Multiple Pathways in the Control of the Shade Avoidance Response

Abstract

To detect the presence of neighboring vegetation, shade-avoiding plants have evolved the ability to perceive and integrate multiple signals. Among them, changes in light quality and quantity are central to elicit and regulate the shade avoidance response. Here, we describe recent progresses in the comprehension of the signaling mechanisms underlying the shade avoidance response, focusing on Arabidopsis, because most of our knowledge derives from studies conducted on this model plant. Shade avoidance is an adaptive response that results in phenotypes with a high relative fitness in individual plants growing within dense vegetation. However, it affects the growth, development, and yield of crops, and the design of new strategies aimed at attenuating shade avoidance at defined developmental stages and/or in specific organs in high-density crop plantings is a major challenge for the future. For this reason, in this review, we also report on recent advances in the molecular description of the shade avoidance response in crops, such as maize and tomato, and discuss their similarities and differences with Arabidopsis.

Keywords: Arabidopsis; HD-Zip transcription factors; auxin; light environment; photoreceptors.

Figure 1

Shade avoidance phenotypes in Arabidopsis seedlings. Seedlings were grown for four days in high red (R)/far-red (FR) _{High PAR} and then either maintained in the same light regime or transferred to low R/FR _{Low PAR} for six days in a 16-h light/8-h dark photoperiod to simulate, respectively, sunlight and shade. Light outputs were as previously reported [9]. Scale bar, 2 mm.

Figure 2

Regulatory routes in the shade avoidance response. Changes in R/FR light causing a shift in the equilibrium between Pr and the FR light-absorbing photo-convertible isoform (Pfr) toward the R light-absorbing photo-convertible isoform (Pr) result in the deactivation of phyB, phyD, and phyE. This, in turn, results in the enhanced stability and/or activity of several phytochrome-interacting transcription factors (PIFs). PIFs, within a few minutes, activate the transcription of HD-Zips II, YUCs, and HFR1/SICS1 genes, encoding positive and negative regulators of shade avoidance, respectively. HFR1/SICS1 form non-functional heterodimers with PIF proteins, thereby inhibiting their activity. Shade avoidance is counteracted by the action of phyA, which positively regulates HY5, a central regulator of seedling photomorphogenesis. phyA and phyB oppositely affect the activity of COP1/SPA complexes.

Figure 3

Shade affects adaxial epidermal cell expansion in the Arabidopsis leaf. (A) Dark-field images of cleared first/second leaves of wild type grown for eight days in high R/FR _{High PAR} (high R/FR _{High PAR}), or for four days in high R/FR _{High PAR} and then for 5.5 days in low R/FR _{Low PAR} (low R/FR _{Low PAR}), respectively. The insets show a paradermal view of leaf adaxial epidermis; the borders of a few cells have been highlighted manually with a blue line. Light outputs were as previously reported [9]. Scale bars: (A), 100 μm; insets, 10 μm. (B) The graph shows the mean epidermal cell area at three positions along the proximo-distal leaf axis, distal (D), median (M) and proximal (P) in the two light conditions. At least 100 adaxial epidermal cells in 10 leaves were analyzed for each condition. Statistical analysis was performed as described [94].

Figure 4

hfr1/sics1 mutation causes an exaggerated leaf primordium phenotype in shade. (A) hfr1/sics1 and control (Col-0) seedlings were grown for four days in high R/FR _{High PAR}, and then either maintained in the same light regime (red lines) or transferred to low R/FR _{Low PAR} for different times (garnet red lines). The mean area of the first/second leaf primordium was calculated by analyzing 50 samples in each condition. (B) Leaf primordia, observed under Differential Interference Contrast (DIC) optics, of hfr1/sics1 and Col-0 grown for four days in high R/FR _{High PAR}, and then either maintained in the same light regime or transferred for two days to low R/FR _{Low PAR}. Light outputs were as previously reported [9]. Scale bar, 10 μm.