Shade avoidance syndrome in 4D: illuminating a role for transcriptional repression of protein biogenesis genes

The leaf is the main organ for sunlight absorption and information acquisition from the environment. Such roles have granted the leaf with tremendous plasticity to secure the conversion of photons into sugars and to outcompete neighboring plants (Fritz et al., 2018). While chlorophylls absorb mainly blue (B, 480 nm) and red (R, 660 nm) photons from incoming sunlight to drive photosynthesis and produce organic molecules, phytochromes extract information from reflected light of surrounding green tissues by detecting the ratio of R to far-red (FR, 730 nm) light to shape the final canopy architecture (Ballaré and Casal, 2000; Major et al., 2017). The two photoconvertible forms of phytochrome absorb R and FR photons from the light environment with different efficiency, thus a drop in R:FR ratio detected by phytochromes reveals the proximity of competitors (Ballaré et al., 1990).

The Arabidopsis (Arabidopsis thaliana) genome encodes five phytochromes: phyA-phyE. Depletion of the active form of the main phytochrome in green tissues of Arabidopsis, phyB, unleashes the shade avoidance syndrome (SAS), which is characterized in most environmental conditions by stem and petiole elongation, reduced leaf lamina expansion, reduced branching, and promotion of leaf hyponasty, all of which contribute to improved light absorption. We can artificially induce SAS in a plant by supplementing with FR light, either along with daylight or at the very end-of-the-day (EoD FR). The short EoD FR treatment avoids the activation of phyA and consequently avoids the suppression of SAS (Strasser et al., 2010).

In this issue of Plant Physiology, Romanowski et al. (2021) used EoD FR treatment to explore the dynamics of the transcriptomic landscape during the inhibition of leaf lamina expansion. The authors applied EoD FR light to follow the growth and establish the molecular processes of the transcriptomic response at different developmental stages of leaf number 3 (L3) in Arabidopsis (Gonzalez et al., 2012). The authors also characterized the morphological component of SAS at the cellular level.

The supplementation of EoD FR light at different developmental points exerted interesting differences in the lamina expansion of wild-type plants. In general, EoD FR treatments early in L3 development effectively repressed leaf lamina expansion compared to later treatments. The effect at early stages was associated with a reduced number of abaxial epidermal cells, whereas later in development the EoD FR effect was largely compensated through increased epidermal cell density. As reported before, the phyb9 mutant showed constitutive reduction in leaf lamina area explained by reduced number, not size or density, of abaxial epidermal cells (Tsukaya et al., 2002; Gonzalez et al., 2012). So, Romanowski et al. wondered if different cellular mechanisms mediate the inhibition of lamina expansion during SAS and if this could be connected to different transcriptomic profiles (Romanowski et al., 2021).

Romanowski et al. (2021) showed EoD FR treatment induces broad transcriptomic reprogramming with notable differences between developmental stages of the leaf lamina. Within the group of upregulated genes, the authors found a subgroup with constant induction, including several genes related to SAS and ethylene and auxin signaling, while autophagy-related genes were preferentially expressed at early time points and flowering genes later in leaf development.

Previous studies using reporter line CYCLIN B1;1-GUS show FR light inhibits cell cycle progression (Carabelli et al., 2007; Carabelli et al., 2018). Romanowski et al. found broad gene repression at all times of genes related to cell cycle, such as cell proliferation and cell division, and genes related to DNA replication, repair, and integrity (Figure 1). Late-responding genes to EoD FR light included photosynthesis- and carotenoid-related genes, and more notably, this group included the repression of several genes related to ribosome biogenesis and translation (Figure 1). Romanowski et al. (2021) pointed out the largest group of differentially expressed genes were actually suppressed by EoD FR treatment, despite most studied SAS-related genes belonging to the group of upregulated genes. This finding opens novel questions regarding the contribution of repression not only to the inhibition of leaf lamina expansion but to the whole SAS response.

Figure 1.

Developmental stage processes modulated by EoD FR treatment of leaf lamina. While early-stage EoD FR limits cell division, later stage EoD FR limits cell expansion. This study shows SAS is induced by the activation of several hormone-related genes, but SAS is also controlled by the repression of genes related to ribosome biogenesis and translation. L3 = Leaf 3; dev = development. (Figure from Romanowski et al., 2021).

A key outcome of the present study is evidence of specific transcriptional blueprints of each leaf stage. While early in development EoD FR treatment activates genes related to restraining cell division, later exposure to the same light treatment reduces lamina area mainly through inhibition of cell expansion-related genes. In addition, this study describes a deep change in the hormonal-response signature of each stage, shedding light into the complexity of SAS, likely reflecting the plasticity of this syndrome. How hormone-related genes that normally activate growth responses trigger an inhibition of leaf lamina expansion is still under scrutiny and the mechanism is unclear. The transcriptomic data is now easily accessible through the link https://aromanowski.shinyapps.io/leafdev-app/.

Digging into the time-response, Romanowski et al. (2021) proposed two alternatives to the physiological response leading to the repression of leaf lamina expansion and downregulation of the translation machinery: (1) growth halting results in an abrupt reduction of protein synthesis, including ribosomal and translational proteins, or (2) FR light induces premature senescence, including a remobilization of proteins to newly formed tissues.

Single-cell transcriptomic analysis on different parts of the leaf and at different time points will be crucial to physically and functionally dissect these pathways controlling opposing responses. The addition of the time dimension into studying SAS at the tissue and organ level can help us understand the multiple tiers of plasticity in plants and learn how we can manipulate the SAS response to enhance light absorption in crop plants.