Skip to main content
Log in

Effects of internal conductance and Rubisco on the optimum temperature for leaf photosynthesis in Fallopia japonica growing at different altitudes

  • Original Article
  • Published:
Ecological Research

Abstract

To investigate mechanisms of adjustment of the optimum temperature for leaf photosynthesis in alpine plants, we compared the temperature responses of photosynthesis, internal conductance (g i), and the amounts of activated Rubisco (ε) in two Fallopia japonica populations growing at elevations of 100 m (K0100), and 2250 m (F2250). There was an obvious difference in photosynthesis at high temperatures between the two populations, although there was no significant difference in the CO2/O2 specificity of Rubisco. Optimum temperatures for photosynthesis were 25 and 30 °C in F2250 and K0100, respectively. The temperature response of ε was similar to that of photosynthesis. The mean values of ε decreased 25 % (F2250) and 24 % (K0100), for temperatures 5 °C above the optimum for photosynthesis. In contrast, g i exponentially increased with increasing temperature in both populations. There was no significant difference in g i between populations for any given temperature. In both populations, there were no changes in CO2 concentrations at the Rubisco active site, when temperatures were above the photosynthetic optimum temperature. This clearly shows that photosynthetic optimum temperatures were not affected by photosynthetic limitation of CO2 diffusing from intercellular air spaces to Rubisco. Furthermore, the atmospheric pressure had a minor effect on the temperature response of photosynthesis. Thus, the decrease in ε in response to elevated temperatures reduced the photosynthetic optimum temperature in highland population of F. japonica, which was adjusted to the habitat.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barry RG (1981) Mountain weather and climate. Methunen, London

    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 Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Billings WD, Bliss LC (1959) An alpine snowbank environment and its effects on vegetation, plant development, and productivity. Ecology 40:388–397

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cen Y, Sage RF (2005) The regulation of rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:979–990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. PNAS 97:13430–43435

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Decker JP (1959) Some effects of temperature and carbon dioxide concentration on photosynthesis of mimules. Plant Physiol 34:103–106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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  Google Scholar 

  • Dwyer SA, Ghannoum O, Nicotra A, von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant, Cell Environ 30:53–66

    Article  CAS  Google Scholar 

  • Edwards GE, Walker DA (1983) C3, C4: Mechanisms, and cellular and environmental regulation of photosynthesis. Blackwell, Oxford

    Google Scholar 

  • Epron D, Godard D, Cornic G, Genty B (1995) Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two species (Fagus sylvatica L. and Castanea sativa Mill.). Plant, Cell Environ 18:43–51

    Article  Google Scholar 

  • Evans JR, Terashima I (1988) Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiol 29:157–165

    CAS  Google Scholar 

  • Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiol 110:339–346

    CAS  PubMed Central  PubMed  Google Scholar 

  • Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust. J Plant Physiol 13:281–292

    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 

  • Friend AD, Woodward FI (1990) Evolutionary and ecophysiological responses of mountain plants to the growing season environment. Adv Ecol Res 20:59–124

    Article  Google Scholar 

  • Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529

    Article  CAS  PubMed  Google Scholar 

  • Hesketh JD, Larson EM, Gordon AJ, Peters DB (1983) Internal factors influencing photosynthesis and respiration. In: Dale JE, Milthorpe FL (eds) The growth and functioning of leaves. Cambridge University Press, Cambridge, pp 381–411

    Google Scholar 

  • 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. J Exp Bot 57:291–302

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa C, Hatanaka T, Misoo S, Fukayama H (2009) Screening of high k cat Rubisco among poaceae for improvement of photosynthetic CO2 assimilation in rice. Plant Prod Sci 12:345–350

    Article  CAS  Google Scholar 

  • Kim K, Portis AR Jr (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. Plant Cell Physiol 46:522–530

    Article  CAS  PubMed  Google Scholar 

  • Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant, Cell Environ 24:529–538

    Article  CAS  Google Scholar 

  • Körner C (1982) CO2 exchange in the alpine sedge Carex curvula as influenced by canopy structure, light and temperature. Oecologia 53:98–104

    Article  Google Scholar 

  • Körner C (1999) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin

  • Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 74:623–632

    Article  Google Scholar 

  • Kubien DS, von Cammerer S, Furbank RT, Sage RF (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132:1577–1585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kubien DS, Whitney SM, Moore PV, Jesson LK (2008) The biochemistry of Rubisco in Flaveria. J Exp Bot 59:1767–1777

    Article  CAS  PubMed  Google Scholar 

  • Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Plant Physiol 110:903–912

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD (1992) Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant, Cell Environ 15:873–899

    Article  CAS  Google Scholar 

  • Makino A, Sage RF (2007) Temperature response of photosynthesis in transgenic rice transformed with ‘sense’ or ‘antisense’ rbcS. Plant Cell Physiol 48:1472–1483

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Mae T, Ohira K (1988) Differences between wheat and rice in the enzymic properties of ribulose 1.5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange. Planta 174:30–38

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Sakashita H, Hidema J, Mae T, Ojima K, Osmond B (1992) Distinctive responses of ribulose-1,5-bisphosphate carboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationships to CO2-transfer resistance. Plant Physiol 100:1737–1743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mooney HA, Strain BR, West M (1966) Photosynthetic efficiency at reduced carbon dioxide tensions. Ecology 47:490–491

    Article  Google Scholar 

  • Moser W, Brzoska W, Zachhuber K, Larcher W (1977) Ergebnisse des IBP-Projekts “Hoher Nebelkogel 3184 m”. Stitzungsber Österr Akad Wiss 186:387–419

    Google Scholar 

  • Parkhurst DF, Mott KA (1990) Intercellular diffusion limits to CO2 uptake in leaves. Plant Physiol 94:1024–1032

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr.) Wats. Plant Physiol 59:795–799

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pearcy RW, Ehleringer J, Mooney HA, Rundel PW (1989) Plant physiological ecology. Chapman and Hall, London

    Book  Google Scholar 

  • Sage RF (2002) Variation in the k cat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53:609–620

    Article  CAS  PubMed  Google Scholar 

  • Sakata T, Yokoi Y (2002) Analysis of the O2 dependency in leaf-level photosynthesis of two Reynoutria japonica populations growing at different altitudes. Plant, Cell Environ 25:65–74

    Article  Google Scholar 

  • Sakata T, Kachi N, Yokoi Y (2007) Quantitative evaluation of the counterbalance between photosynthetic stimulation and depression caused by low partial pressure of O2 and CO2 in alpine atmospheres. Polar Sci 1:55–62

    Article  CAS  Google Scholar 

  • Sasaki H, Samejima M, Ishii R (1996) Analysis by delta-13C measurement on mechanism of cultivar difference in leaf photosynthesis on rice (Oryza sativa L.). Plant Cell Physiol 37:1161–1166

    Article  CAS  Google Scholar 

  • Scafaro AP, von Caemmerer S, Evans JR, Atwell BJ (2011) Temperature response of mesophyll conductance in cultivated and wild Oryza species with contrasting mesophyll cell wall thickness. Plant, Cell Environ 34:1999–2008

    Article  CAS  Google Scholar 

  • Seemann JR, Badger MR, Berry JA (1984) Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiol 74:791–794

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen H, Wang S, Tang Y (2013) Grazing alters warming effects on leaf photosynthesis and respiration in Gentiana straminea, an alpine forb species. J Plant Ecol 6:418–427

    Article  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 

  • Terashima I, Masuzawa T, Ohba H, Yokoi Y (1995) Is photosynthesis suppressed at high elevations due to low CO2 pressure? Ecology 76:2663–2668

    Article  Google Scholar 

  • Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487

    Article  CAS  PubMed  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 

  • Yamori W, von Caemmerer S (2009) Effect of Rubisco activase deficiency on the temperature response of CO2 assimilation rate and Rubisco activation state: insights from transgenic tobacco with reduced amounts of Rubisco activase. Plant Physiol 151:2073–2082

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamori W, Noguchi K, Hanba YT, Terashima I (2006a) 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 

  • Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006b) 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 Environ 29:1659–1670

    Article  CAS  Google Scholar 

  • Yeoh H-H, Badger MR, Watson L (1980) Variations in K m (CO2) of ribulose 1,5-bisphosphate carboxylase among grasses. Plant Physiol 66:1110–1112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshie F (1986) Intercellular CO2 concentration and water-use efficiency of temperate plants with different life forms and from different microhabitats. Oecologia 69:370–374

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Y. Yokoi for significant ideas and discussions. We thank members of Biological Laboratory of Kitasato University for comments and suggestions on this study. We thank Prof. I. Terashima for helpful advice for the model. We also thank Prof. Y. S. Bekku for significant suggestions. This study was supported by the Biological Laboratory of Kitasato University and partially supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (No. 19570025).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tsuyohi Sakata.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sakata, T., Nakano, T. & Kachi, N. Effects of internal conductance and Rubisco on the optimum temperature for leaf photosynthesis in Fallopia japonica growing at different altitudes. Ecol Res 30, 163–171 (2015). https://doi.org/10.1007/s11284-014-1223-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-014-1223-5

Keywords

Navigation