Photoacoustic Analysis Indicates That Chloroplast Movement Does Not Alter Liquid-Phase CO2 Diffusion in Leaves of Alocasia brisbanensis    

Abstract

Light-mediated chloroplast movements are common in plants. When leaves of Alocasia brisbanensis (F.M. Bailey) Domin are exposed to dim light, mesophyll chloroplasts spread along the periclinal walls normal to the light, maximizing absorbance. Under high light, the chloroplasts move to anticlinal walls. It has been proposed that movement to the high-light position shortens the diffusion path for CO 2 from the intercellular air spaces to the chloroplasts, thus reducing CO 2 limitation of photosynthesis. To test this hypothesis, we used pulsed photoacoustics to measure oxygen diffusion times as a proxy for CO 2 diffusion in leaf cells. We found no evidence that chloroplast movement to the high-light position enhanced gas diffusion. Times for oxygen diffusion were not shorter in leaves pretreated with white light, which induced chloroplast movement to the high-light position, compared with leaves pretreated with 500 to 700 nm light, which did not induce movement. From the oxygen diffusion time and the diffusion distance from chloroplasts to the intercellular gas space, we calculated an oxygen permeability of 2.25 ϫ 10 Ϫ6 cm 2 s Ϫ1 for leaf cells at 20°C. When leaf temperature was varied from 5°C to 40°C, the permeability for oxygen increased between 5°C and 20°C but changed little between 20°C and 40°C, indicating changes in viscosity or other physical parameters of leaf cells above 20°C. Resistance for CO 2 estimated from oxygen permeability was in good agreement with published values, validating photoacoustics as another way of assessing internal resistances to CO 2 diffusion.Light-mediated chloroplast movements in the leaves of some plants are so striking that they create patterns visible to the naked eye. They have attracted the attention of plant physiologists for more than a century. Chloroplast movements of all types have been the subject of numerous reviews (Britz, 1979; Haupt and Scheuerlein, 1990; Wada et al., 1993; Yatsuhashi, 1996; Haupt, 1999; Wada and Kagawa, 2001; Kagawa and Wada, 2002). In leaves, chloroplasts spread along the periclinal walls of mesophyll cells (the face position) in low light, whereas in high light, they move toward the anticlinal walls (the profile position), effectively forming cylinders of chloroplasts in palisade tissue. In darkness, the chloroplasts are generally in an intermediate position, although this varies among species (Inoue and Shibata, 1974) and depends on the growth environment (Trojan and Gabrys, 1996). Because of the optical sieve effect (Britz and Briggs, 1987), these marked chloroplast movements alter light absorption (Zurzycki, 1961), which, in many leaves, gives rise to the visible color changes that have attracted attention for so long.Chloroplast movements are widespread in algae, mosses, ferns, and seed plants. Among seed plants, they are common in both monocots and dicots, and they occur in plants with widely differing leaf anatomy, from submerged aquatic plants (Zurzycki and Lelatko, 1969) to sclerophyllous evergreens (Del Hierro et al., 2000). Chl...

Chloroplast Photorelocation Movement: A Sophisticated Strategy for Chloroplasts to Perform Efficient Photosynthesis

“…This group measured oxygen diffusion times using pulsed photoacoustics (as a substitution for CO 2 diffusion) between control and strong lightirradiated Alocasia leaf samples, but they could not find any differences in CO 2 diffusion rates between the two samples (Gorton et al, 2003). Additionally, they could found no difference in the distance between the centers of the chloroplasts and the closest air spaces between two samples (Gorton et al, 2003). Another group found that blue light rapidly reduced CO 2 diffusion from intercellular air spaces to the chloroplasts in both Nicotiana and Platanus leaves and that this reduction was completed before chloroplasts finished the avoidance movement to the aniticlinal walls (Loreto et al, 2009).…”

“…Senn (1908) hypothesized that this positioning might result from the chemotaxis of chloroplasts to the CO 2 in air spaces. Using different approaches and plant species, three groups examined whether chloroplast photorelocation movement, especially the avoidance response, influenced CO 2 diffusion in leaves (Gorton et al, 2003;Loreto et al, 2009;Tholen et al, 2008). One research group hypothesized that chloroplast distribution on the anticlinal walls by the avoidance response facilitated CO 2 utilization by shortening the CO 2 diffusion path length from air spaces to the mesophyll chloroplasts (Gorton et al, 2003).…”

“…Collectively, these results suggested that the chloroplast avoidance response was not involved in CO 2 diffusion or that it possibly decreased, rather than increased, the diffusion rate. However, these three groups examined the contribution of chloroplast movement to CO 2 diffusion using different plant species and techniques: pulsed photoacoustics (Gorton et al, 2003), a chlorophyll fluorescence-based method (Loreto et al, 2009) and a carbon isotope discrimination method (Tholen et al, 2008). The examination of one plant species using different techniques and/or that of various plant species by one technique are required to uncover whether chloroplast photorelocation movement influences CO 2 diffusion.…”

“…One research group hypothesized that chloroplast distribution on the anticlinal walls by the avoidance response facilitated CO 2 utilization by shortening the CO 2 diffusion path length from air spaces to the mesophyll chloroplasts (Gorton et al, 2003). This group measured oxygen diffusion times using pulsed photoacoustics (as a substitution for CO 2 diffusion) between control and strong lightirradiated Alocasia leaf samples, but they could not find any differences in CO 2 diffusion rates between the two samples (Gorton et al, 2003). Additionally, they could found no difference in the distance between the centers of the chloroplasts and the closest air spaces between two samples (Gorton et al, 2003).…”

“…Using different approaches and plant species, three groups examined whether chloroplast photorelocation movement, especially the avoidance response, influenced CO 2 diffusion in leaves (Gorton et al, 2003;Loreto et al, 2009;Tholen et al, 2008). One research group hypothesized that chloroplast distribution on the anticlinal walls by the avoidance response facilitated CO 2 utilization by shortening the CO 2 diffusion path length from air spaces to the mesophyll chloroplasts (Gorton et al, 2003). This group measured oxygen diffusion times using pulsed photoacoustics (as a substitution for CO 2 diffusion) between control and strong lightirradiated Alocasia leaf samples, but they could not find any differences in CO 2 diffusion rates between the two samples (Gorton et al, 2003).…”