Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration

Implications for the evolution of stomatal behaviour

Travis E. Huxman, Russell Monson

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

Stomatal function mediates physiological trade-offs associated with maintaining a favourable H2O balance in leaf tissues while acquiring CO2 as a photosynthetic substrate. The C3 and C4 species appear to have different patterns of stomatal response to changing light conditions, and variation in this behaviour may have played a role in the functional diversification of the different photosynthetic pathways. In the current study, we used gain analysis theory to characterize the stomatal conductance response to light intensity in nine different C3, C4 and C3-C4 intermediate species Flaveria species. The response of stomatal conductance (gs) to a change in light intensity represents both a direct (related to a change in incident light intensity, I) and indirect (related to a change in intercellular CO2 concentration, Ci) response. The slope of the line relating the change in gs to Ci was steeper in C4 species, compared with C3 species, with C3-C4 species having an intermediate response. This response reflects the greater relative contribution of the indirect versus direct component of the gs versus I response in the C4 species. The C3-C4 species, Flaveria floridana, exhibited a C4-like response whereas the C3-C4 species, Flaveria sonorensis and Flaveria chloraefolia, exhibited C3-like responses, similar to their hypothesized position along the evolutionary trajectory of the development of C4 photosynthesis. There was a positive correlation between the relative contribution of the indirect component of the gs versus I response and water use efficiency when evaluated across all species. Assuming that the C3-C4 intermediate species reflect an evolutionary progression from fully expressed C3 ancestors, the results of the current study demonstrate an increase in the contribution of the indirect component of the gs versus I response as taxa evolve toward the C4 extreme. The greater relative contribution of the indirect component of the stomatal response occurs through both increases in the indirect stomatal components and through decreases in the direct. Increases in the magnitude of the indirect component may be related to the maintenance of higher water use efficiencies in the intermediate evolutionary stages, before the appearance of fully integrated C4 photosynthesis.

Original languageEnglish (US)
Pages (from-to)313-322
Number of pages10
JournalPlant, Cell and Environment
Volume26
Issue number2
DOIs
StatePublished - Feb 1 2003
Externally publishedYes

Fingerprint

Flaveria
C4 plants
Light
Photosynthesis
light intensity
C4 photosynthesis
C3 plants
water use efficiency
stomatal conductance
Water
trajectories
ancestry

Keywords

  • CO feedback
  • Gain analysis
  • Gas exchange
  • Light response
  • Photosynthesis
  • Water use efficiency

ASJC Scopus subject areas

  • Plant Science

Cite this

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title = "Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: Implications for the evolution of stomatal behaviour",
abstract = "Stomatal function mediates physiological trade-offs associated with maintaining a favourable H2O balance in leaf tissues while acquiring CO2 as a photosynthetic substrate. The C3 and C4 species appear to have different patterns of stomatal response to changing light conditions, and variation in this behaviour may have played a role in the functional diversification of the different photosynthetic pathways. In the current study, we used gain analysis theory to characterize the stomatal conductance response to light intensity in nine different C3, C4 and C3-C4 intermediate species Flaveria species. The response of stomatal conductance (gs) to a change in light intensity represents both a direct (related to a change in incident light intensity, I) and indirect (related to a change in intercellular CO2 concentration, Ci) response. The slope of the line relating the change in gs to Ci was steeper in C4 species, compared with C3 species, with C3-C4 species having an intermediate response. This response reflects the greater relative contribution of the indirect versus direct component of the gs versus I response in the C4 species. The C3-C4 species, Flaveria floridana, exhibited a C4-like response whereas the C3-C4 species, Flaveria sonorensis and Flaveria chloraefolia, exhibited C3-like responses, similar to their hypothesized position along the evolutionary trajectory of the development of C4 photosynthesis. There was a positive correlation between the relative contribution of the indirect component of the gs versus I response and water use efficiency when evaluated across all species. Assuming that the C3-C4 intermediate species reflect an evolutionary progression from fully expressed C3 ancestors, the results of the current study demonstrate an increase in the contribution of the indirect component of the gs versus I response as taxa evolve toward the C4 extreme. The greater relative contribution of the indirect component of the stomatal response occurs through both increases in the indirect stomatal components and through decreases in the direct. Increases in the magnitude of the indirect component may be related to the maintenance of higher water use efficiencies in the intermediate evolutionary stages, before the appearance of fully integrated C4 photosynthesis.",
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