The Coleoptile Chloroplast
Guard cell chloroplasts are a conspicuous structural feature of guard cells (see textbook Figure 10.1), and their physiology and biochemistry have been studied for several decades. In contrast, the chloroplasts of phototropically sensitive coleoptiles have only recently been analyzed in detail. The coleoptile chloroplast had been suggested as a possible site for photoreception in oat coleoptiles by Kenneth V. Thimann and his coworkers in 1960, but interest in the flavin hypothesis later in that decade shifted attention away from coleoptile chloroplasts and these organelles have been virtually ignored for several decades.
Recent studies have shown that the coleoptile chloroplast evolves oxygen, fixes CO2 photosynthetically, and operates the xanthophyll cycle (Zhu et al. 1995). Dark-grown, etiolated coleoptile tips have violaxanthin and antheraxanthin but no zeaxanthin, and they accumulate zeaxanthin when irradiated (Quiñones and Zeiger 1994).
When dark-grown coleoptiles are pretreated with red light for different lengths of time, their zeaxanthin content is proportional to the length of the red-light treatment (Web Figure 10.3.A). Exposure of coleoptiles with different zeaxanthin content to a brief pulse of blue light elicitis phototropic bending that is linearly related to the zeaxanthin content of the coleoptiles (see Web Figure 10.3.A). Most interestingly, the regression line through the data points extrapolates to zero (see Web Figure 10.3.A, part 1), suggesting that there is no phototropic response in the absence of zeaxanthin (Quiñones and Zeiger 1994).
Web Figure 10.3.A The relationship between the zeaxanthin content of corn coleoptile tips and bending in response to a pulse of blue light. Zeaxanthin content was altered by preillumination time under red light (1), transfer of zeaxanthin-containing coleoptiles to the dark (2), and a saturating red-light pretreatment in the presence of increasing concentrations of DTT, an inhibitor of zeaxanthin formation (3). (After Quiñones and Zeiger 1994.)
Red light–treated coleoptiles with a high zeaxanthin content convert their zeaxanthin to violaxanthin when transferred to the dark. Phototropic bending in response to a pulse of blue light given at different time intervals after the transfer to the dark is linearly related to zeaxanthin content (see Web Figure 10.3.A, part 2).
When corn coleoptiles are given a saturating red-light pretreatment and a blue-light pulse in the presence of increasing concentrations of DTT (an inhibitor of zeaxanthin formation), bending and zeaxanthin content decrease linearly as a function of DTT concentration (see Web Figure 10.3.A, part 3).
Thus the relationship between the zeaxanthin content of coleoptile chloroplasts and blue light–dependent phototropic sensitivity is very similar to the relationship between the zeaxanthin content of the guard cell chloroplast and the blue-light sensitivity of stomatal opening.
Coleoptile and guard cell chloroplasts share some properties that are clearly distinct from mesophyll chloroplasts, including high rates of oxygen evolution and low rates of photosynthetic carbon fixation, a high sensitivity of their xanthophyll cycle to low levels of incident photon fluxes, and a high starch content (Zhu et al. 1995). The coleoptile and guard cell chloroplasts also show a specific blue light response with an action spectrum that closely matches the action spectra for blue light–stimulated stomatal opening and coleoptile phototropism (Quiñones et al. 1996).
These remarkable similarities suggest that these distinct characteristics are typical of chloroplasts specialized in signal transduction, as opposed to the classic role of the mesophyll chloroplast, specialized in photosynthetic carbon fixation.