Phosphorus deficiency alters scaling relationships between leaf gas exchange and associated traits in a wide range of contrasting Eucalyptus species
Nur H. A. Bahar A B , Paul P. G. Gauthier C D , Odhran S. O’Sullivan A , Thomas Brereton E F , John R. Evans A G and Owen K. Atkin A B H
+ Author Affiliations
- Author Affiliations
A Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
B ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
C Department of Geosciences, Princeton University, Princeton, NJ 08544, USA.
D Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA.
E Research School of Chemistry, Australian National University, Canberra, ACT 2601, Australia.
F Agriculture and Food, CSIRO, Canberra, ACT 2601, Australia.
G ARC Centre of Excellence for Translational Photosynthesis, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
H Corresponding author. Email: owen.atkin@anu.edu.au
Functional Plant Biology 45(8) 813-826 https://doi.org/10.1071/FP17134
Submitted: 4 May 2017 Accepted: 2 February 2018 Published: 16 March 2018
Abstract
Phosphorus (P) limitation is known to have substantial impacts on leaf metabolism. However, uncertainty remains around whether P deficiency alters scaling functions linking leaf metabolism to associated traits. We investigated the effect of P deficiency on leaf gas exchange and related leaf traits in 17 contrasting Eucalyptus species that exhibit inherent differences in leaf traits. Saplings were grown under controlled-environment conditions in a glasshouse, where they were subjected to minus and plus P treatments for 15 weeks. P deficiency decreased P concentrations and increased leaf mass per area (LMA) of newly-developed leaves. Rates of photosynthesis (A) and respiration (R) were also reduced in P-deficient plants compared with P-fertilised plants. By contrast, P deficiency had little effect on the temperature sensitivity of R. Irrespective of P treatment, on a log-log basis A and R scaled positively with increasing leaf nitrogen concentration [N] and negatively with increasing LMA. Although P deficiency had limited impact on A-R-LMA relationships, rates of CO2 exchange per unit N were consistently lower in P-deficient plants. Our results highlight the importance of P supply for leaf carbon metabolism and show how P deficiencies (i.e. when excluding confounding genotypic and environmental effects) can have a direct effect on commonly used leaf trait scaling relationships.
Additional keywords: eucalypt, leaf respiration, photosynthesis, scaling relationships.
References
Ali AA, Xu C, Rogers A, McDowell NG, Medlyn BE, Fisher RA, Wullschleger SD, Reich PB, Vrugt JA, Bauerle WL, Santiago LS, Wilson CJ (2015) Global-scale environmental control of plant photosynthetic capacity. Ecological Applications 25, 2349–2365.| Global-scale environmental control of plant photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar |
Asner GP, Martin RE, Tupayachi R, Anderson CB, Sinca F, Carranza-Jiménez L, Martinez P (2014) Amazonian functional diversity from forest canopy chemical assembly. Proceedings of the National Academy of Sciences of the United States of America 111, 5604–5609.
| Amazonian functional diversity from forest canopy chemical assembly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlyhs7w%3D&md5=2e188696c451ff11e1b2354de25c5664CAS |
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=cc1e8d9cb9846ec479600e5082b68ff1CAS |
Atkin OK, Turnbull MH, Zaragoza-Castells J, Fyllas NM, Lloyd J, Meir P, Griffin KL (2013) Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method. Plant and Soil 367, 163–182.
| Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVKitrs%3D&md5=bc29135e4476958fabc98283dfd0fe66CAS |
Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytologist 190, 1003–1018.
| Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature.Crossref | GoogleScholarGoogle Scholar |
Bahar NHA, Ishida FY, Weerasinghe LK, Guerrieri R, O’Sullivan OS, Bloomfield KJ, Asner GP, Martin RE, Lloyd J, Malhi Y, Phillips OL, Meir P, Salinas N, Cosio EG, Domingues TF, Quesada CA, Sinca F, Escudero Vega A, Zuloaga Ccorimanya PP, del Aguila-Pasquel J, Quispe Huaypar K, Cuba Torres I, Butrón Loayza R, Pelaez Tapia Y, Huaman Ovalle J, Long BM, Evans JR, Atkin OK (2017) Leaf-level photosynthetic capacity in lowland Amazonian and high-elevation Andean tropical moist forests of Peru. New Phytologist 214, 1002–1018.
| Leaf-level photosynthetic capacity in lowland Amazonian and high-elevation Andean tropical moist forests of Peru.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlvVegu7w%3D&md5=cae7406f05134e0f0fb877c260df7f11CAS |
Bloomfield KJ, Domingues TF, Saiz G, Bird MI, Crayn DM, Ford A, Metcalfe D, Farquhar GD, Lloyd J (2014a) Contrasting photosynthetic characteristics of forest vs savanna species (far North Queensland, Australia). Biogeosciences 11, 7331–7347.
| Contrasting photosynthetic characteristics of forest vs savanna species (far North Queensland, Australia).Crossref | GoogleScholarGoogle Scholar |
Bloomfield KJ, Farquhar GD, Lloyd J (2014b) Photosynthesis–nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: a controlled environment study. Functional Plant Biology 41, 820–832.
| Photosynthesis–nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: a controlled environment study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyntrzI&md5=78b03134c8286940b96ec334b1b11dc6CAS |
Bown HE, Watt MS, Mason EG, Clinton PW, Whitehead D (2009) The influence of nitrogen and phosphorus supply and genotype on mesophyll conductance limitations to photosynthesis in Pinus radiata. Tree Physiology 29, 1143–1151.
| The influence of nitrogen and phosphorus supply and genotype on mesophyll conductance limitations to photosynthesis in Pinus radiata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGrs7bO&md5=cdff96be20f0dbd053cdbc52debe9d49CAS |
Brooker MIH, Kleinig DA (2006) ‘Field guide to eucalypts. Vol. 1. South-eastern Australia.’ (Bloomings Books: Melbourne)
Brooks A, Woo KC, Wong SC (1988) Effects of phosphorus nutrition on the response of photosynthesis to CO2 and O2, activation of ribulose bisphosphate carboxylase and amounts of ribulose bisphosphate and 3-phosphoglycerate in spinach leaves. Photosynthesis Research 15, 133–141.
| Effects of phosphorus nutrition on the response of photosynthesis to CO2 and O2, activation of ribulose bisphosphate carboxylase and amounts of ribulose bisphosphate and 3-phosphoglycerate in spinach leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVersrs%3D&md5=ea86a3eda9cab10646127ba5e45ee825CAS |
Cernusak LA, Hutley LB, Beringer J, Holtum JAM, Turner BL (2011) Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia. Agricultural and Forest Meteorology 151, 1462–1470.
| Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Covey-Crump EM, Attwood RG, Atkin OK (2002) Regulation of root respiration in two species of Plantago that differ in relative growth rate: the effect of short- and longterm changes in temperature. Plant, Cell & Environment 25, 1501–1513.
| Regulation of root respiration in two species of Plantago that differ in relative growth rate: the effect of short- and longterm changes in temperature.Crossref | GoogleScholarGoogle Scholar |
Cox P (2001) ‘Description of the ‘TRIFFID’ dynamic global vegetation model.’ (Hadley Centre, Met Office: Bracknell, England)
Crous KY, O’Sullivan OS, Zaragoza-Castells J, Bloomfield KJ, Alves Negrini A, Meir P, Turnbull MH, Griffin KL, Atkin OK (2017) Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study. New Phytologist 215, 992–1008.
| Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtFChsLnE&md5=5faf9ce3c5906c6d2845b94f53649b39CAS |
De Kauwe MG, Lin Y-S, Wright IJ, Medlyn BE, Crous KY, Ellsworth DS, Maire V, Prentice IC, Atkin OK, Rogers A, Niinemets Ü, Serbin SP, Meir P, Uddling J, Togashi HF, Tarvainen L, Weerasinghe LK, Evans BJ, Ishida FY, Domingues TF (2016) A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytologist 210, 1130–1144.
| A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvF2ktL0%3D&md5=0f1151a5fe1f7764b8f70650eb2ca466CAS |
Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H, Diallo A, Grace J, Lloyd J (2010) Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33, 959–980.
| Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVagsbw%3D&md5=aa027b359919c93e775a824fe44d8fa4CAS |
Ellsworth DS, Crous KY, Lambers H, Cooke J (2015) Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species. Plant, Cell & Environment 38, 1142–1156.
| Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotVSmsL8%3D&md5=b3e7a305731cc30f5ba4d7e1b4c32c23CAS |
Ellsworth DS, Anderson IC, Crous KY, Cooke J, Drake JE, Gherlenda AN, Gimeno TE, Macdonald CA, Medlyn BE, Powell JR, Tjoelker MG, Reich PB (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nature Climate Change 7, 279–282.
| Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlslansrg%3D&md5=45b96cabcef8a25a211c9809e8570e56CAS |
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
| Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |
Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. Journal of Experimental Botany 60, 2235–2248.
| Resistances along the CO2 diffusion pathway inside leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitb4%3D&md5=3246066d742c43a9e5063ccf0fdf9bbfCAS |
Farquhar GD, 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=8d1285c7bfb2dfe7b8cf9b5cf09248dfCAS |
Field CB, Mooney HA (1986) The photosynthetic-nitrogen relationship in wild plants. In ‘On the economy of form and function’. (Ed. T Givnish) pp. 22–55. (Cambridge University Press: Cambridge, UK)
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
| Mesophyll conductance to CO2: current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFehtbc%3D&md5=4333c8c47b463cc022ddb4fb70f02ce1CAS |
Fyllas NM, Patino S, Baker TR, Bielefeld Nardoto G, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jim’enez EM, Luiz˜ao FJ, Neill A, Silva N, Prieto A, Rudas A, Silviera M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6, 2677–2708.
| Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate.Crossref | GoogleScholarGoogle Scholar |
Gonzalez-Meler MA, Giles L, Thomas RB, Siedow JN (2001) Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply. Plant, Cell & Environment 24, 205–215.
| Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFGrt70%3D&md5=5d87f7e0875942155b387c9fefffdb7eCAS |
Gonzàlez-Meler MA, Blanc-Betes E, Flower CE, Ward JK, Gomez-Casanovas N (2009) Plastic and adaptive responses of plant respiration to changes in atmospheric CO2 concentration. Physiologia Plantarum 137, 473–484.
| Plastic and adaptive responses of plant respiration to changes in atmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar |
Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
| N: P ratios in terrestrial plants: variation and functional significance.Crossref | GoogleScholarGoogle Scholar |
Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. Journal of Experimental Botany 60, 2303–2314.
| Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiurs%3D&md5=83a3326b49eb29252f29311292ea7753CAS |
Hedin LO (2004) Global organization of terrestrial plant–nutrient interactions. Proceedings of the National Academy of Sciences of the United States of America 101, 10849–10850.
| Global organization of terrestrial plant–nutrient interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVCmsL0%3D&md5=d0debd363a0ac83f734227b100917f52CAS |
Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta – Bioenergetics 1366, 235–255.
| Interdependence between chloroplasts and mitochondria in the light and the dark.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtlSit7g%3D&md5=39dd3ff3b647cdc87e71fc7148da0779CAS |
Hüve K, Bichele I, Rasulov B, Niinemets Ü (2011) When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant, Cell & Environment 34, 113–126.
| When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation.Crossref | GoogleScholarGoogle Scholar |
Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. Journal of Experimental Botany 42, 1003–1011.
| Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFGht7s%3D&md5=d534e099cf941c587cf4e69ad47c24a9CAS |
Jacob J, Lawlor DW (1993) Extreme phosphate deficiency decreases the in vivo CO2/O2 specificity factor of ribulose 1,5-bisphosphate carboxylase-oxygenase in intact leaves of sunflower. Journal of Experimental Botany 44, 1635–1641.
| Extreme phosphate deficiency decreases the in vivo CO2/O2 specificity factor of ribulose 1,5-bisphosphate carboxylase-oxygenase in intact leaves of sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltlOrtw%3D%3D&md5=98b76d9a6fb24abed7303018d302f15aCAS |
Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant, Cell & Environment 30, 1176–1190.
| Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrE&md5=24720358a441c1249aae9ab8ee7d8d5bCAS |
Kattge J, Knorr W, Raddatz T, Wirth C (2009) Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15, 976–991.
| Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models.Crossref | GoogleScholarGoogle Scholar |
Kirschbaum MUF, Tompkins D (1990) Photosynthetic responses to phosphorus-nutrition in Eucalyptus grandis seedlings. Australian Journal of Plant Physiology 17, 527–535.
| Photosynthetic responses to phosphorus-nutrition in Eucalyptus grandis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmtFSitQ%3D%3D&md5=9d862a13b9ef7fb96242571d53b49542CAS |
Kirschbaum M, Bellingham D, Cromer R (1992) Growth analysis of the effect of phosphorus nutrition on seedlings of Eucalyptus grandis. Functional Plant Biology 19, 55–66.
Krömer S (1995) Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46, 45–70.
| Respiration during photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution 23, 95–103.
| Plant nutrient-acquisition strategies change with soil age.Crossref | GoogleScholarGoogle Scholar |
Lewis JD, Phillips NG, Logan BA, Hricko CR, Tissue DT (2011) Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden. Tree Physiology 31, 997–1006.
| Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCls7jP&md5=62fbd04299d1c014ed80f92bd396f2bdCAS |
Loustau D, Ben Brahim M, Gaudillere JP, Dreyer E (1999) Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings. Tree Physiology 19, 707–715.
| Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings.Crossref | GoogleScholarGoogle Scholar |
Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A, Reich PB, Santiago LS (2015) Global effects of soil and climate on leaf photosynthetic traits and rates. Global Ecology and Biogeography 24, 706–717.
| Global effects of soil and climate on leaf photosynthetic traits and rates.Crossref | GoogleScholarGoogle Scholar |
Meir P, Grace J, Miranda AC (2001) Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature. Functional Ecology 15, 378–387.
| Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature.Crossref | GoogleScholarGoogle Scholar |
Meir P, Levy PE, Grace J, Jarvis PG (2007) Photosynthetic parameters from two contrasting woody vegetation types in West Africa. Plant Ecology 192, 277–287.
| Photosynthetic parameters from two contrasting woody vegetation types in West Africa.Crossref | GoogleScholarGoogle Scholar |
Mercado LM, Patiño S, Domingues TF, Fyllas NM, Weedon GP, Sitch S, Quesada CA, Phillips OL, Aragão LEOC, Malhi Y, Dolman AJ, Restrepo-Coupe N, Saleska SR, Baker TR, Almeida S, Higuchi N, Lloyd J (2011) Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 366, 3316–3329.
| Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply.Crossref | GoogleScholarGoogle Scholar |
Mooney HA, Ferrar PJ, Slatyer RO (1978) Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36, 103–111.
| Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznslOnsg%3D%3D&md5=166c0445e7d73172e94d3b6b0c666821CAS |
Musavi T, Migliavacca M, van de Weg MJ, Kattge J, Wohlfahrt G, van Bodegom PM, Reichstein M, Bahn M, Carrara A, Domingues TF, Gavazzi M, Gianelle D, Gimeno C, Granier A, Gruening C, Havránková K, Herbst M, Hrynkiw C, Kalhori A, Kaminski T, Klumpp K, Kolari P, Longdoz B, Minerbi S, Montagnani L, Moors E, Oechel WC, Reich PB, Rohatyn S, Rossi A, Rotenberg E, Varlagin A, Wilkinson M, Wirth C, Mahecha MD (2016) Potential and limitations of inferring ecosystem photosynthetic capacity from leaf functional traits. Ecology and Evolution 6, 7352–7366.
| Potential and limitations of inferring ecosystem photosynthetic capacity from leaf functional traits.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü, Wright IJ, Evans JR (2009) Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. Journal of Experimental Botany 60, 2433–2449.
| Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyiuro%3D&md5=c9681e57c33593d48dd89e80a2b3c34dCAS |
O’Sullivan OS, Weerasinghe KWLK, Evans JR, Egerton JJG, Tjoelker MG, Atkin OK (2013) High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant, Cell & Environment 36, 1268–1284.
| High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function.Crossref | GoogleScholarGoogle Scholar |
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Functional Ecology 18, 419–425.
| Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency.Crossref | GoogleScholarGoogle Scholar |
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytologist 214, 1447–1463.
| Physiological and structural tradeoffs underlying the leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXnt1Cgsrk%3D&md5=713aca05a4cbfc75df3449bc9be23bc8CAS |
Parsons HL, Yip JYH, Vanlerberge GC (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiology 121, 1309–1320.
| Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFyis74%3D&md5=ba5889b7d7159e1a0f0f09d67f4f0911CAS |
Plaxton WC, Podesta FE (2006) The functional organization and control of plant perspiration. Critical Reviews in Plant Sciences 25, 159–198.
| The functional organization and control of plant perspiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVKqtrs%3D&md5=e2524493098e7efde366d31ba639e551CAS |
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the United States of America 101, 11001–11006.
| Global patterns of plant leaf N and P in relation to temperature and latitude.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVCmt74%3D&md5=ed3d759edc1ddce48778c92b3acd738fCAS |
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the United States of America 94, 13730–13734.
| From tropics to tundra: global convergence in plant functioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXotValtb8%3D&md5=f0b7726c185315a73a465252e15f1f6cCAS |
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: A test across six biomes. Ecology 80, 1955–1969.
| Generality of leaf trait relationships: A test across six biomes.Crossref | GoogleScholarGoogle Scholar |
Reich P, Oleksyn J, Wright I (2009) Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207–212.
| Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species.Crossref | GoogleScholarGoogle Scholar |
Rowland L, Zaragoza-Castells J, Bloomfield KJ, Turnbull MH, Bonal D, Burban B, Salinas N, Cosio E, Metcalfe DJ, Ford A, Phillips OL, Atkin OK, Meir P (2017) Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents. New Phytologist 214, 1064–1077.
| Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlvVegu70%3D&md5=52eaaf316b24d4fcce3ea9b0f9b80c3cCAS |
Sands P, Cromer R, Kirschbaum M (1992) A model of nutrient response in Eucalyptus grandis seedlings. Functional Plant Biology 19, 459–470.
Sharwood RE, Crous KY, Whitney SM, Ellsworth DS, Ghannoum O (2017) Linking photosynthesis and leaf N allocation under future elevated CO2 and climate warming in Eucalyptus globulus. Journal of Experimental Botany 68, 1157–1167.
Singh SK, Badgujar G, Reddy VR, Fleisher DH, Bunce JA (2013) Carbon dioxide diffusion across stomata and mesophyll and photo-biochemical processes as affected by growth CO2 and phosphorus nutrition in cotton. Journal of Plant Physiology 170, 801–813.
| Carbon dioxide diffusion across stomata and mesophyll and photo-biochemical processes as affected by growth CO2 and phosphorus nutrition in cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFaht7c%3D&md5=174b115c06e7b56154dbc355f2e672c2CAS |
Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum. Plant Physiology 95, 1089–1095.
| Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVCjt7w%3D&md5=0bd0b58641f822b810e2109dbb45401eCAS |
Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N : P ratios in tropical rain forests. Ecology 88, 107–118.
| Controls over foliar N : P ratios in tropical rain forests.Crossref | GoogleScholarGoogle Scholar |
Turnbull MH, Tissue DT, Griffin KL, Richardson SJ, Peltzer DA, Whitehead D (2005) Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence. Oecologia 143, 271–279.
| Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence.Crossref | GoogleScholarGoogle Scholar |
Turnbull MH, Griffin KL, Fyllas NM, Lloyd J, Meir P, Atkin OK (2016) Separating species and environmental determinants of leaf functional traits in temperate rainforest plants along a soil-development chronosequence. Functional Plant Biology 43, 751–765.
| Separating species and environmental determinants of leaf functional traits in temperate rainforest plants along a soil-development chronosequence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1SitrjJ&md5=085bca7404f19d2de5260c46be129ba7CAS |
Turner NC, Schulze E-D, Nicolle D, Schumacher J, Kuhlmann I (2008) Annual rainfall does not directly determine the carbon isotope ratio of leaves of Eucalyptus species. Physiologia Plantarum 132, 440–445.
| Annual rainfall does not directly determine the carbon isotope ratio of leaves of Eucalyptus species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktLc%3D&md5=a2d97bb6962d90c245933ee8ca5c5b28CAS |
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=0f25d5d0b257be2607d07c323daefdeeCAS |
von Uexküll HR, Mutert E (1995) Global extent, development and economic-impact of acid soils. Plant and Soil 171, 1–15.
| Global extent, development and economic-impact of acid soils.Crossref | GoogleScholarGoogle Scholar |
Walker AP, Beckerman AP, Gu L, Kattge J, Cernusak LA, Domingues TF, Scales JC, Wohlfahrt G, Wullschleger SD, Woodward FI (2014) The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4, 3218–3235.
| The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study.Crossref | GoogleScholarGoogle Scholar |
Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305, 509–513.
| Ecosystem properties and forest decline in contrasting long-term chronosequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVOktbs%3D&md5=efc7537bcf3df66594f95244ba45db42CAS |
Warren CR (2011) How does P affect photosynthesis and metabolite profiles of Eucalyptus globulus? Tree Physiology 31, 727–739.
| How does P affect photosynthesis and metabolite profiles of Eucalyptus globulus? Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1GgtbbF&md5=f87d413580e61dedb701b986ff7eea90CAS |
Warren CR, Adams MA (2004) What determines rates of photosynthesis per unit nitrogen in Eucalyptus seedlings? Functional Plant Biology 31, 1169–1178.
| What determines rates of photosynthesis per unit nitrogen in Eucalyptus seedlings?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCqtbfJ&md5=6ab1f3fef7c76291f46840710a24522bCAS |
Warren CR, Adams MA, Chen Z (2000) Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Functional Plant Biology 27, 407–416.
| Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksF2rs7Y%3D&md5=4a6aa3e062d840aee88d731fa6c6822cCAS |
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biological Reviews of the Cambridge Philosophical Society 81, 259–291.
| Bivariate line-fitting methods for allometry.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Functional Ecology 15, 423–434.
| Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Groom PK, Lamont BB, Poot P, Prior LD, Reich PB, Schulze ED, Veneklaas EJ, Westoby M (2004a) Leaf trait relationships in Australian plant species. Functional Plant Biology 31, 551–558.
| Leaf trait relationships in Australian plant species.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004b) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=f752755637bf822e879e8c9d3c0bbf3cCAS |
