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The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity

  • Physiological Ecology - Original Paper
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Abstract

Photosynthetic capacity is known to vary considerably among species. Its physiological cause and ecological significance have been one of the most fundamental questions in plant ecophysiology. We studied the contents of Rubisco (a key enzyme of photosynthesis) and cell walls in leaves of 26 species with a large variation in photosynthetic rates. We focused on photosynthetic nitrogen-use efficiency (PNUE, photosynthetic rate per nitrogen), which can be expressed as the product of Rubisco-use efficiency (RBUE, photosynthetic rate per Rubisco) and Rubisco nitrogen fraction (RNF, Rubisco nitrogen per total leaf nitrogen). RBUE accounted for 70% of the interspecific variation in PNUE. The variation in RBUE was ascribed partly to stomatal conductance, and other factors such as mesophyll conductance and Rubisco kinetics might also be involved. RNF was also significantly related to PNUE but the correlation was relatively weak. Cell wall nitrogen fraction (WNF, cell wall nitrogen per total leaf nitrogen) increased with increasing leaf mass per area, but there was no correlation between RNF and WNF. These results suggest that nitrogen allocation to cell walls does not explain the variation in PNUE. The difference in PNUE was not caused by a sole factor that was markedly different among species but by several factors each of which was slightly disadvantageous in low PNUE species.

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Abbreviations

Ci/Ca:

Ratio of CO2 concentration in intercellular spaces to that in air

LLS:

Leaf life span

LMA:

Leaf mass per area

N :

Leaf nitrogen

R :

Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase)

RNF:

Rubisco nitrogen fraction

P :

Photosynthetic rate

PNUE:

Photosynthetic nitrogen-use efficiency

RBUE:

Rubisco-use efficiency

WM:

Cell wall mass

WN:

Cell wall nitrogen

WNF:

Cell wall nitrogen fraction

Subscripted “area”:

Per unit leaf area

Subscripted “mass”:

Per unit mass

References

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a low land tropical forest. Ecol Monogr 53:209–233

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Evans JR, Seemann JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences and control. In: Crigs WR (ed) Photosynthesis. Liss, New York, pp 183–205

    Google Scholar 

  • Falster D, Warton D, Wright I (2006) Standardised major axis tests and routines. Version 2. http://www.bio.mq.edu.au/ecology/SMATR

  • 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  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Feng YL (2008) Nitrogen allocation and partitioning in invasive and native Eupatorium species. Physiol Plant 132:350–358

    Article  PubMed  CAS  Google Scholar 

  • Feng YL, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153:501–510

    Article  PubMed  Google Scholar 

  • Field C, Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 25–55

    Google Scholar 

  • Field C, Merino J, Mooney HA (1983) Compromises between water-use efficiency and nitrogen-use efficiency in five species of California evergreens. Oecologia 60:384–389

    Article  Google Scholar 

  • Flexas J, Ribas-Carbó 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  PubMed  CAS  Google Scholar 

  • Fry SC (1988) The growing plant cell wall. Longman, Harlow

    Google Scholar 

  • Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579

    Article  Google Scholar 

  • Gleadow RM, Foley WJ, Woodrow IE (1998) Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant Cell Environ 21:12–22

    Article  CAS  Google Scholar 

  • Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen use efficiency. Plant Cell Environ 32:259–270

    Article  PubMed  CAS  Google Scholar 

  • Hasebe M, Ando T, Iwatsuki K (1998) Intrageneric relationships of maple trees based on the chloroplast DNA restriction fragment length polymorphisms. J Plant Res 111:441–451

    Article  CAS  Google Scholar 

  • Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494

    Article  PubMed  Google Scholar 

  • Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Ann Bot 95:521–533

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka K, Hirose T (2000) Photosynthetic nitrogen-use efficiency in species coexisting in a warm-temperate evergreen forest. Tree Physiol 20:1249–1254

    PubMed  CAS  Google Scholar 

  • Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in woody and herbaceous plants. Funct Ecol 12:896–905

    Article  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 

  • Lamb Frye AS, Kron KA (2003) rbcL phylogeny and character evolution in Polygonaceae. Syst Bot 28:326–332

    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 

  • Martins EP (2004) COMPARE Version 4.6b. http://compare.bio.indiana.edu/~martinsl/compare/

  • Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866

    Article  Google Scholar 

  • Ohyama M, Baba K, Itoh T, Shiraishi S (1999) Polymorphism analysis of Fagaceae and DNA-based identification of Fagus species grown in Japan based on the rbcL gene. J Wood Sci 45:183–187

    Article  CAS  Google Scholar 

  • Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425

    Article  Google Scholar 

  • Onoda Y, Schieving F, Anten NPR (2008) Effects of light and nutrient availability on leaf mechanical properties of Plantago major: a conceptual approach. Ann Bot 101:727–736

    Article  PubMed  Google Scholar 

  • Pons TL, Westbeek MHK (2004) Analysis of differences in photosynthetic nitrogen-use efficiency between four contrasting species. Physiol Plant 122:68–78

    Article  CAS  Google Scholar 

  • Pons TL, van der Werf A, Lambers H (1994) Photosynthetic nitrogen use efficiency of inherently low- and fast-growing species: possible explanations for observed differences. In: Roy J, Garnier E (eds) A whole plant perspective on carbon–nitrogen interactions. SPB, The Hague, pp 61–77

    Google Scholar 

  • Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific area. Oecologia 116:26–37

    Article  Google Scholar 

  • Poorter H, Farquhar GD (1994) Transpiration, intercellular carbon dioxide concentration and carbon-isotope discrimination of 24 wild species differing in relative growth rate. Aust J Plant Physiol 21:507–516

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1991) Leaf lifespan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86:16–24

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: Global convergence in plant functioning. Proc Nat Acad Sci USA 94:13730–13734

    Article  PubMed  CAS  Google Scholar 

  • Stevens PF (2008) Angiosperm phylogeny website. Version 9. http://www.mobot.org/MOBOT/research/APweb/

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354

    Article  PubMed  CAS  Google Scholar 

  • 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

    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  PubMed  CAS  Google Scholar 

  • Warren CR, Adams MA (2004a) Evergreen trees do not maximize instantaneous photosynthesis. Trends Plant Sci 9:270–274

    Article  PubMed  CAS  Google Scholar 

  • Warren CR, Adams MA (2004b) What determines rates of photosynthesis per unit nitrogen in Eucalyptus seedlings? Funct Plant Biol 31:1169–1178

    Article  CAS  Google Scholar 

  • Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201

    Article  PubMed  CAS  Google Scholar 

  • Warren CR, Dreyer E, Tausz M, Adams MA (2006) Ecotype adaptation and acclimation of leaf traits to rainfall in 29 species of 16-year-old Eucalyptus at two common gardens. Funct Ecol 20:929–940

    Article  Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Westbeek HMH, Pons TL, Cambridge ML, Atkin OK (1999) Analysis of differences in photosynthetic nitrogen use efficiency of alpine and lowland Poa species. Oecologia 120:19–26

    Article  Google Scholar 

  • Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Funct Ecol 15:351–359

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby B et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

  • Wright IJ, Reich PB, Cornelissen JHC et al (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496

    Article  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 68:370–374

    Article  Google Scholar 

Download references

Acknowledgments

We thank Shimpei Oikawa, Yusuke Onoda, Yuko Yasumura, Onno Muller and John Evans for kind help in the field experiment and valuable suggestions. This study was supported in part by grants from the Japan Ministry of Education, Culture, Sports, Science and Technology (KAKENHI) and from the Global Environment Research Fund (F-052) from the Japan Ministry of the Environment and by the GCOE program J03 of the MEXT, Japan.

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Authors and Affiliations

  1. Graduate School of Life Science, Tohoku University, Aoba, Sendai, 980-8578, Japan

    Kouki Hikosaka & Aki Shigeno

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  1. Kouki Hikosaka
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  2. Aki Shigeno
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Correspondence to Kouki Hikosaka.

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Communicated by R. Sage.

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Hikosaka, K., Shigeno, A. The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity. Oecologia 160, 443–451 (2009). https://doi.org/10.1007/s00442-009-1315-z

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