Vegetation stands have a heterogeneous distribution of light quality, including the red/far-red light ratio (R/FR) that informs plants about proximity of neighbors. Adequate responses to changes in R/FR are important for competitive success. How the detection and response to R/FR are spatially linked and how this spatial coordination between detection and response affects plant performance remains unresolved. We show in Arabidopsis thaliana and Brassica nigra that localized FR enrichment at the lamina tip induces upward leaf movement (hyponasty) from the petiole base. Using a combination of organ-level transcriptome analysis, molecular reporters, and physiology, we show that PIF-dependent spatial auxin dynamics are key to this remote response to localized FR enrichment. Using computational 3D modeling, we show that remote signaling of R/FR for hyponasty has an adaptive advantage over local signaling in the petiole, because it optimizes the timing of leaf movement in response to neighbors and prevents hyponasty caused by self-shading.leaf movement | auxin | phytochrome | functional-structural plant model | shade avoidance P lant canopies have pronounced gradients of light intensity between the top and bottom because leaves shade one another (1). As a consequence of the clustering of leaves, light intensities also vary horizontally. Because light drives photosynthesis, this variable light intensity creates selection pressure for plants to position their leaves for optimal light capture. Leaves do not absorb all wavelengths of the incoming light equally, and therefore light quality also differs vertically and horizontally in canopies (1-3) and even across the surface of individual leaves (4). Leaves preferentially absorb red (R) (λ = 600-700 nm) and blue (B) (λ = 400-500 nm) light for photosynthesis while reflecting most of the far-red (FR) (λ= 700-800 nm) light. This preference leads to a relative enrichment of FR light (low R/FR) in the local vicinity of leaves, a signal of neighbor proximity (5).Low R/FR is sensed by phytochrome photoreceptors, mainly phytochrome B (phyB), and induces upward leaf movement (hyponasty) through differential petiole growth and elongation of stems and petioles, thus bringing the leaves higher, toward the more illuminated parts of the canopy (6-8). Plants are modular organisms, and such shade-avoidance responses could thus be restricted to the specific modules that sense shade cues (9-11). Although spatial separation was shown recently for hypocotyl elongation in small Brassica rapa seedlings (12), only more established plants are large enough to experience light quality heterogeneity over the plant body. It is unknown whether responses to a low R/FR in relatively mature Arabidopsis plants act locally or integrate detection from different plant parts.A low R/FR inactivates phytochromes, leading to the accumulation of active PHYTOCHROME INTERACTING FACTOR (PIF) transcription factors, notably PIF4, PIF5, and PIF7, that trigger expression of growth-promoting genes (13), including auxin s...

Plants growing at high densities interact via a multitude of pathways. Here, we provide an overview of mechanisms and functional consequences of plant architectural responses initiated by light cues that occur in dense vegetation. We will review the current state of knowledge about shade avoidance, as well as its possible applications. On an individual level, plants perceive neighbour‐associated changes in light quality and quantity mainly with phytochromes for red and far‐red light and cryptochromes and phototropins for blue light. Downstream of these photoreceptors, elaborate signalling and integration takes place with the PHYTOCHROME INTERACTING FACTORS, several hormones and other regulators. This signalling leads to the shade avoidance responses, consisting of hyponasty, stem and petiole elongation, apical dominance and life cycle adjustments. Architectural changes of the individual plant have consequences for the plant community, affecting canopy structure, species composition and population fitness. In this context, we highlight the ecological, evolutionary and agricultural importance of shade avoidance.

Summary Global food production is set to keep increasing despite a predicted decrease in total arable land [ 1 ]. To achieve higher production, denser planting will be required on increasingly degraded soils. When grown in dense stands, crops elongate and raise their leaves in an effort to reach sunlight, a process termed shade avoidance [ 2 ]. Shade is perceived by a reduction in the ratio of red (R) to far-red (FR) light and results in the stabilization of a class of transcription factors known as PHYTOCHROME INTERACTING FACTORS (PIFs) [ 3 , 4 ]. PIFs activate the expression of auxin biosynthesis genes [ 4 , 5 ] and enhance auxin sensitivity [ 6 ], which promotes cell-wall loosening and drives elongation growth. Despite our molecular understanding of shade-induced growth, little is known about how this developmental program is integrated with other environmental factors. Here, we demonstrate that low levels of NaCl in soil strongly impair the ability of plants to respond to shade. This block is dependent upon abscisic acid (ABA) signaling and the canonical ABA signaling pathway. Low R:FR light enhances brassinosteroid (BR) signaling through BRASSINOSTEROID SIGNALING KINASE 5 (BSK5) and leads to the activation of BRI1 EMS SUPPRESSOR 1 (BES1). ABA inhibits BSK5 upregulation and interferes with GSK3-like kinase inactivation by the BR pathway, thus leading to a suppression of BES1:PIF function. By demonstrating a link between light, ABA-, and BR-signaling pathways, this study provides an important step forward in our understanding of how multiple environmental cues are integrated into plant development.

Plants that grow in high density communities activate shade avoidance responses to consolidate light capture by individuals. Although this is an evolutionary successful strategy, it may not enhance performance of the community as a whole. Resources are invested in shade responses at the expense of other organs and light penetration through the canopy is increased, allowing invading competitors to grow better. Here we investigate if suppression of shade avoidance responses would enhance group performance of a monoculture community that is invaded by a competitor. Using different Arabidopsis genotypes, we show that suppression of shade-induced upward leaf movement in the pif7 mutant increases the pif7 communal performance against invaders as compared to a wild-type canopy. The invaders were more severely suppressed and the community grew larger as compared to wild type. Using computational modelling, we show that leaf angle variations indeed strongly affect light penetration and growth of competitors that invade the canopy. Our data thus show that modifying specific shade avoidance aspects can improve plant community performance. These insights may help to suppress weeds in crop stands.

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