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...

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Light absorption by plants changes the composition of light inside vegetation. Blue (B) and red (R) light are used for photosynthesis whereas far-red (FR) and green light are reflected. A combination of UV-B, blue and R:FR-responsive photoreceptors collectively measures the light and temperature environment and adjusts plant development accordingly. This developmental plasticity to photoreceptor signals is largely regulated through the phytohormone auxin. The phytochrome, cryptochrome and UV Resistance Locus 8 (UVR8) photoreceptors are inactivated in shade and/or elevated temperature, which releases their repression of Phytochrome Interacting Factor (PIF) transcription factors. Active PIFs stimulate auxin synthesis and reinforce auxin signalling responses through direct interaction with Auxin Response Factors (ARFs). It was recently discovered that shade-induced hypocotyl elongation and petiole hyponasty depend on long-distance auxin transport towards target cells from the cotyledon and leaf tip, respectively. Other responses, such as phototropic bending, are regulated by auxin transport and signalling across only a few cell layers. In addition, photoreceptors can directly interact with components in the auxin signalling pathway, such as Auxin/Indole Acetic Acids (AUX/IAAs) and ARFs. Here we will discuss the complex interactions between photoreceptor and auxin signalling, addressing both mechanisms and consequences of these highly interconnected pathways.

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