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...
Timely perception of adverse environmental changes is critical for survival. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In Arabidopsis thaliana , changes in oxygen and nitric oxide (NO) control the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced hypoxia. However, how plants detect and transduce early submergence signals remains elusive. Here we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent hypoxia. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies key regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.
Plants in dense vegetation perceive their neighbors primarily through changes in light quality. Initially, the ratio between red (R) and far-red (FR) light decreases due to reflection of FR by plant tissue well before shading occurs. Perception of low R:FR by the phytochrome photoreceptors induces the shade avoidance response [1], of which accelerated elongation growth of leaf-bearing organs is an important feature. Low R:FR-induced phytochrome inactivation leads to the accumulation and activation of the transcription factors PHYTOCHROME-INTERACTING FACTORs (PIFs) 4, 5, and 7 and subsequent expression of their growth-mediating targets [2, 3]. When true shading occurs, transmitted light is especially depleted in red and blue (B) wavelengths, due to absorption by chlorophyll [4]. Although the reduction of blue wavelengths alone does not occur in nature, long-term exposure to low B light induces a shade avoidance-like response that is dependent on the cryptochrome photoreceptors and the transcription factors PIF4 and PIF5 [5-7]. We show in Arabidopsis thaliana that low B in combination with low R:FR enhances petiole elongation similar to vegetation shade, providing functional context for a low B response in plant competition. Low B potentiates the low R:FR response through PIF4, PIF5, and PIF7, and it involves increased PIF5 abundance and transcriptional changes. Low B attenuates a low R:FR-induced negative feedback loop through reduced gene expression of negative regulators and reduced HFR1 levels. The enhanced response to combined phytochrome and cryptochrome inactivation shows how multiple light cues can be integrated to fine-tune the plant's response to a changing environment.
25 Timely perception of adverse environmental changes is critical for survival. Dynamic 26 changes in gases are important cues for plants to sense environmental perturbations, such 27 as submergence. In Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control 28 the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-29 degron pathway and mediates adaptation to flooding-induced hypoxia. However, how 30 plants detect and transduce early submergence signals remains elusive. Here we show that 31 plants can rapidly detect submergence through passive ethylene entrapment and use this 32 signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to 33 hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO 34 depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent 35 hypoxia. Our results reveal the biological link between three gaseous signals for the 36 regulation of flooding survival and identifies novel regulatory targets for early stress 37 perception that could be pivotal for developing flood-tolerant crops. 38 39 42 cellular oxygen (O 2 ) deprivation (hypoxia) and survival strongly depends on molecular responses 43 that enhance hypoxia tolerance 2,3 . In submerged plant tissues the limited gas diffusion causes 44 passive ethylene accumulation. This rapid ethylene build-up can occur prior to the onset of 45 severe hypoxia, making it a timely and reliable signal for submergence 4,5 . In several plant 46 species, ethylene regulates adaptive responses to flooding involving morphological and 47anatomical modifications that prevent hypoxia 5 . Surprisingly, ethylene has so far not been 48 linked to metabolic responses that reduce hypoxia damage. In addition, how plants detect and 49 transduce early submergence signals to enhance survival remains elusive. 50 Here we show that plants can quickly detect submergence using passive ethylene accumulation 51 and integrate this signal to acclimate to subsequent hypoxia. This ethylene-mediated hypoxia 52 acclimation is dependent on enhanced ERFVII stability prior to hypoxia. We show that ethylene 53 limits ERFVII proteolysis under normoxic conditions by increasing the NO-scavenger 54 3 PHYTOGLOBIN1. Our results reveal a molecular mechanism that plants use to integrate early 55 stress signals to pre-adapt to forthcoming severe stress. 57 Results 58Early ethylene signalling enhances hypoxia acclimation 59 To unravel the spatial and temporal dynamics of ethylene signalling upon plant submergence, we 60 monitored the nuclear accumulation of ETHYLENE INSENSITIVE 3 (EIN3) 6-9 , an essential 61 transcription factor for mediating ethylene responses. We show, through an increase in EIN3- 62GFP fluorescence signal, that ethylene is rapidly perceived (within 1-2 h) in Arabidopsis 63 thaliana (hereafter Arabidopsis) root tips upon submergence (Supplementary Figure 1a-c). An 64 ethylene or submergence pre-treatment of only 4 hours was sufficient to increase root m...
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