Redundant roles of photoreceptors and cytokinins in regulating photosynthetic acclimation to canopy density

Abstract

The regulation of photosynthetic acclimation to canopy density was investigated in tobacco canopies and in tobacco and Arabidopsis plants with part of their foliage experimentally shaded. Both species acclimated to canopy light gradients and partial shading by allocating photosynthetic capacity to leaves in high light and adjusting chloroplast organization to the local light conditions. An investigation was carried out to determine whether signalling mediated by photoreceptors, sugars, cytokinin, and nitrate is involved in and necessary for proper photosynthetic acclimation. No evidence was found for a role for sugars, or for nitrate. The distribution of cytokinins in tobacco stands of contrasting density could be explained in part by irradiance-dependent delivery of cytokinins through the transpiration stream. Functional studies using a comprehensive selection of Arabidopsis mutants and transgenics showed that normal wild-type responses to partial shading were retained when signalling mediated by photoreceptors or cytokinins was disrupted. This indicates that these pathways probably operate in a redundant manner. However, the reduction of the chlorophyll a/b ratio in response to local shade was completely absent in the Arabidopsis Ws-2 accession mutated in PHYTOCHROME D and in the triple phyAphyCphyD mutant. Moreover, cytokinin receptor mutants also showed a reduced response, suggesting a previously unrecognized function of phyD and cytokinins.

Fig. 1.

Canopy density effects on putative signal parameters and photosynthetic acclimation in tobacco. Shown are PPFD (A), R: FR (B), soluble sugars (C), and nitrate (D), photosynthetic capacity per unit chlorophyll (A_max/Chl) (E) and the chlorophyll a/b ratio (Chl a/b) (F) measured in open (3.6 plants m⁻²) and dense (35 plants m⁻²) tobacco canopies at three heights representative for maximal, intermediate, and minimal irradiance in each stand. Data are means±SE, n=6–12. Note the log-scale on the y-axis in A and B.

Fig. 2.

Effects of shading a single leaf of a plant on putative signals and photosynthetic acclimation in tobacco (A, C, E, G, H, I) and Arabidopsis (B, D, F, H, J). Shown are soluble sugars (A, B), nitrate (C, D), photosynthetic capacity per unit chlorophyll (A_max/Chl) (E, F), chlorophyll a/b ratio (Chl a/b) (G, H), and photosynthetic capacity per unit area (A_max) (I). One attached leaf was shaded (PPFD ∼14 μmol m⁻² s⁻¹; low light, LL) for 5–6 d and compared with a leaf on a different plant that remained in the light (PPFD ∼200 μmol m⁻² s⁻¹; high light, HL). Data are means±SE, n=2–6. *, P <0.05 (Student's t-test).

Fig. 3.

Effects of shading a single leaf of a plant on photosynthetic acclimation in Arabidopsis mutants and transgenics disrupted in signalling mediated by cytokinin, photoreceptors, or sugars. Shown are the light-saturated rate of electron transport per unit area (ETR_max) (A) and chlorophyll a/b ratio (Chl a/b) (B). One attached leaf was shaded (PPFD ∼14 μmol m⁻² s⁻¹; low light, LL) for 6 d and compared with a leaf on a different plant that remained in the light (PPFD ∼200 μmol m⁻² s⁻¹; high light, HL). The Chl a/b of hy2 in HL was 6.22±0.198. Shading induced significant (P <0.05; Student's t-test) decreases in ETR_max in all genotypes tested. Data are means±SE, n=6. In B, NS, not significant; *, P < 0.1; **, P <0.05 (Student's t-test).

Fig. 4.

Effects of experimental reduction of the transpiration rate on chloroplast-level acclimation in Arabidopsis. One attached leaf was placed in a cuvette flushed with humid air or with growth chamber air (dry) as a control for 6 d. Shown are photosynthetic capacity per unit chlorophyll (A_max/Chl) (A) and chlorophyll a/b ratio (Chl a/b) (B). Data are means±SE, n=6. *P <0.05; (Student's t-test).