How Plants Find Light in Patchy Canopies. A Comparison between Wild-Type and Phytochrome-B-Deficient Mutant Plants of Cucumber

Abstract

We address the following questions : (a) do plants that colonize horizontally-patchy environments preferentially project leaf area into light gaps and avoid poorly illuminated sites ? (b) is this 'foraging' ability impaired in plants that lack phytochrome B, one of the plants' information-acquiring photoreceptors ? We used cucumber (Cucumis sativus L.) plants as test material and our approach was based on studies of the dynamics of gap colonization by wild-type (WT) and lh-mutant plants. The lh mutant lacks phytochrome B but has WT levels of phytochrome A. When de-etiolated, lh seedlings show reduced or no response to alterations of the red (R) to far-red (FR) ratio of the incident light, one of the environmental factors that plants use to monitor the proximity of other plants. Controlled-environment experiments showed that seedlings of both genotypes are able to sense irradiance gradients and actively project nodes towards light gaps via phototropic (stem-bending) responses. A mechanism independent of phytochrome B also appeared to control the angle of display of individual leaves with respect to the direction of illumination. However, when compared over periods of several weeks, WT plants were far more efficient than lh mutants at invading light gaps. Thus, WT plants grown in the field for 4 weeks at the edges of an experimental maize canopy projected outside the canopy nearly all the nodes produced. In contrast, ∼50% of the nodes and more than 80% of the apical buds of lh mutant plants were deployed under the maize canopy. The lower ability of the phytochrome B-deficient lh mutant to 'forage' for light, compared with WT plants, appears to be the integrated product of a lower capacity to locate light gaps (owing to the lack of R :FR-driven phototropism) and a lower capacity to retain modules into high-light patches. In relation to the latter, lh shoots exposed to high R :FR ratios (simulated gap-light) retain a phenotype characterized by long inter-nodes and high apical dominance, two features that would increase the likelihood of exiting light gaps. We show that shoots of mature WT plants grown under high R :FR ratio are diagravitropic, whereas lh shoots are orthogravitropic. The diagravitropic habit, coupled with an efficient phototropic system, appears to help WT shoots to escape from the shaded sectors and invade light gaps. Compared with lh plants, WT plants grown under high R :FR have delayed tendril production and reduced stem-bending responses to mechanical stress exerted by tendrils. These two factors combine with the ones listed above to cause the direction of shoot spreading in WT plants to be dictated mainly by the spatial distribution of light gaps and not by the distribution of potential points of support for tendril attachment.