Abstract
Rubisco specificity factor (Sc/o), a measure of the relative capacities of an enzyme to catalyze carboxylation and oxygenation of ribulose-1,5-bisphosphate, determines the extent of photosynthetic CO2 assimilation and photorespiratory CO2 release. The current model of C3 photosynthesis, the Farquhar–von Caemmerer–Berry (FvCB) model, requires a species-specific Sc/o. However, Sc/o values have never been reported in conifers, likely because in vitro kinetic analysis of conifer Rubisco presents difficulties. To estimate the Sc/o of conifers and compare it with angiosperm Sc/o, we measured changes in leaf CO2 compensation points (Γ) in response to O2 partial pressure for a variety of leaves, with different rates of day respiration (Rday) and maximum Rubisco carboxylation (Vcmax) in gymnosperms (Ginkgo biloba), conifers (Metasequoia glyptostroboides and Cryptomeria japonica), and angiosperms (Nicotiana tabacum and Phaseolus vulgaris). As predicted by the FvCB model, the slope of a linear function of Γ vs O2 partial pressure, d, increased alongside increasing Rday/Vcmax. The Sc/o was obtainable from this relationship between d and Rday/Vcmax, because the d values at Rday/Vcmax = 0 corresponded to α/Sc/o, where α was the photorespiratory CO2 release rate per Rubisco oxygenation rate (generally assumed to be 0.5). The calculated Sc/o values of N. tabacum and P. vulgaris exhibited good agreement with those reported by in vitro studies. The Sc/o values of both conifers were similar to those of the two angiosperm species. In contrast, the Sc/o value of G. biloba was significantly lower than those of the other four studied species. These results suggest that our new method for Sc/o estimation is applicable to C3 plants, including those for which in vitro kinetic analysis is difficult. Furthermore, results also suggest that conifer Sc/o does not differ significantly from that of C3 angiosperms, assuming α remains unchanged.
Similar content being viewed by others
References
Beadle CL, Hart JW, Jarvis PG (1983) The extraction and activity of carboxylases in Sitka spruce and some other conifers. Photosynthetica 17:321–333
Berner RA (1999) Atmospheric oxygen over Phanerozoic time. Proc Natl Acad Sci USA 96:10955–10957
Bird IF, Cornelius MJ, Keys AJ (1982) Affinity of RuBP carboxylases for carbon dioxide and inhibition of the enzymes be oxygen. J Exp Bot 33:1004–1013
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
Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212
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 Environ 27:137–153
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Flamholz A, Prywes N, Moran U, Davidi D, Bar-On Y, Oltrogge L et al (2019) Revisiting tradeoffs between Rubisco kinetic parameters. Biochemistry 58:3365–3376
Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgewick PJ et al (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
Galmés J, Medrano H, Flexas J (2006) Acclimation of Rubisco specificity factor to drought in tobacco: discrepancies between in vitro and in vivo estimations. J Exp Bot 57:3659–3667
Galmés J, Kapralov MV, Andralojc PJ, Conesa M, Keys AJ, Parry MAJ et al (2014) Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant Cell Environ 37:1989–2001
Haworth M, Elliott-Kingston C, McElwain JC (2011) Stomatal control as a driver of plant evolution. J Exp Bot 62:2419–2423
Heldt H-W (2000) Pflanzenbiochemie. Speringer-Verlag, Tokyo
Hermida-Carrera C, Kapralov MV, Galmés J (2016) Rubisco catalytic properties and temperature response in crops. Plant Physiol 171:2549–2561
Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature 291:513–514
Kane HJ, Viil J, Entsch B, Paul K, Morell MK, Andrews TJ (1994) An improved method for measuring the CO2/O2 specificity of ribulose bisphosphate carboxylase-oxygenase. Aust J Plant Physiol 21:449–461
Key AJ, Parry MAJ (1990) Ribulose bisphosphate carboxylase/oxygenase and carbonic anhydrase. In: Lea PJ (ed) Methods in plant biochemistry: vol, 3. enzymes of primary metabolism. Academic Press, London, pp 1–14
Laing WA, Ogren WL, Hageman RH (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose 1,5-diphosphate carboxylase. Plant Physiol 54:678–685
Ma QW, Li CS, Li FL (2007) Epidermal structures of Cryptomeria japonica and implications to the fossil record. Acta Palaeobot 47:281–289
Mao K, Milne RI, Zhang L, Peng Y, Liu J, Thomas P et al (2012) Distribution of living Cupressaceae reflects the breakup of Pangea. Proc Natl Acad Sci USA 109:7793–7798
Miyazawa S-I, Nishiguchi M, Futamura N, Yukawa T, Miyao M, Maruyama TE et al (2018) Low assimilation efficiency of photorespiratory ammonia in conifer leaves. J Plant Res 131:789–802
Miyazawa S-I, Terashima I (2001) Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant Cell Environ 24:279–291
Occhialini A, Lin MT, Andralojc PJ, Hanson MR, Parry MAJ (2016) Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO2. Plant J 85:148–160
Orr DJ, Alcântara A, Kapralov MV, Andralojc PJ, Carmo-Silva E, Parry MAJ (2016) Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency. Plant Physiol 172:707–717
Rudall PJ, Rowland A, Bateman RM (2012) Ultrastructure of stomatal development in Ginkgo biloba. Int J Plant Sci 173:849–860
Šesták Z (1985) Photosynthesis during leaf development. W. Junk Publishers, Dordrecht
Sharwood RE, von Caemmerer S, Maliga P, Whitney SM (2008) The catalytic properties of hybrid Rubisco comprising tobacco small and sunflower large subunits mirror the kinetically equivalent source Rubiscos and can support tobacco growth. Plant Physiol 146:83–96
Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103:7246–7251
Tholen D, Ethier G, Genty B, Pepin S, Zhu X-G (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103
Veromann-Jurgenson LL, Tosens T, Laanisto L, Niinemets U (2017) Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living! J Exp Bot 68:1639–1653
Viil J, Ivanova H, Pärnik T (2012) Specificity factor of Rubisco: estimation in intact leaves by carboxylation at different CO2/O2 ratios. Photosynthetica 50:247–253
Von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, Collingwood
Walker BJ, Ort DR (2015) Improved method for measuring the apparent CO2 photocompensation point resolves the impact of multiple internal conductances to CO2 to net gas exchange. Plant Cell Environ 38:2462–2474
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
Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ (1987) Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiol 83:155–158
Whitney SM, Birch R, Kelso C, Beck JL, Kapralov MV (2015) Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone. Proc Natl Acad Sci USA 112:3564–3569
Yeoh HH, Badger MR, Watson L (1981) Variations in kinetic properties of ribulose-1,5-bisphosphate carboxylases among plants. Plant Physiol 67:1151–1155
Acknowledgements
We thank Dr. Ko Tahara, Dr. Mitsuru Nishiguchi, and Dr. Takafumi Miyama in FFPRI for their helpful discussion and also thank Ms. Ai Hagiwara and Ms. Rie Yamamoto for their assistance with experiments. We used SAS software provided by AFFRIT, MAFF, Japan. This work was supported by Research Grant #201705 of FFPRI and JSPS KAKENHI Grant Number JP16K07791.
Author information
Authors and Affiliations
Contributions
S-IM performed experiments and analyses and wrote the manuscript; HT prepared the plant materials; TU-I analyzed the rbcL alignments; YS supported the experimental design. HT, TU-I, and YS edited the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Electronic Supplementary Material
Below is the link to the electronic supplementary material
Rights and permissions
About this article
Cite this article
Miyazawa, SI., Tobita, H., Ujino-Ihara, T. et al. Oxygen response of leaf CO2 compensation points used to determine Rubisco specificity factors of gymnosperm species. J Plant Res 133, 205–215 (2020). https://doi.org/10.1007/s10265-020-01169-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-020-01169-0