Skip to main content
SpringerLink
Log in

Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

This study evaluates acclimation of photosynthesis and stomatal conductance in three evolutionary lineages of C3, C3–C4 intermediate, and C4 species grown in the low CO2 and hot conditions proposed to favo r the evolution of C4 photosynthesis. Closely related C3, C3–C4, and C4 species in the genera Flaveria, Heliotropium, and Alternanthera were grown near 380 and 180 μmol CO2 mol−1 air and day/night temperatures of 37/29°C. Growth CO2 had no effect on photosynthetic capacity or nitrogen allocation to Rubisco and electron transport in any of the species. There was also no effect of growth CO2 on photosynthetic and stomatal responses to intercellular CO2 concentration. These results demonstrate little ability to acclimate to low CO2 growth conditions in closely related C3 and C3–C4 species, indicating that, during past episodes of low CO2, individual C3 plants had little ability to adjust their photosynthetic physiology to compensate for carbon starvation. This deficiency could have favored selection for more efficient modes of carbon assimilation, such as C3–C4 intermediacy. The C3–C4 species had approximately 50% greater rates of net CO2 assimilation than the C3 species when measured at the growth conditions of 180 μmol mol−1 and 37°C, demonstrating the superiority of the C3–C4 pathway in low atmospheric CO2 and hot climates of recent geological time.

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

Access this article

Log in via an institution

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

  • Anderson LJ, Maherali H, Johnson HB, Polley HW, Jackson RB (2001) Gas exchange and photosynthetic acclimation over sub-ambient to elevated CO2 in a C3–C4 grassland. Glob Change Biol 7:693–707

    Article  Google Scholar 

  • Arakaki M, Christin PA, Nyffeler R et al (2011) Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proc Natl Acad Sci USA 108:8379–8384

    Article  PubMed  CAS  Google Scholar 

  • Arntz AM, DeLucia EH, Jordan N (2000a) Fitness effects of a photosynthetic mutation across contrasting environments. J Evolut Biol 13:792–803

    Article  Google Scholar 

  • Arntz AM, DeLucia EH, Jordan N (2000b) From fluorescence to fitness: variation in photosynthetic rate affects fecundity and survivorship. Ecology 81:2567–2576

    Article  Google Scholar 

  • Campbell CD, Sage RF, Kocacinar F, Way DA (2005) Estimation of the whole-plant CO2 compensation point of tobacco (Nicotiana tabacum L.). Glob Change Biol 11:1956–1967

    Google Scholar 

  • Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43

    Article  PubMed  CAS  Google Scholar 

  • Christin PA, Osborne CP, Sage RF, Arakaki M, Edwards EJ (2011) C4 eudicots are not younger than C4 monocots. J Exp Bot 62:3171–3181

    Article  PubMed  CAS  Google Scholar 

  • Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant Cell Environ 21:427–435

    Article  CAS  Google Scholar 

  • Devi MT, Rajagopalan AV, Raghavendra AS (1995) Predominant localization of mitochondria enriched with glycine-decarboxylating enzymes in bundle sheath cells of Alternanthera tenella, a C3–C4 intermediate species. Plant Cell Environ 18:589–594

    Article  CAS  Google Scholar 

  • Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals I. Growth and biomass allocation. Oecologia 101:13–20

    Article  Google Scholar 

  • Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc Natl Acad Sci USA 107:2532–2537

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer JR, Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiol 73:555–559

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer JR, Sage RF, Flanagan LB, Pearcy RW (1991) Climate change and the evolution of C4 photosynthesis. Trends Ecol Evol 6:95–99

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299

    Article  Google Scholar 

  • Evans JR (1983) Photosynthesis and nitrogen partitioning in leaves of Triticum aestivum and related species. PhD dissertation, Australian National University, Canberra

  • Farris MA, Lechowicz MJ (1990) Functional interactions among traits that determine reproductive success in a native annual plant. Ecology 71:548–557

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Frohlich MW (1978) Systematics of Heliotropium section Orthostachys in Mexico. PhD dissertation, Harvard University

  • Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytol 188:674–695

    Article  PubMed  Google Scholar 

  • Herrick JD, Maherali H, Thomas RB (2004) Reduced stomatal conductance in sweetgum (Liquidambar styraciflua) sustained over long-term CO2 enrichment. New Phytol 162:387–396

    Article  Google Scholar 

  • Huxman TE, Monson RK (2003) Stomatal responses of C3, C3–C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant Cell Environ 26:313–322

    Article  CAS  Google Scholar 

  • Janacek SH, Trenkamp S, Palmer B et al (2009) Photosynthesis in cells around veins of the C3 plant Arabidopsis thaliana is important for both the shikimate pathway and leaf senescence as well as contributing to plant fitness. Plant J 59:329–343

    Article  PubMed  CAS  Google Scholar 

  • Johnson HB, Polley HW, Mayeux HS (1993) Increasing CO2 and plant-plant interactions: effects on natural vegetation. Vegetatio 104(105):157–170

    Article  Google Scholar 

  • Ku MSB, Monson RK, Littlejohn RO, Nakamoto H, Fisher DB, Edwards GE (1983) Photosynthetic characteristics of C3–C4 intermediate Flaveria species I. Leaf anatomy, photosynthetic responses to O2 and CO2 and activities of key enzymes in the C3 and C4 pathways. Plant Physiol 71:944–948

    Article  PubMed  CAS  Google Scholar 

  • Ku MSB, Wu J, Dai Z, Scott RA, Chu C, Edwards GE (1991) Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiol 96:518–528

    Article  PubMed  CAS  Google Scholar 

  • Kurschner WM, Kvacek Z, Dilcher DL (2008) The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proc Natl Acad Sci USA 105:449–453

    Article  PubMed  Google Scholar 

  • Lodge RJ, Dijkstra P, Drake BG, Morison JIL (2001) Stomatal acclimation to increased CO2 concentration in a Florida scrub oak species Quercus myrtifolia Wild. Plant Cell Environ 24:77–88

    Article  CAS  Google Scholar 

  • Maherali H, Reid CD, Polley HW, Johnson HB, Jackson RB (2002) Stomatal acclimation over a sub-ambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ 25:557–566

    Article  CAS  Google Scholar 

  • McKown AD, Moncalvo JM, Dengler NG (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am J Bot 92:1911–1928

    Article  PubMed  CAS  Google Scholar 

  • Monson RK (2003) Gene duplication, neofunctionalization and the evolution of C4 photosynthesis. Int J Plant Sci 164:S43–S54

    Google Scholar 

  • Monson RK, Jaeger CH (1991) Photosynthetic characteristics of C3–C4 intermediate Flaveria floridana (Asteraceae) in natural habitats: evidence of advantages to C3–C4 photosynthesis at high leaf temperatures. Am J Bot 78:795–800

    Article  Google Scholar 

  • Monson RK, Rawsthorne S (2000) CO2 assimilation in C3–C4 intermediate plants. In: Leegood RC, Sharkey TD, Von Caemmerer S (eds) Photosynthesis: physiology, metabolism. Kluwer, The Netherlands, pp 533–550

    Google Scholar 

  • Monson RK, Moore BD, Ku MSB, Edwards GE (1986) Co-function of C3- and C4-photosynthetic pathways in C3, C4 and C3–C4 intermediate Flaveria species. Planta 168:493–502

    Article  CAS  Google Scholar 

  • Morgan JA, Brown RH (1979) Photosynthesis in grass species differing in carbon dioxide fixation pathways. Plant Physiol 64:257–262

    Article  PubMed  CAS  Google Scholar 

  • Muhaidat R, Sage TL, Frohlich MW, Dengler NG, Sage RF (2011) Characterization of C3–C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity. Plant Cell Environ 34:1723–1736

    Article  PubMed  CAS  Google Scholar 

  • Pagani M, Freeman KH, Arthur MA (1999) Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285:876–879

    Article  PubMed  CAS  Google Scholar 

  • Pagani M, Zachos JC, Freeman KH, Tipple B, Bohaty S (2005) Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309:600–603

    Article  PubMed  CAS  Google Scholar 

  • Pearson PN, Palmer MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406:695–699

    Article  PubMed  CAS  Google Scholar 

  • Petit JR, Jouzel J, Raynaud D et al (1999) Climate and atmospheric history of the past 420, 000 years from the Vostok ice core, Antarctica. Nature 399:429–436

    Article  CAS  Google Scholar 

  • Polley HW, Johnson HB, Mayeux HS (1992) Growth and gas exchange of oats (Avena sativa) and wild mustard (Brassica kaber) at subambient CO2 concentrations. Int J Plant Sci 153:453–461

    Article  CAS  Google Scholar 

  • Polley HW, Johnson HB, Derner J (2002) Soil- and plant-water dynamics in a C3/C4 grassland exposed to a sub-ambient to super-ambient CO2 gradient. Glob Change Biol 8:1118–1129

    Article  Google Scholar 

  • Powell AM (1978) Systematics of Flaveria (Flaveriinae-Asteraceae). Ann Mo Bot Gard 65:590–636

    Article  Google Scholar 

  • Rajendrudu G, Prasad JSR, Das VSR (1986) C3–C4 intermediate species in Alternanthera (Amaranthaceae): leaf anatomy, CO2 compensation point, net CO2 exchange and activities of photosynthetic enzymes. Plant Physiol 80:409–414

    Article  PubMed  CAS  Google Scholar 

  • Royer DL, Wing SL, Beerling DJ, Jolley DW, Koch PL, Hickey LJ, Berner RA (2001) Paleobotanical evidence for near present-day levels of atmospheric CO2 during part of the tertiary. Science 292:2310–2313

    Article  PubMed  CAS  Google Scholar 

  • Sage RF (1995) Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture? Glob Change Biol 1:93–106

    Article  Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370

    Article  CAS  Google Scholar 

  • Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends Plant Sci 6:19–24

    Article  Google Scholar 

  • Sage RF, Reid CD (1992) Photosynthetic acclimation to sub-ambient CO2 (20 Pa) in the C3 annual Phaseolus vulgaris L. Photosynthetica 27:605–617

    CAS  Google Scholar 

  • Sage RF, Pearcy RW, Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants III. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 85:355–359

    Article  PubMed  CAS  Google Scholar 

  • Sage RF, Reid CD, Moore BD, Seemann JR (1993) Long-term kinetics of the light-dependent regulation of ribulose-1, 5-bisphosphate carboxylase oxygenase activity in plants with and without 2-carboxyarabitinol 1-phosphate. Planta 191:222–230

    Article  CAS  Google Scholar 

  • Sage RF, Christin PA, Edwards EA (2011a) The lineages of C4 photosynthesis on planet Earth. J Exp Bot (in press)

  • Sage TL, Sage RF, Vogan PJ, Rahman B, Johnson DC, Oakley JC, Heckel MA (2011b) The occurrence of C2 photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae). J Exp Bot 62:3183–3195

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-del Pino I, Borsch T, Motley TJ (2009) trnL-F and rpl16 sequence data and dense taxon sampling reveal monophyly of unilocular anthered Gomphrenoideae (Amaranthaceae) and an improved picture of their internal relationships. Syst Bot 34:57–67

    Article  Google Scholar 

  • Santrucek J, Sage RF (1996) Acclimation of stomatal conductance to a CO2-enriched atmosphere and elevated temperature in Chenopodium album. Aust J Plant Physiol 23:467–478

    Article  CAS  Google Scholar 

  • Schuster WS, Monson RK (1990) An examination of the advantages of C3–C4 intermediate photosynthesis in warm environments. Plant Cell Environ 13:903–912

    Article  Google Scholar 

  • Solbrig OT (1981) Studies on the population ecology of the genus Viola II. The effect of plant size on fitness in Viola sororia. Evolution 35:1080–1093

    Article  Google Scholar 

  • Sudderth EA, Espinosa-Garcia FJ, Holbrook NM (2009) Geographical distributions and physiological characteristics of co-existing Flaveria species in south-central Mexico. Flora 204:89–98

    Article  Google Scholar 

  • Tissue DT, Griffin KL, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals II. Photosynthesis and biochemistry. Oecologia 101:21–28

    Article  Google Scholar 

  • Tognetti R, Minnocci A, Penuelas J, Raschi A, Jones MB (2000) Comparative field water relations of three Mediterranean shrub species co-occurring at a natural CO2 vent. J Exp Bot 51:1135–1146

    Article  PubMed  CAS  Google Scholar 

  • Tripati AK, Roberts CD, Eagle RA (2009) Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394–1397

    Article  PubMed  CAS  Google Scholar 

  • Vincentini A, Barber JC, Aliscioni SA, Giussani LM, Kellogg EA (2008) The age of grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14:2963–2977

    Article  Google Scholar 

  • Vogan PJ (2010) The physiological ecology of C3-C4 intermediate eudicots in warm environments. PhD dissertation, University of Toronto, Toronto

  • Vogan PJ, Sage RF (2011) The water-use and nitrogen-use efficiencies of C3–C4 intermediate species of Flaveria Juss (Asteraceae). Plant Cell Environ 34:1415–1430

    Article  PubMed  CAS  Google Scholar 

  • Vogan PJ, Frohlich MW, Sage RF (2007) The functional significance of C3–C4 intermediate traits in Heliotropium L. (Boraginaceae): gas exchange perspectives. Plant Cell Environ 30:1337–1345

    Article  PubMed  CAS  Google Scholar 

  • von Caemmerer S (1989) A model of photosynthetic CO2 assimilation and carbon-isotope discrimination in leaves of certain C3–C4 intermediates. Planta 178:463–474

    Article  Google Scholar 

  • Ward JK, Tissue DT, Thomas RB, Strain RB (1999) Comparative responses of C3 and C4 plants to drought in low and elevated CO2. Glob Change Biol 5:857–867

    Article  Google Scholar 

  • Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451:279–283

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by Discovery grants from the Natural Science and Engineering Research Council of Canada to R.F. Sage. We thank Professor P. Westhoff and Dr. U. Gowik for providing Alternanthera sessilis and A. tenella seeds, and Professor G. Edwards for the gift of Flaveria bidentis seeds.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, ON, N1G 2W1, Canada

    Patrick J. Vogan

  2. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Toronto, ON, M5S 3B2, Canada

    Rowan F. Sage

Authors
  1. Patrick J. Vogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rowan F. Sage
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rowan F. Sage.

Additional information

Communicated by Russell Monson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 376 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vogan, P.J., Sage, R.F. Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis. Oecologia 169, 341–352 (2012). https://doi.org/10.1007/s00442-011-2201-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2201-z

Keywords

Search

Navigation