez Menendez-Riedl S, Smets-Scheel A (1989) Functional morphology of mountain plants. Flora 182, 353–383.
Larigauderie A, Körner C (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Annals of Botany 76, 245–252.
| Acclimation of leaf dark respiration to temperature in alpine and lowland plant species.Crossref | GoogleScholarGoogle Scholar |
Leuning R (2002) Temperature dependence of two parameters in a photosynthesis model. Plant, Cell & Environment 25, 1205–1210.
| Temperature dependence of two parameters in a photosynthesis model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWitLg%3D&md5=5dd76b3333d7f8aeb4af08de63ad68f2CAS |
Medek DE, Ball MC, Schortemeyer M (2007) The relative contributions of leaf area ratio and net assimilation rate to change in growth rate depend on growth temperature: comparative analysis of subantarctic and alpine grasses. New Phytologist 175, 290–300.
| The relative contributions of leaf area ratio and net assimilation rate to change in growth rate depend on growth temperature: comparative analysis of subantarctic and alpine grasses.Crossref | GoogleScholarGoogle Scholar | 17587377PubMed |
Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A, Wang K, Loustau D (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25, 1167–1179.
| Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWitL0%3D&md5=7ceaf02ceff7664ed7b835b39f8e82e6CAS |
Ögren E, Evans JR (1993) Photosynthetic light-response curves. I. The influence of CO2 partial pressure and leaf inversion. Planta 189, 182–190.
| Photosynthetic light-response curves. I. The influence of CO2 partial pressure and leaf inversion.Crossref | GoogleScholarGoogle Scholar |
Pammenter NW, Drennan PA, Smith VR (1986) Physiological and anatomical aspects of photosynthesis of two Agrostis species at a sub-Antarctic island. New Phytologist 102, 143–160.
| Physiological and anatomical aspects of photosynthesis of two Agrostis species at a sub-Antarctic island.Crossref | GoogleScholarGoogle Scholar |
Richard Y, Rouault M, Pohl B, Crétat J, Duclot I, Taboulot S, Reason CJC, Macron C, Buiron D (2013) Temperature changes in the mid- and high-latitudes of the Southern Hemisphere. International Journal of Climatology 33, 1948–1963.
| Temperature changes in the mid- and high-latitudes of the Southern Hemisphere.Crossref | GoogleScholarGoogle Scholar |
Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. Journal of Experimental Botany 53, 609–620.
| Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCksrk%3D&md5=c0e3e1b8a8d20cb0f21d1cbcb0048423CAS | 11886880PubMed |
Scott JJ, Bergstrom DM (2006) Vegetation of Heard and McDonald Islands. In ‘Heard Island: Southern Ocean sentinel’. (Eds K Green, E Woehler) pp. 69–90. (Surrey Beatty and Sons: Sydney)
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
| Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=82578db68694d79cb87c996f505523e8CAS |
Slayter RO (1977) Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. IV. Temperature response of four populations grown at different temperatures. Australian Journal of Plant Physiology 4, 583–594.
| Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. IV. Temperature response of four populations grown at different temperatures.Crossref | GoogleScholarGoogle Scholar |
Slayter RO, Morrow PA (1977) Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. I. Seasonal changes under field conditions in the Snowy Mountains area of south-eastern Australia. Australian Journal of Botany 25, 1–20.
| Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. I. Seasonal changes under field conditions in the Snowy Mountains area of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Thost DE, Allison I (2006) The climate of Heard Island. In ‘Heard Island: Southern Ocean sentinel’. (Eds K Green, E Woehler) pp. 52–68. (Surrey Beatty and Sons: Sydney)
Thost DE, Truffer M (2008) Glacier recession on Heard Island, southern Indian Ocean. Arctic, Antarctic, and Alpine Research 40, 199–214.
| Glacier recession on Heard Island, southern Indian Ocean.Crossref | GoogleScholarGoogle Scholar |
Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adapative phenotypic plasticity – consensus and controversy. Trends in Ecology & Evolution 10, 212–217.
| Adapative phenotypic plasticity – consensus and controversy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFagtQ%3D%3D&md5=56e05de8314530ab81878ae78625c2aeCAS |
Vitasse Y, Lenz A, Kollas C, Randin CF, Hoch G, Körner C (2014) Genetic vs. non-genetic responses of leaf morphology and growth to elevation in temperate tree species. Functional Ecology 28,
| Genetic vs. non-genetic responses of leaf morphology and growth to elevation in temperate tree species.Crossref | GoogleScholarGoogle Scholar |
von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtFyjug%3D%3D&md5=46ca7684cc0e730de59cadefbd3f6508CAS | 24276943PubMed |
von Caemmerer S, Evans JR, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195, 88–97.
| The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1yjt7g%3D&md5=795a60c85ae726b4579be1e712e822deCAS |
Wang KY, Kellomäki S, Laitinen K (1996) Acclimation of photosynthetic paramaters in Scots pine after three years exposure to elevated temperature and CO2. Agricultural and Forest Meteorology 82, 195–217.
| Acclimation of photosynthetic paramaters in Scots pine after three years exposure to elevated temperature and CO2.Crossref | GoogleScholarGoogle Scholar |
Woodward FI (1983) The significance of interspecific differences in specific leaf area to the growth of selected herbaceous species from different altitudes. New Phytologist 95, 313–323.
| The significance of interspecific differences in specific leaf area to the growth of selected herbaceous species from different altitudes.Crossref | GoogleScholarGoogle Scholar |
Xiong FS, Mueller EC, Day TA (2000) Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. American Journal of Botany 87, 700–710.
| Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1Kmug%3D%3D&md5=652724c8083f9bcb48d8a1db60bc61c7CAS | 10811794PubMed |
Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant, Cell & Environment 29, 1659–1670.
| Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlSmur4%3D&md5=e51721e1be9c57ce9481ec22bfeda5d2CAS |
Zha TS, Kellomäki S, Wang KY (2003) Seasonal variation in respiration of 1-year-old shoots of Scots pine exposed to elevated carbon dioxide and temperature for 4 years. Annals of Botany 92, 89–96.
| Seasonal variation in respiration of 1-year-old shoots of Scots pine exposed to elevated carbon dioxide and temperature for 4 years.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3psFynsg%3D%3D&md5=7456f809c38f8bba0d79b33839dc910cCAS | 12763759PubMed |
Ziska LH (2001) Growth temperature can alter the temperature dependent stimulation of photosynthesis by elevated carbon dioxide in Abutilon theophrasti. Physiologia Plantarum 111, 322–328.
| Growth temperature can alter the temperature dependent stimulation of photosynthesis by elevated carbon dioxide in Abutilon theophrasti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFWjsb4%3D&md5=300e3175057749af1e115bf6880be3e9CAS | 11240916PubMed |