Oecologia

, Volume 171, Issue 1, pp 71–82 | Cite as

Co-ordination of physiological and morphological responses of stomata to elevated [CO2] in vascular plants

  • Matthew Haworth
  • Caroline Elliott-Kingston
  • Jennifer C. McElwain
Physiological ecology - Original research

Abstract

Plant stomata display a wide range of short-term behavioural and long-term morphological responses to atmospheric carbon dioxide concentration ([CO2]). The diversity of responses suggests that plants may have different strategies for controlling gas exchange, yet it is not known whether these strategies are co-ordinated in some way. Here, we test the hypothesis that there is co-ordination of physiological (via aperture change) and morphological (via stomatal density change) control of gas exchange by plants. We examined the response of stomatal conductance (Gs) to instantaneous changes in external [CO2] (Ca) in an evolutionary cross-section of vascular plants grown in atmospheres of elevated [CO2] (1,500 ppm) and sub-ambient [O2] (13.0 %) compared to control conditions (380 ppm CO2, 20.9 % O2). We found that active control of stomatal aperture to [CO2] above current ambient levels was not restricted to angiosperms, occurring in the gymnosperms Lepidozamia peroffskyana and Nageia nagi. The angiosperm species analysed appeared to possess a greater respiratory demand for stomatal movement than gymnosperm species displaying active stomatal control. Those species with little or no control of stomatal aperture (termed passive) to Ca were more likely to exhibit a reduction in stomatal density than species with active stomatal control when grown in atmospheres of elevated [CO2]. The relationship between the degree of stomatal aperture control to Ca above ambient and the extent of any reduction in stomatal density may suggest the co-ordination of physiological and morphological responses of stomata to [CO2] in the optimisation of water use efficiency. This trade-off between stomatal control strategies may have developed due to selective pressures exerted by the costs associated with passive and active stomatal control.

Keywords

Carbon dioxide Conifer Angiosperm evolution Stomatal conductance Stomatal density Stomatal evolution 

Supplementary material

442_2012_2406_MOESM1_ESM.pdf (13.1 mb)
Supplementary material 1 (PDF 13424 kb)

References

  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedCrossRefGoogle Scholar
  2. Beerling DJ, Chaloner WG (1993) Evolutionary responses of stomatal density to global CO2 change. Biol J Linn Soc 48:343–353Google Scholar
  3. Beerling DJ, Woodward FI (1997) Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record. Bot J Linn Soc 124:137–153Google Scholar
  4. Beerling DJ, McElwain JC, Osborne CP (1998a) Stomatal responses of the ‘living fossil’ Ginkgo biloba L. to changes in atmospheric CO2 concentrations. J Exp Bot 49:1603–1607Google Scholar
  5. Beerling DJ, Woodward FI, Lomas MR, Wills MA, Quick WP, Valdes PJ (1998b) The influence of Carboniferous palaeoatmospheres on plant function: an experimental and modelling assessment. Phil Trans R Soc Lond B 353:131–139CrossRefGoogle Scholar
  6. Belcher CM, Yearsley JM, Hadden RM, McElwain JC, Rein G (2010) Baseline intrinsic flammability of Earth’s ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proc Natl Acad Sci USA 107:22448–22453PubMedCrossRefGoogle Scholar
  7. Bernacchi CJ, Kimball BA, Quarles DR, Long SP, Ort DR (2007) Decreases in stomatal conductance of soybean under open-air elevation of CO2 are closely coupled with decreases in ecosystem evapotranspiration. Plant Physiol 143:134–144PubMedCrossRefGoogle Scholar
  8. Berner RA (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim Cosmochim Acta 70:5653–5664CrossRefGoogle Scholar
  9. Berner RA (2009) Phanerozoic atmospheric oxygen: new results using the geocarbsulf model. Am J Sci 309:603–606CrossRefGoogle Scholar
  10. Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the earth system, past and present. Curr Opin Plant Biol 13:233–240PubMedCrossRefGoogle Scholar
  11. Bettarini I, Vaccari FP, Miglietta F (1998) Elevated CO2 concentrations and stomatal density: observations from 17 plant species growing in a CO2 spring in central Italy. Glob Change Biol 4:17–22CrossRefGoogle Scholar
  12. Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585PubMedCrossRefGoogle Scholar
  13. Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol 183:839–847PubMedCrossRefGoogle Scholar
  14. Chater C et al (2011) Regulatory mechanism controlling stomatal behaviour conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029PubMedCrossRefGoogle Scholar
  15. De Boer HJ, Lammertsma EI, Wagner-Cremer F, Dilcher DL, Wassen MJ, Dekker SC (2011) Climate forcing due to optimization of maximal leaf conductance in subtropical vegetation under rising CO2. Proc Natl Acad Sci USA 108:4041–4046PubMedCrossRefGoogle Scholar
  16. Doi M, Shimazaki K-i (2008) The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiol 147:922–930PubMedCrossRefGoogle Scholar
  17. Doi M, Wada M, Shimazaki K-I (2006) The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant Cell Physiol 47:748–755PubMedCrossRefGoogle Scholar
  18. Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefGoogle Scholar
  19. Feild TS, Zweiniecki MA, Donoghue MJ, Holbrook NM (1998) Stomatal plugs of Drimys winteri (Winteraceae) protect leaves from mist but not drought. Proc Natl Acad Sci USA 95:14256–14259PubMedCrossRefGoogle Scholar
  20. Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347PubMedCrossRefGoogle Scholar
  21. Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol 143:78–87PubMedCrossRefGoogle Scholar
  22. Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philos Trans R Soc Lond B 367:537–546CrossRefGoogle Scholar
  23. Grein M, Konrad W, Wilde V, Utescher T, Roth-Nebelsick A (2011) Reconstruction of atmospheric CO2 during the early middle Eocene by application of a gas exchange model to fossil plants from the Messel Formation, Germany. Palaeogeogr Palaeoclimatol Palaeoecol 309:383–391CrossRefGoogle Scholar
  24. Hammer PA, Hopper DA (1997) Experimental design. In: Langhans RW, Tibbitts TW (eds) Plant growth chamber handbook. Iowa State University, Ames, pp 177–187Google Scholar
  25. Haworth M, Hesselbo SP, McElwain JC, Robinson SA, Brunt JW (2005) Mid-Cretaceous pCO2 based on stomata of the extinct conifer Pseudofrenelopsis (Cheirolepidiaceae). Geology 33:749–752CrossRefGoogle Scholar
  26. Haworth M, Heath J, McElwain JC (2010) Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers. Ann Bot 105:411–418PubMedCrossRefGoogle Scholar
  27. Haworth M, Elliott-Kingston C, McElwain J (2011a) The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167:11–19PubMedCrossRefGoogle Scholar
  28. Haworth M, Elliott-Kingston C, McElwain JC (2011b) Stomatal control as a driver of plant evolution. J Exp Bot 62:2419–2423PubMedCrossRefGoogle Scholar
  29. Haworth M, Fitzgerald A, McElwain JC (2011c) Cycads show no stomatal density and index response to elevated carbon dioxide and sub-ambient oxygen. Aust J Bot 59:629–638CrossRefGoogle Scholar
  30. Heath OVS (1950) Studies in stomatal behaviour. V. The role of carbon dioxide in the light response of stomata. J Exp Bot 1:29–62CrossRefGoogle Scholar
  31. Heimhofer U, Hochuli PA, Burla S, Dinis JML, Weissert H (2005) Timing of Early Cretaceous angiosperm diversification and possible links to major paleoenvironmental change. Geology 33:141–144CrossRefGoogle Scholar
  32. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedCrossRefGoogle Scholar
  33. Hirano A, Hongo I, Koike T (2012) Morphological and physiological responses of Siebold’s beech (Fagus crenata) seedlings grown under CO2 concentrations ranging from pre-industrial to expected future levels. Landscape Ecol Eng 8:59–67CrossRefGoogle Scholar
  34. Hu H et al (2010) Carbonic anhydrases are upstream regulators of CO2 controlled stomatal movements in guard cells. Nat Cell Biol 12:87–93PubMedCrossRefGoogle Scholar
  35. Kouwenberg LLR et al. (2003) Stomatal frequency adjustment of four conifer species to historical changes in atmospheric CO2. Am J Bot 90:610–619Google Scholar
  36. Kürschner WM, Wagner F, Visscher EH, Visscher H (1997) Predicting the response of leaf stomatal frequency to a future CO2-enriched atmosphere: constraints from historical observations. Geol Rundsch 86:512–517CrossRefGoogle Scholar
  37. Kürschner 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 105:449–453PubMedCrossRefGoogle Scholar
  38. Lammertsma EI, Boer HJD, Dekker SC, Dilcher DL, Lotter AF, Wagner-Cremer F (2011) Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation. Proc Natl Acad Sci USA 108:4035–4040PubMedCrossRefGoogle Scholar
  39. Levine LH, Richards JT, Wheeler RM (2009) Super-elevated CO2 interferes with stomatal response to ABA and night closure in soybean (Glycine max). J Plant Physiol 166:903–913PubMedCrossRefGoogle Scholar
  40. Marler TE, Willis LE (1997) Leaf gas-exchange characteristics of sixteen cycad species. J Am Soc Hortic Sci 122:38–42Google Scholar
  41. Mawson BT (1993) Modulation of photosynthesis and respiration in guard and mesophyll cell protoplasts by oxygen concentration. Plant Cell Environ 16:207–214CrossRefGoogle Scholar
  42. McAdam SAM, Brodribb TJ (2012) Stomatal innovation and the rise of seed plants. Ecol Lett 15:1–8PubMedCrossRefGoogle Scholar
  43. McAdam SAM, Brodribb TJ, Ross JJ, Jordan GJ (2011) Augmentation of abscisic acid (ABA) levels by drought does not induce short-term stomatal sensitivity to CO2 in two divergent conifer species. J Exp Bot 62:195–203PubMedCrossRefGoogle Scholar
  44. McElwain JC, Willis KJ, Lupia R (2004) Cretaceous CO2 decline and the radiation and diversification of angiosperms. In: Ehleringer JR, Dearing MD, Cerling T (eds) History of Atmospheric CO2 and Implications on plants animals and ecosystems. Springer, New YorkGoogle Scholar
  45. Meidner H (1968) The comparative effects of blue and red light on the stomata of Allium cepa L. and Xanthium pennsylvanicum. J Exp Bot 19:146–151CrossRefGoogle Scholar
  46. Miller-Rushing AJ, Primack RB, Templer PH, Rathbone S, Mukunda S (2009) Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees. Am J Bot 96:1779–1786PubMedCrossRefGoogle Scholar
  47. Miziorko HM, Llorimer GH (1983) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem 52:507–535PubMedCrossRefGoogle Scholar
  48. Parsons R, Weyers JDB, Lawson T, Godber IM (1998) Rapid and straightforward estimates of photosynthetic characteristics using a portable gas exchange system. Photosynthetica 34:265–279CrossRefGoogle Scholar
  49. Passalia MG (2009) Cretaceous pCO2 estimation from stomatal frequency analysis of gymnosperm leaves of Patagonia, Argentina. Palaeogeogr Palaeoclimatol Palaeoecol 273:17–24CrossRefGoogle Scholar
  50. Poole I, Kürschner WM (1999) Stomatal density and index: the practise. In: Jones TP, Rowe NP (eds) Fossil plants and spores: modern techniques. Geological Society, London, pp 257–260Google Scholar
  51. Raghavendra AS (1981) Energy supply for stomatal opening in epidermal strips of Commelina benghalensis. Plant Physiol 67:385–387PubMedCrossRefGoogle Scholar
  52. Reid CD, Maherali H, Johnson HB, Smith SD, Wullschleger SD, Jackson RB (2003) On the relationship between stomatal characters and atmospheric CO2. Geophys Res Lett 30:1983–1986CrossRefGoogle Scholar
  53. Robinson JM (1994) Speculations on carbon dioxide starvation, late Tertiary evolution of stomatal regulation and floristic modernization. Plant Cell Environ 17:345–354CrossRefGoogle Scholar
  54. Roth-Nebelsick A, Grein M, Utescher T, Konrad W (2012) Stomatal pore length change in leaves of Eotrigonobalanus furcinervis (Fagaceae) from the Late Eocene to the Latest Oligocene and its impact on gas exchange and CO2 reconstruction. Rev Palaeobot Palynol 174:106–112CrossRefGoogle Scholar
  55. Royer DL et al (2001) Paleobotanical evidence for near present-day levels of atmospheric CO2 during part of the Tertiary. Science 292:2310–2313PubMedCrossRefGoogle Scholar
  56. Ruszala EM et al (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21:1030–1035PubMedCrossRefGoogle Scholar
  57. Sager JC, McFarlane JC (1997) Radiation. In: Langhans RW, Tibbitts TW (eds) Plant Growth Chamber Handbook. Iowa State University, Ames, pp 1–30Google Scholar
  58. Smith RY, Greenwood DR, Basinger JF (2010) Estimating paleoatmospheric pCO2 during the Early Eocene Climatic Optimum from stomatal frequency of Ginkgo, Okanagan Highlands, British Columbia, Canada. Palaeogeogr Palaeoclimatol Palaeoecol 293:120–131CrossRefGoogle Scholar
  59. Srivastava A, Lu ZM, Zeiger E (1995) Modification of guard cell properties in advanced lines of Pima cotton bred for higher yields and heat-resistance. Plant Sci 108:125–131CrossRefGoogle Scholar
  60. Stults DZ, Wagner-Cremer F, Axsmith BJ (2011) Atmospheric palaeo-CO2 estimates based on Taxodium distichum (Cupressaceae) fossils from the Miocene and Pliocene of Eastern North America. Palaeogeogr Palaeoclimatol Palaeoecol 309:327–332CrossRefGoogle Scholar
  61. Wagner F et al (1996) A natural experiment on plant acclimation: lifetime stomatal frequency response of an individual tree to annual atmospheric CO2 increase. Proc Natl Acad Sci USA 93:11705–11708PubMedCrossRefGoogle Scholar
  62. Walker DA, Zelitch I (1963) Some effects of metabolic inhibitors, temperature, and anaerobic conditions on stomatal movement. Plant Physiol 38:390PubMedCrossRefGoogle Scholar
  63. Weyers JDB, Lawson LG (1985) Accurate estimation of stomatal aperture from silicone rubber impressions. New Phytol 101:109–115CrossRefGoogle Scholar
  64. Wheeler RM, Mackowiak CL, Yorio NC, Sager JC (1999) Effects of CO2 on stomatal conductance: do stomata open at very high CO2 concentrations? Ann Bot 83:243–251PubMedCrossRefGoogle Scholar
  65. Willmer CM, Mansfield TA (1970) Effects of some metabolic inhibitors and temperature on ion-stimulated stomatal opening in detached epidermis. New Phytol 69:983–992CrossRefGoogle Scholar
  66. Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from preindustrial levels. Nature 327:617–618CrossRefGoogle Scholar
  67. Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Matthew Haworth
    • 1
  • Caroline Elliott-Kingston
    • 2
  • Jennifer C. McElwain
    • 2
  1. 1.CNRIstituto di Biometeorologia (IBIMET)FlorenceItaly
  2. 2.School of Biology and Environmental ScienceUniversity College DublinDublin 4Ireland

Personalised recommendations