Advertisement

Photosynthesis Research

, Volume 131, Issue 1, pp 1–13 | Cite as

Influence of light and nitrogen on the photosynthetic efficiency in the C4 plant Miscanthus × giganteus

  • Jian-Ying Ma
  • Wei Sun
  • Nuria K. Koteyeva
  • Elena Voznesenskaya
  • Samantha S. Stutz
  • Anthony Gandin
  • Andreia M. Smith-Moritz
  • Joshua L. Heazlewood
  • Asaph B. Cousins
Original Article

Abstract

There are numerous studies describing how growth conditions influence the efficiency of C4 photosynthesis. However, it remains unclear how changes in the biochemical capacity versus leaf anatomy drives this acclimation. Therefore, the aim of this study was to determine how growth light and nitrogen availability influence leaf anatomy, biochemistry and the efficiency of the CO2 concentrating mechanism in Miscanthus × giganteus. There was an increase in the mesophyll cell wall surface area but not cell well thickness in the high-light (HL) compared to the low-light (LL) grown plants suggesting a higher mesophyll conductance in the HL plants, which also had greater photosynthetic capacity. Additionally, the HL plants had greater surface area and thickness of bundle-sheath cell walls compared to LL plants, suggesting limited differences in bundle-sheath CO2 conductance because the increased area was offset by thicker cell walls. The gas exchange estimates of phosphoenolpyruvate carboxylase (PEPc) activity were significantly less than the in vitro PEPc activity, suggesting limited substrate availability in the leaf due to low mesophyll CO2 conductance. Finally, leakiness was similar across all growth conditions and generally did not change under the different measurement light conditions. However, differences in the stable isotope composition of leaf material did not correlate with leakiness indicating that dry matter isotope measurements are not a good proxy for leakiness. Taken together, these data suggest that the CO2 concentrating mechanism in Miscanthus is robust under low-light and limited nitrogen growth conditions, and that the observed changes in leaf anatomy and biochemistry likely help to maintain this efficiency.

Keywords

Carbon isotope discrimination C4 photosynthesis Miscanthus Nitrogen Light 

Notes

Acknowledgments

This research was supported by the National Natural Science Foundation of China [Grant Nos. 41071032, 31270445], the 9th Thousand Talents Program of China, the US Department of Energy, Office of Basic Energy Science [DE-FG02_09ER16062] and Office of Science, Office of Biological and Environmental Research [DE-AC02-05CH11231]. Instrumentation was obtained through an NSF Major Research Instrumentation Grant [#0923562]. JLH was supported by an Australian Research Council Future Fellowship [FT130101165]. We thank C. Cody for plants growth management, Dr. Steve Long for Miscanthus plant material and the Franceschi Microscopy and Imaging Center of Washington State University for use of its facilities.

Supplementary material

11120_2016_281_MOESM1_ESM.docx (175 kb)
Supplementary material 1 (DOCX 174 kb)

References

  1. Barbour MM, Evans JR, Simonin KA, von Caemmerer S (2016) Online CO2 and H2O oxygen isotope fractionations allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants. New PhytologistGoogle Scholar
  2. Bellasio C, Griffiths H (2014a) Acclimation of C4 metabolism to low light in mature maize leaves could limit energetic losses during progressive shading in a crop canopy. J Exp Bot 65:3725–3736CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bellasio C, Griffiths H (2014b) Acclimation to low light by C4 maize: implications for bundle sheath leakiness. Plant Cell Environ 37:1046–1058CrossRefPubMedGoogle Scholar
  4. Bellasio C, Griffiths H (2014c) The operation of two decarboxylases, transamination, and partitioning of C4 metabolic processes between mesophyll and bundle sheath cells allows light capture to be balanced for the maize C4 pathway. Plant Physiol 164:466–480CrossRefPubMedGoogle Scholar
  5. Bowling DR, Sargent SD, Tanner BD, Ehleringer JR (2003) Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem-atmosphere CO2 exchange. Agric For Meteorol 118:1–19CrossRefGoogle Scholar
  6. Clifton-Brown JC, Breuer J, Jones MB (2007) Carbon mitigation by the energy crop, Miscanthus. Glob Change Biol 13:2296–2307CrossRefGoogle Scholar
  7. Cousins AB, Badger MR, Von Caemmerer S (2006) Carbonic anhydrase and its influence on carbon isotope discrimination during C4 photosynthesis. Insights from antisense RNA in Flaveria bidentis. Plant Physiol 141:232–242CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cousins AB, Badger MR, von Caemmerer S (2008) C4 photosynthetic isotope exchange in NAD-ME- and NADP-ME-type grasses. J Exp Bot 59:1695–1703CrossRefPubMedGoogle Scholar
  9. Ellsworth PZ, Cousins AB (2016) Carbon isotopes and water use efficiency in C4 plants. Curr Opin Plant Biol 31:155–161CrossRefPubMedGoogle Scholar
  10. 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 13:281–292CrossRefGoogle Scholar
  11. Evans JR, von 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. Aust J Plant Physiol 21:475–495CrossRefGoogle Scholar
  12. Farage PK, Blowers D, Long SP, Baker NR (2006) Low growth temperatures modify the efficiency of light use by photosystem II for CO2 assimilation in leaves of two chilling-tolerant C4 species, Cyperus longus L. and Miscanthus x giganteus. Plant Cell Environ 29:720–728CrossRefPubMedGoogle Scholar
  13. Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205–226CrossRefGoogle Scholar
  14. Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35:1221–1231CrossRefPubMedGoogle Scholar
  15. Flexas J, Carriqui M, Coopman RE, Gago J, Galmes J, Martorell S, Morales F, Diaz-Espejo A (2014) Stomatal and mesophyll conductances to CO2 in different plant groups: underrated factors for predicting leaf photosynthesis responses to climate change? Plant Sci 226:41–48CrossRefPubMedGoogle Scholar
  16. Ghashghaie J, Duranceau M, Badeck F-W (2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 24:505–515CrossRefGoogle Scholar
  17. Gillon JS, Yakir D (2000) Naturally low carbonic anhydrase activity in C4 and C3 plants limits discrimination against (COO)-O18 during photosynthesis. Plant Cell Environ 23:903–915CrossRefGoogle Scholar
  18. Hansen EM, Christensen BT, Jensen LS, Kristensen K (2004) Carbon sequestration in soil beneath long-term Miscanthus plantations as determined by C13 abundance. Biomass Bioenergy 26:97–105CrossRefGoogle Scholar
  19. Harholt J, Jensen JK, Sorensen SO, Orfila C, Pauly M, Scheller HV (2006) ARABINAN DEFICIENT 1 is a putative arabinosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol 140:49–58CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hatch MD, Slack CR, Johnson HS (1967) Further studies on a new pathway of photosynthetic carbon dioxide fixation in sugarcane and its occurence in other plant species. Biochem J 102:417–422CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hatch MD, Agostino A, Jenkins CLD (1995) Measurement of the leakage of CO2 from bundle-sheath cells of leaves during C4 photosynthesis. Plant Physiol 108:173–181CrossRefPubMedPubMedCentralGoogle Scholar
  22. Heaton EA, Long SP, Voigt TB, Jones MB, Clifton-Brown J (2004) Miscanthus for renewable energy generation: European Union experience and projections for Illinois. Mitig Adapt Strat Glob Change 9:433–451CrossRefGoogle Scholar
  23. Henderson SA, von Caemmerer S, Farquhar GD (1992) Short-Term Measurements of Carbon Isotope Discrimination in Several C4 Species. Aust J Plant Physiol 19:263–285CrossRefGoogle Scholar
  24. Kromdijk J, Schepers HE, Albanito F, Fitton N, Carroll F, Jones MB, Finnan J, Lanigan GJ, Griffiths H (2008) Bundle Sheath Leakiness and Light Limitation during C4 Leaf and Canopy CO2 Uptake. Plant Physiol 148:2144–2155CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kromdijk J, Griffiths H, Schepers HE (2010) Can the progressive increase of C4 bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration? Plant Cell Environ 33:1935–1948CrossRefPubMedGoogle Scholar
  26. Kromdijk J, Ubierna N, Cousins AB, Griffiths H (2014) Bundle-sheath leakiness in C4 photosynthesis: a careful balancing act between CO2 concentration and assimilation. J Exp Bot 65:3443–3457CrossRefPubMedGoogle Scholar
  27. Kubásek J, Šetlík J, Dwyer S, Šantruc J (2007) Light and growth temperature alter carbon isotope discrimination and estimated bundle sheath leakiness in C4 grasses and dicots. Photosynth Res 91:47–58CrossRefPubMedGoogle Scholar
  28. Meinzer FC, Zhu J (1998) Nitrogen stress reduces the efficiency of the C4 CO2 concentrating system, and therefore quantum yield, in Saccharum (sugarcane) species. J Exp Bot 49:1227–1234Google Scholar
  29. Naidu SL, Long SP (2004) Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus × giganteus: an in vivo analysis. Planta 220:145–155CrossRefPubMedGoogle Scholar
  30. ØBro J, Harholt J, Scheller HV, Orfila C (2004) Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures. Phytochemistry 65:1429–1438CrossRefPubMedGoogle Scholar
  31. Pengelly JJ, Sirault XRR, Tazoe Y, Evans JR, Furbank RT, von Caemmerer S (2010) Growth of the C4 dicot Flaveria bidentis: photosynthetic acclimation to low light through shifts in leaf anatomy and biochemistry. J Exp Bot 61:4109–4122CrossRefPubMedPubMedCentralGoogle Scholar
  32. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents, verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
  33. Sage RF (2014) Stopping the leaks: new insights into C4 photosynthesis at low light. Plant Cell Environ 37:1037–1041CrossRefPubMedGoogle Scholar
  34. Scheller HV, Jensen JK, Sorensen SO, Harholt J, Geshi N (2007) Biosynthesis of pectin. Physiol Plantarum 129:283–295CrossRefGoogle Scholar
  35. Sims REH, Hastings A, Schlamadinger B, Taylor G, Smith P (2006) Energy crops: current status and future prospects. Glob Change Biol 12:2054–2076CrossRefGoogle Scholar
  36. Stutz SS, Edwards GE, Cousins AB (2014) Single-cell C4 photosynthesis: efficiency and acclimation of Bienertia sinuspersici to growth under low light. New Phytol 202:220–232CrossRefPubMedGoogle Scholar
  37. Sun W, Ubierna N, Ma J-Y, Cousins AB (2012) The influence of light quality on C4 photosynthesis under steady-state conditions in Zea mays and Miscanthus × giganteus: changes in rates of photosynthesis but not the efficiency of the CO2 concentrating mechanism. Plant Cell Environ 35:982–993CrossRefPubMedGoogle Scholar
  38. Sun W, Ubierna N, Ma J-Y, Walker B, Kramer D, Cousins AB (2014) The coordination of C4 photosynthesis and the CO2 concentrating mechanism in Zea mays and Miscanthus × giganteus in response to transient changes in light quality. Plant Physiol 164:1283–1292CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tazoe Y, Noguchi K, Terashima I (2006) Effects of growth light and nitrogen nutrition on the organization of the photosynthetic apparatus in leaves of a C4 plant, Amaranthus cruentus. Plant Cell Environ 29:691–700CrossRefPubMedGoogle Scholar
  40. Tazoe Y, Hanba YT, Furumoto T, Noguchi K, Terashima I (2008) Relationships between quantum yield for CO2 assimilation, activity of key enzymes and CO2 leakiness in Amaranthus cruentus, a C4 dicot, grown in high or low light. Plant Cell Physiol 49:19–29CrossRefPubMedGoogle Scholar
  41. Ubierna N, Sun W, Cousins AB (2011) The efficiency of C4 photosynthesis under low light conditions: assumptions and calculations with CO2 isotope discrimination. J Exp Bot 61:3119–3134CrossRefGoogle Scholar
  42. Ubierna N, Sun W, Kramer DM, Cousins AB (2013) The efficiency of C4 photosynthesis under low light conditions in Zea mays, Miscanthus × giganteus and Flaveria bidentis. Plant Cell Environ 36:365–381CrossRefPubMedGoogle Scholar
  43. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, VictoriaGoogle Scholar
  44. von Caemmerer S, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynth Res 77:191–207CrossRefGoogle Scholar
  45. von Caemmerer S, Evans JR, Cousins AB, Badger MR, Furbank RT (2008) C4 photosynthesis and CO2 diffusion. In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting New Pathways to C4 Rice. International Rice Research Institue, Los BosGoogle Scholar
  46. von Caemmerer S, Ghannoum O, Pengelly JJ, Cousins AB (2014) Carbon isotope discrimination as a tool to explore C4 photosynthesis. J Exp Bot 65:3459–3470CrossRefGoogle Scholar
  47. Wang D, Portis AR, Moose SP, Long SP (2008) Cool C4 photosynthesis: pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus × giganteus. Plant Physiol 148:557–567CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yin Z, van der Putten PEL, Driever SM, Struik PC (2016) Temperature response of bundle-sheath conductance in maize leaves. J Exp Bot. doi: 10.1083/jxb/era104 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Jian-Ying Ma
    • 1
    • 2
  • Wei Sun
    • 2
    • 3
  • Nuria K. Koteyeva
    • 4
  • Elena Voznesenskaya
    • 4
  • Samantha S. Stutz
    • 2
  • Anthony Gandin
    • 2
  • Andreia M. Smith-Moritz
    • 5
  • Joshua L. Heazlewood
    • 5
    • 6
  • Asaph B. Cousins
    • 2
  1. 1.Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and GeographyChinese Academy of SciencesUrumqiChina
  2. 2.School of Biological ScienceWashington State UniversityPullmanUSA
  3. 3.Institute of Grassland Science, Key Laboratory of Vegetation Ecology, Ministry of EducationNortheast Normal UniversityChangchunChina
  4. 4.Laboratory of Anatomy and MorphologyV.L. Komarov Botanical Institute of the Russian Academy of SciencesSt. PetersburgRussia
  5. 5.Joint BioEnergy Institute and Physical Biosciences DivisionLawrence Berkeley National LaboratoryBerkeleyUSA
  6. 6.ARC Centre of Excellence in Plant Cell Walls, School of BioSciencesThe University of MelbourneMelbourneAustralia

Personalised recommendations