The guard cell chloroplast: a perspective for the twenty‐first century

Abstract

SummaryThe guard cell chloroplast is the site of perception of blue light and of photosynthetically active radiation, and of at least one of the mechanisms sensing CO 2 in the guard cell. The guard cell chloroplast has been the focus of intense controversy over its capacity for light sensing and photosynthetic carbon fixation, and the osmoregulatory mechanisms mediating stomatal movements. It is argued here that a primary reason behind these long-lived controversies is the remarkable plasticity of the guard cell, which has resulted in responses being generalized as basic properties when opposite responses appear to be the norm under different environmental or experimental conditions. Examples of guard cell plasticity are described, including variation of chlorophyll fluorescence transients over a daily course, acclimation of the guard cell responses to blue light and CO 2 , the shift from potassium to sucrose in daily courses of osmoregulation and the transduction of red light into different osmoregulatory pathways. Recent findings on the properties of the guard cell chloroplast are also presented, including the role of the chloroplastic carotenoid, zeaxanthin, in blue light photoreception, the blue-green reversibility of stomatal movements, and the involvement of phytochrome in the stomatal response to light in the orchid, Paphiopedilum .© New Phytologist (2002 ) 153 : 415 -424

Evidence for Involvement of Photosynthetic Processes in the Stomatal Response to CO2

“…Zeaxanthin, one of the putative BL receptors in guard cells is another possibility. The equilibrium for interconversion of violaxanthin and zeaxanthin depends on thylakoid pH, which in turn depends on the balance between the light reactions and the carbon reactions in photosynthesis (Zeiger et al, 2002). Our data do not appear to rule out guard cell chloroplastic zeaxanthin, ATP, or any other photosynthetic intermediary, nor do they indicate clearly that the putative sensor is located in mesophyll or guard cells.…”

“…It is worth noting the existence of a third hypothesis concerning guard cell photosynthesis and g s . This hypothesis holds that the Calvin cycle generates Suc or other osmotica within guard cells, driving osmotic swelling and stomatal opening in RL, or more generally in PAR (Zeiger et al, 2002;Outlaw, 2003). However, in contrast to observations, this mechanism predicts greater stomatal opening under elevated c i .…”

“…Another possibility is that the c i response involves C 3 photosynthetic processes in guard cells. It now seems clear that the Calvin cycle and photosynthetic electron transport are operational in guard cell chloroplasts (see Zeiger et al, 2002;Vavasseur and Raghavendra, 2005) and that these two processes can occur at similar relative rates in guard and mesophyll cells (Cardon and Berry, 1992;Lawson et al, 2002). These results form the basis for two hypotheses that link guard cell photosynthesis with the stomatal responses to light and c i .…”

“…In addition, the action spectra for mesophyll photosynthesis and for the stomatal response to RL are similar to one another (Sharkey and Raschke, 1981a), and the RL response is abolished by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), a PSII inhibitor (Sharkey and Raschke, 1981b;Schwartz and Zeiger, 1984;Tominaga et al, 2001;Olsen et al, 2002). For these reasons, chlorophyll is commonly assumed to be the RL receptor (Assmann and Shimazaki, 1999;Zeiger et al, 2002). Despite the accumulation of evidence showing that guard cells respond directly to RL, this conclusion has recently been challenged based on electrophysiological measurements of the guard cell plasma membrane (Roelfsema et al, 2002).…”

“…The first of these hypotheses (Zeiger et al, 2002;Outlaw, 2003) is an extension of the zeaxanthin hypothesis for the BL response . Zeaxanthin functions in nonphotochemical quenching.…”