The Control of Transpiration. Insights from Arabidopsis

Abstract

Stomatal complexes in the epidermes of aerial plant parts are critical sites for the regulation of gas exchange between the plant and the atmosphere. Stomata consist of microscopic pores, each flanked by a pair of guard cells. Guard cells can increase or decrease the size of the pore via changes in their turgor status, hence regulating both CO2 entry into the leaf and transpiration, or the loss of water from the leaf. This Update focuses on recent progress in our understanding of the regulation of transpiration and drought tolerance that has been garnered through the use of Arabidopsis (Arabidopsis thaliana) as a model experimental system. The coordinated regulation of gas exchange is integral to land plant survival because CO2 must be able to penetrate the leaf to allow photosynthesis, yet water loss (transpiration) must be minimized to prevent desiccation, drought stress, and plant death. Transpiration also provides the driving force for the transport of water and nutrients from the roots to the aerial tissues, and the evaporation of water from the substomatal cavity cools the plant (Lambers et al., 1998). While a number of morphological traits can contribute to the overall level of leaf gas exchange (e.g. the density and distribution of stomata, leaf epidermal structure and internal organization, cuticle thickness), the regulation of stomatal aperture size is unique in that it is a dynamic and reversible process by which water loss and CO2 influx can be rapidly fine tuned in response to a number of environmental and intrinsic signals, such as light, CO2, and the plant stress hormone abscisic acid (ABA; Schroeder et al., 2001). Because guard cells integrate and respond to a plethora of signals, they have become a model cell type in the field of plant cell signaling (Blatt, 2000; Schroeder et al., 2001; Roelfsema and Hedrich, 2005). This Update highlights recent research reports on the guard cell physiology of Arabidopsis that include some quantitative measure of stomatal function. These measures include transpiration, stomatal conductance (stomatal conductance is defined as stomatal transpiration divided by the vapor pressure difference between the leaf and the air, and increases with increasing stomatal aperture), leaf water status, and water-use efficiency/transpiration efficiency (the ratio of photosynthetic assimilation to transpiration). By focusing the article in this manner, we hope to promote the synthesis of ideas and approaches between whole-plant physiologists and molecular biologists/geneticists. The former typically measure stomatal regulation of gas exchange and its impact on whole-plant physiology, and may treat the cellular and molecular biology of guard cells as a “black box” that receives and reacts to inputs. The latter typically use model plant species to investigate cell and molecular regulation of guard cell function, and may employ gene expression, stomatal aperture, or a specific guard cell parameter, such as ion fluxes, as a “readout,” without quantifying alterations in gas exchange and concomitant whole-plant impacts. Our premise is that Arabidopsis is an excellent reference plant in which these complementary approaches can be readily combined, and that such an integrated approach has great potential to yield new insights into the biology of transpiration in C3 angiosperms. Arabidopsis is a powerful biological tool for the identification and characterization of the molecular regulators of transpiration because it has a small, sequenced genome and is easy to transform. These characteristics allow researchers to experimentally modulate the levels of candidate regulatory molecules via techniques such as RNA interference, insertional mutagenesis, or genetic overexpression, and many studies that employ such tools are discussed in the following sections. Additionally, the availability of collections of genetic mutants allows for large-scale screens for potential regulators of transpiration and for functional analyses of candidate regulators. For example, one such screen used infrared thermography to detect differences in leaf temperature, a correlate of transpiration, among a collection of Arabidopsis mutants (Merlot et al., 2002; Wang et al., 2004). The screen identified two novel mutations in stomatal regulation, ost1 and ost2; OST1 has been cloned and identified as encoding an Arabidopsis homolog of an ABA-activated protein kinase first identified in Vicia faba and is discussed further below (Li et al., 2000; Mustilli et al., 2002). Quantitative trait loci (QTL) analysis is an alternative to mutant analysis that harnesses naturally occurring variation within a species to identify putative genes and genomic regions involved in the regulation of quantitative traits such as transpiration (Alonso-Blanco and Koornneef, 2000). QTL mapping involves the generation of a segregating population for a particular trait, often either an F2 population or a population of homozygous recombinant inbr