Photoreceptor crosstalk in shade avoidance
Introduction
Shading from neighbouring vegetation limits photosynthetic productivity and represents a major survival threat to plants grown in dense canopies. Some understory species have therefore evolved shade tolerance strategies which enable them to survive and reproduce at low light levels [1]. Other species compete for light, using an escape strategy termed shade avoidance [2]. Plants detect the presence of competing vegetation and use this information to trigger a suite of developmental responses termed the shade avoidance syndrome (SAS). Rapid SAS responses include leaf hyponasty and stem elongation, which raise leaves above the canopy or towards canopy gaps, facilitating light capture [2]. In Arabidopsis thaliana, light quality-mediated changes in gene expression have been detected within 15 minutes [3] and changes in hypocotyl length within 45 minutes [4]. Longer term SAS responses include reduced branching, altered leaf development and accelerated flowering [2]. SAS responses in 3 species (Barley (Hordeum vulgare), Coriander (Coriandrum sativum) and Arabidopsis are shown in Figure 1.
To detect neighbouring vegetation, plants use multiple aboveground cues including the physical touching of leaf tips, the sensing of plant-emitted volatile chemicals and alterations in light quantity and quality [5]. Light quality signals are of paramount importance. Sunlight reflected or transmitted through living vegetation is depleted in red, blue and UV-B wavebands which are absorbed by green tissue. Reflected/transmitted light is enriched in green and far-red wavebands, resulting in reduced ratios of red to far-red light (R:FR) and blue to green light (B:G). Plants sense these spectral differences using specialised photoreceptors. These include the red (R) and far-red light (FR)-absorbing phytochromes, the blue (B)/UV-A light sensing cryptochromes and phototropins and the UV-B photoreceptor protein, UVR8. Horizontally propagated FR signals from nearby plants can reduce R:FR ratio (R:FR), providing a pre-canopy closure warning of competition [6]. Once shaded, R:FR is lowered further, B:G ratios decrease and UV-B levels are severely depleted [2]. Recent studies have revealed that red/far-red, blue and UV-B photoreceptors converge on a shared signalling network to control shade avoidance. This review will summarise current understanding of this topic, focussing on elongation of the Arabidopsis hypocotyl.
Section snippets
Plant photoreceptors
Phytochromes absorb light using a linear tetrapyrrole chromophore, phytochromobilin, and display R/FR photoreversibility. Synthesised in the biologically inactive Pr form, phytochromes acquire biological activity following photoconversion to the biologically active Pfr form. Conversion of Pr to Pfr is optimised at R wavelengths (600–700 nm), while Pfr to Pr conversion is optimised at FR wavelengths (700–750 nm). The R:FR of ambient light therefore controls Pr:Pfr equilibrium and hence phytochrome
Phytochromes and shade avoidance
phyB performs a dominant role in SAS inhibition, with redundant roles identified for phyD and phyE in Arabidopsis [8]. High R:FR establishes a high proportion of active phyB Pfr [7], which is translocated to the nucleus where it binds to the PHYTOCHROME INTERACTING FACTOR (PIF) family of basic Helix-Loop-Helix (bHLH) transcription factors via a conserved Active Phytochrome Binding (APB) domain (Figure 2). Pfr binding triggers PIF phosphorylation, ubiquitination and degradation by the 26s
Cryptochromes and shade avoidance
Alongside decreases in R:FR ratio, plants shaded within a canopy also perceive a reduction of ultraviolet-A (UV-A) and blue light (B) and an enrichment of green light [2]. The attenuation of blue light is perceived by cry1 and cry2 in seedlings, with cry1 adopting a dominant role in adult plants [38, 39]. Green light has been shown to partially inactivate cryptochrome signalling [40] (Figure 2). Decreased B:G ratios within canopies may therefore further exacerbate low B (LBL)-mediated shade
Phototropins and shade avoidance
Another B signal which may have a role in shade-avoidance under deep shade is the directionality of light filtering through the canopy. Phototropins re-orient leaves and stems towards B/UV-A and reposition chloroplasts to the surface of the leaf. Lateral B gradients in patchy canopies can induce phototropic curvature of stems [46]. This may be important to maximise energy capture in energy limiting conditions [5]. A role for PIF4 and PIF5 in B-mediated phototropism has been proposed involving
UVR8 and shade avoidance
UV-B is strongly filtered by canopies [2] so could provide information on the levels of competition faced by a plant. Contrasting with its role in R and B signalling, COP1 acts as a positive regulator of UV-B signalling [49]. UVR8 monomers bind directly to COP1, promoting the expression of HY5 and its close relative HY5 HOMOLOGUE (HYH) [12, 50, 51, 52]. HY5 and HYH are required for the regulation of a large proportion of UVR8-regulated genes [50, 51, 52]. Downstream of UVR8 monomerization, UV-B
Conclusions
Recent advances in photomorphogenesis research have revealed a complex shade avoidance signalling network involving multiple photoreceptors (summarised in Figure 2). PIFs 4, 5 and 7 perform a dominant role as integrators of multiple light cues, driving hormone signalling, the expression of cell wall modifying enzymes and stem elongation in an environment-dependent and possibly cell type-specific manner [23, 42••]. The ability to control auxin sensitivity and biosynthesis enables plants to
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We acknowledge the Royal Society, BBSRC and NERC for financial support.
References (68)
- et al.
Shade tolerance: when growing tall is not an option
Trends Plant Sci
(2013) - et al.
Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors
Plant J
(2008) - et al.
The shade avoidance syndrome in Arabidopsis: the antagonistic role of phytochrome A and B differentiates vegetation proximity and canopy shade
PLoS One
(2014) - et al.
The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription
PLoS Genet
(2014) - et al.
Auxin and ethylene regulate elongation responses to neighbour proximity signals independent of gibberellin and della proteins in Arabidopsis
Plant Physiol
(2009) - et al.
UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance
Proc Natl Acad Sci USA
(2014) Shade Avoidance
(2012)- et al.
Gating of the rapid shade avoidance response by the circadian clock in plants
Nature
(2003) - et al.
A dynamic analysis of hypocotyl growth during shade avoidance in Arabidopsis
Plant J
(2011) - et al.
Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues
J Exp Bot
(2014)
Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies
Science
The function of phytochrome in plants growing in the natural environment
Nature
Phytochrome functions in Arabidopsis development
J Ex Bot
Plant flavoprotein photoreceptors
Plant Cell Physiol
Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation
Plant Cell
Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor Cryptochrome 2
Proc Natl Acad Sci USA
Perception of UV-B by the Arabidopsis UVR8 protein
Science
Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges
Science
Structural basis of ultraviolet-B perception by UVR8
Nature
In vivo function of tryptophans in the Arabidopsis UV-B photoreceptor UVR8
Plant Cell
Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8
Nat Plants
PIFs: systems integrators in plant development
Plant Cell
A mutually assured destruction mechanism attenuates light signaling in Arabidopsis
Science
SUMOylation of phytochrome-B negatively regulates light-induced signaling in Arabidopsis thaliana
Proc Natl Acad Sci USA
Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling
Plant J
Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants
Cell
Linking photoreceptor excitation to changes in plant architecture
Genes Dev
Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition
Proc Natl Acad Sci USA
Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PIF5 as a modulator of auxin signaling in Arabidopsis
Plant Physiol
Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis
Proc Natl Acad Sci USA
Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers
EMBO J
The shade avoidance syndrome in Arabidopsis: a fundamental role for atypical basic helix-loop-helix proteins as transcriptional cofactors
Plant J
Interactions between HLH and bHLH factors modulate light-regulated plant development
Mol Plant
Both PHYTOCHROME RAPIDLY REGULATED1 (PAR1) and PAR2 promote seedling photomorphogenesis in multiple light signaling pathways
Plant Cell
Cited by (0)
- 3
These authors contributed equally.