Skip to main content
SpringerLink
Log in

The temperature response of mesophyll conductance, and its component conductances, varies between species and genotypes

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The temperature response of mesophyll conductance to CO2 diffusion (gm) has been shown to vary considerably between species but remains poorly understood. Here, we tested the hypothesis that increases in chloroplast surface area with increasing temperature, due to the formation of chloroplast protrusions, caused observed positive responses of gm to temperature. We found no evidence of chloroplast protrusions. Using simultaneous measurements of carbon and oxygen isotope discrimination during photosynthesis to separate total gm (gm13) into cell wall and plasma membrane conductance (gm18) and chloroplast membrane conductance (gcm) components, we explored the temperature response in genotypes of soybean and barley, and sunflower plants grown at differing CO2 concentrations. Differences in the temperature sensitivity of gm18 were found between genotypes and between plants grown at differing CO2 concentration but did not relate to measured anatomical features such as chloroplast surface area or cell wall thickness. The closest fit of modelled gm13 to estimated values was found when cell wall thickness was allowed to decline at higher temperatures and transpiration rates, but it remains to be tested if this decline is realistic. The temperature response of gcm (calculated from the difference between 1/gm13 and 1/gm18) varied between barley genotypes, and was best fitted by an optimal response in sunflower. Taken together, these results indicate that gm is a highly complex trait with unpredictable sensitivity to temperature that varies between species, between genotypes within a single species, with growth environment, between replicate leaves, and even with age for an individual leaf.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Almeida-Rodriguez AM, Cooke JEK, Yeh F, Zwiazek JJ (2010) Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii × balsamifera clones with different drought resistance strategies. Physiol Plant 140:321–333

    Article  CAS  PubMed  Google Scholar 

  • Barbour MM, McDowell NG, Tcherkez G, Bickford CP, Hanson DT (2007a) A new measurement technique reveals rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2. Plant Cell Environ 30:469–482

    Article  CAS  PubMed  Google Scholar 

  • Barbour MM, Farquhar GD, Hanson DT, Bickford CP, Powers H, McDowell NG (2007b) A new measurement technique reveals temporal variation in ïδ18O of leaf-respired CO2. Plant Cell Environ 30:456–468

    Article  CAS  PubMed  Google Scholar 

  • Barbour MM, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant Cell Environ 33:1176–1185

    PubMed  Google Scholar 

  • Barbour MM, Evans JR, Simonin KA, von Caemmerer S (2016) Online CO2 and H2O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants. New Phytol 210:875–889

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernacchi CJ, Pimentel C, Long SP (2003) In vivo tmperature response functions of parameters required to model RuBP-limited photosynthesis. Plant Cell Environ 26:1419–1430

    Article  CAS  Google Scholar 

  • Boyd RA, Gandin A, Cousins AB (2015) Temperature responses of C4 photosynthesis: biochemical analysis of Rubisco, phosphoenolpyruvate carboxylase, and carbonic anhydrase in Setaria viridis. Plant Physiol 169:1850–1861

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brenninkmeijer C, Kraft P, Mook W (1983) Oxygen isotope fractionation between CO2 and H2O. Isotope Geosci 1:181–190

    CAS  Google Scholar 

  • Buchner O, Moser T, Karadar M, Roach T, Kranner I, Holzinger A (2015) Formation of chloroplast protrusions and catalase activity in alpine Ranunculus glacialis under elevated temperature and different CO2/O2 ratios. Protoplasma 252:1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canny M, Wong SC, Huang C, Miller C (2012) Differential shrinkage of mesophyll cells in transpiring cotton leaves: implications for static and dynamic pools of water, and for water transport pathways. Funct Plant Biol 39:91–102

    Article  CAS  Google Scholar 

  • Cernusak LA, Farquhar GD, Wong SC, Stuart-Williams H (2004) Measurement and interpretation of the oxygen isotope composition of carbon dioxide respired by leaves in the dark. Plant Physiol 136:3350–3363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craig H, Gordon LI (1965) Deuterium and oxygen-18 variations in the ocean and the marine atmosphere. In: E., T (ed.) Proceedings of a Conference on Stable Isotopes in Oceanographic Studies and Paleotemperatures. Laboratory of Geology and Nuclear Science, Pisa

  • Diaz-Espejo A, Nicolás E, Fernández JE (2007) Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell Environ 30:922–933

    Article  CAS  PubMed  Google Scholar 

  • Ellsworth PV, Ellsworth PZ, Koteyeva NK, Cousins AB (2018) Cell wall properties in Oryza sativa influence mesophyll CO2 conductance. New Phytol. https://doi.org/10.1111/nph.15173

    Article  PubMed  Google Scholar 

  • Evans JR, von Caemmerer S (2013) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ 36::745–756

    Article  CAS  Google Scholar 

  • Evans J, Sharkey T, Berry J, Farquhar G (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Funct Plant Biol 13:281–292

    Article  CAS  Google Scholar 

  • Evans JR, Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Funct Plant Biol 21:475–495

    Article  CAS  Google Scholar 

  • Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248

    Article  CAS  PubMed  Google Scholar 

  • Fabre N, Reiter IM, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30:617–629

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35:1221–1231

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. Stable isotopes and plant carbon-water relations. Elsevier, Amsterdam, pp 47–70

    Google Scholar 

  • Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552

    Article  CAS  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Flanagan LB, Comstock JP, Ehleringer JR (1991) Comparison of modeled and observed environmental influences on the stable oxygen and hydrogen isotope composition of leaf water in Phaseolus Vulgaris L. Plant Physiol 96:588–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flexas J, Diaz-Espejo A (2015) Interspecific differences in temperature response of mesophyll conductance: food for thought on its origin and regulation. Plant Cell Environ 38:625–628

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193::70–84

    Article  CAS  Google Scholar 

  • Gillon JS, Yakir D (2000) Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves. Plant Physiol 123:201–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu L, Sun Y (2014) Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant Cell Environ 37:1231–1249

    Article  CAS  PubMed  Google Scholar 

  • Guy RD, Fogel ML, Berry JA (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101:37–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harwood K, Gillon J, Griffiths H, Broadmeadow M (1998) Diurnal variation of ∆13CO2, ∆C18O16O and evaporative site enrichment of δH2 18O in Piper aduncum under field conditions in Trinidad. Plant Cell Environ 21:269–283

    Article  CAS  Google Scholar 

  • He Y, Yu C, Zhou L, Chen Y, Liu A, Jin J, Hong J, Qi Y, Jiang D (2014) Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max.) under salt stress. Plant Physiol Biochem 74:118–124

    Article  CAS  PubMed  Google Scholar 

  • Holzinger A, Buchner O, Lütz C, Hanson M (2007a) Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana. Protoplasma 230:23–30

    Article  CAS  PubMed  Google Scholar 

  • Holzinger A, Wasteneys G, Lütz C (2007b) Investigating cytoskeletal function in chloroplast protrusion formation in the arctic-alpine plant Oxyria digyna. Plant Biology 9:400–410

    Article  CAS  PubMed  Google Scholar 

  • Hulikova A, Swietach P (2014) Rapid CO2 permeation across biological membranes: implications for CO2 venting from tissue. FASEB J 28:2762–2774

    Article  CAS  PubMed  Google Scholar 

  • Jahan E, Amthor JS, Farquhar GD, Trethowan R, Barbour MM (2014) Variation in mesophyll conductance among Australian wheat genotypes. Funct Plant Biol 41:568–580

    Article  Google Scholar 

  • Jia W, Davies WJ (2007) Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced abscisic acid signals. Plant Physiol 143:68–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaldenhoff R (2012) Mechanisms underlying CO2 diffusion in leaves. Curr Opin Plant Biol 15::276–281

    Article  CAS  Google Scholar 

  • Kodama N, Cousins A, Tu KP, Barbour MM (2011) Spatial variation in photosynthetic CO2 carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum x Secale) relates to mesophyll conductance and the Peclet effect. Plant Cell Environ 34::1548–1562

    Article  CAS  Google Scholar 

  • Li Y, Ren B, Yang X, Xu G, Shen Q, Guo S (2012) Chloroplast downsizing under nitrate nutrition restrained mesophyll conductance and photosynthesis in rice (Oryza sativa L.) under drought conditions. Plant Cell Physiol 53:892–900

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Ren B, Ding L, Shen Q, Peng S, Guo S (2013) Does chloroplast size influence photosynthetic nitrogen use efficiency? PLoS ONE 8:e62036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loucos KE, Simonin KA, Song X, Barbour MM (2015) Observed relationships between leaf H218O Péclet effective length and leaf hydraulic conductance reflect assumptions in Craig-Gordon model calculations. Tree Physiol 35:16–26

    Article  CAS  PubMed  Google Scholar 

  • Loucos KE, Simonin KA, Barbour MM (2017) Leaf hydraulic conductance and mesophyll conductance are not closely related within a single species. Plant Cell Environ 40:203–215

    Article  CAS  PubMed  Google Scholar 

  • Lütz C (2010) Cell physiology of plants growing in cold environments. Protoplasma 244:53–73

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, Boursiac Y, Luu D-T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358

    Article  CAS  PubMed  Google Scholar 

  • Missner A, Kügler P, Saparov SM, Sommer K, Mathai JC, Zeidel ML, Pohl P (2008) Carbon dioxide transport through membranes. J Biol Chem 283:25340–25347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori IC, Rhee J, Shibasaka M, Sasano S, Kaneko T, Horie T, Katsuhara M (2014) CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol 55:251–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moser T, Holzinger A, Buchner O (2015) Chloroplast protrusions in leaves of Ranunculus glacialis L. respond significantly to different ambient conditions, but are not related to temperature stress. Plant Cell Environ 38::1347–1356

    Article  CAS  Google Scholar 

  • Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. J Exp Bot 60:2271–2282

    Article  CAS  PubMed  Google Scholar 

  • O’Leary MH (1984) Measurement of the isotope fractionation associated with diffusion of carbon dioxide in aqueous solution. J Phys Chem 88:823–825

    Article  Google Scholar 

  • Ogeé J, Wingate L, Genty B (2018) Estimating mesophyll conductance from measurements of C18OO photosynthetic discrimination and carbonic anhydrase activity. Plant Physiol 178:728–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pons TL, Welschen RA (2003) Midday depression of net photosynthesis in the tropical rainforest tree Eperua grandiflora: contributions of stomatal and internal conductances, respiration and Rubisco functioning. Tree Physiol 23:937–947

    Article  CAS  PubMed  Google Scholar 

  • Pons TL, Flexas J, Von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60:2217–2234

    Article  CAS  PubMed  Google Scholar 

  • Qiu C, Ethier G, Pepin S, Dubé P, Desjardins Y, Gosselin A (2017) Persistent negative temperature response of mesophyll conductance in red raspberry (Rubus idaeus L.) leaves under both high and low vapour pressure deficits: a role for abscisic acid? Plant Cell Environ 40:1940–1959

    Article  CAS  PubMed  Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2007) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    Article  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:035–1040

    Article  CAS  Google Scholar 

  • Simonin KA, Roddy AB, Link P, Apodaca R, Tu KP, Hu JIA, Dawson TE, Barbour MM (2013) Isotopic composition of transpiration and rates of change in leaf water isotopologue storage in response to environmental variables. Plant Cell Environ 36::2190–2206

    Article  CAS  Google Scholar 

  • Song X, Loucos KE, Simonin KA, Farquhar GD, Barbour MM (2015) Measurements of transpiration isotopologues and leaf water to assess enrichment models in cotton. New Phytol 206:637–646

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Gu L, Dickinson RE, Norby RJ, Pallardy SG, Hoffman FM (2014) Impact of mesophyll diffusion on estimated global land CO2 fertilization. PNAS 111:15774–15779

    Article  CAS  PubMed  Google Scholar 

  • Tazoe Y, von Caemmerer S, Badger MR, Evans JR (2009) Light and CO2 do not affect the mesophyll conductance to CO2 diffusion in wheat leaves. J Exp Bot 60:2291–2301

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Schaeufele R, Nogues S, Piel C, Boom A, Lanigan G, Barbaroux C, Mata C, Elhani S, Hemming D (2010) On the 13C/12C isotopic signal of day and night respiration at the mesocosm level. Plant Cell Environ 33::900–913

    Article  CAS  Google Scholar 

  • Terashima I, Ono K (2002) Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant Cell Physiol 43:70–78

    Article  CAS  PubMed  Google Scholar 

  • Thain JF (1983) Curvature correction factors in the measurement of cell surface areas in plant tissues. J Exp Bot 34:87–94

    Article  Google Scholar 

  • Tholen D, Boom C, Noguchi KO, Ueda S, Katase T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environ 31:1688–1700

    Article  CAS  PubMed  Google Scholar 

  • Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103

    Article  CAS  PubMed  Google Scholar 

  • Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Ribas-Carbó M, Tosens T, Vislap V, Niinemets Ü (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J Exp Bot 64:2269–2281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 63:5105–5119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ubierna N, Farquhar GD (2014) Addvances in measurements and models of photosynthetic carbon isotope discrimination in C3 plants. Plant Cell Environ 37:1494–1498

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38::629–637

    Article  CAS  Google Scholar 

  • Walker B, Ariza LS, Kaines S, Badger MR, Cousins AB (2013) Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ 36::2108–2119

    Article  CAS  Google Scholar 

  • Warren C (2008) Does growth temperature affect the temperature responses of photosynthesis and internal conductance to CO2? A test with Eucalyptus regnans. Tree Physiol 28::11–19

    Article  Google Scholar 

  • Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067

    Article  CAS  PubMed  Google Scholar 

  • Yamane K, Mitsuya S, Taniguchi M, Miyake H (2012) Salt-induced chloroplast protrusion is the process of exclusion of ribulose-1, 5-bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm in leaves of rice. Plant Cell Environ 35:1663–1671

    Article  CAS  PubMed  Google Scholar 

  • Yamori W, Noguchi K, Hanba YT, Terashima I (2006) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Physiol 47:1069–1080

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was funded by the Australian Research Council and the Grains Research and Development Corporation through the Industrial Transformation Research Centre, Legumes for Sustainable Agriculture, DP110104269, and US00056. The authors acknowledge the facilities, and the scientific and technical assistance, of the Australian Microscopy & Microanalysis Research Facility at Sydney Microscopy and Microanalysis, The University of Sydney. We thank Svetlana Ryazanova for technical assistance with gas exchange, and Elinor Goodman and Erin Lockhart for microscopy imaging and analysis. We also thank Dr Nerea Ubierna and two anonymous reviewers for helpful comments that greatly improved the manuscript.

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, The University of Sydney, 380 Werombi Road, Brownlow Hill, NSW, 2570, Australia

    Arjina Shrestha, Xin Song & Margaret M. Barbour

  2. School of Life Sciences and Oceanography, Shenzhen University, 3688 Nanhai Ave, Shenzhen, Guangdong, 518060, China

    Xin Song

Authors
  1. Arjina Shrestha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Margaret M. Barbour
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margaret M. Barbour.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 132 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shrestha, A., Song, X. & Barbour, M.M. The temperature response of mesophyll conductance, and its component conductances, varies between species and genotypes. Photosynth Res 141, 65–82 (2019). https://doi.org/10.1007/s11120-019-00622-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-019-00622-z

Keywords

Search

Navigation