Lights, location, action: Shade avoidance signalling over spatial scales.

Plants growing in dense vegetation stands need to flexibly position their photosynthetic organs to ensure optimal light capture in a competitive environment. They do so through a suite of developmental responses referred to as the shade avoidance syndrome. Belowground, root development is also adjusted in response to aboveground neighbour proximity. Canopies are dynamic and complex environments with heterogenous light cues in the far-red, red, blue and UV spectrum, which can be perceived with photoreceptors by spatially separated plant tissues. Molecular regulation of plant architecture adjustment via PHYTOCHROME-INTERACTING FACTOR (PIF) transcription factors and growth-related hormones such as auxin, gibberellic acid, brassinosteroids and abscisic acid were historically studied without much attention to spatial or tissue-specific context. Recent developments and technologies have, however, sparked strong interest in spatially explicit understanding of shade avoidance regulation. Other environmental factors such as temperature and nutrient availability interact with the molecular shade avoidance regulation network, often depending on the spatial location of the signals, and the responding organs. Here, we aim to review recent advances in how plants respond to heterogenous light cues and integrate these with other environmental signals.

Far-red light enrichment affects gene expression and architecture as well as growth and photosynthesis in rice.

Plants use light as a resource and signal. Photons within the 400-700 nm waveband are considered photosynthetically active. Far-red photons (FR, 700-800 nm) are used by plants to detect nearby vegetation and elicit the shade avoidance syndrome. In addition, FR photons have also been shown to contribute to photosynthesis, but knowledge about these dual effects remains scarce. Here, we study shoot-architectural and photosynthetic responses to supplemental FR light during the photoperiod in several rice varieties. We observed that FR enrichment only mildly affected the rice transcriptome and shoot architecture as compared to established model species, whereas leaf formation, tillering and biomass accumulation were clearly promoted. Consistent with this growth promotion, we found that CO2-fixation in supplemental FR was strongly enhanced, especially in plants acclimated to FR-enriched conditions as compared to control conditions. This growth promotion dominates the effects of FR photons on shoot development and architecture. When substituting FR enrichment with an end-of-day FR pulse, this prevented photosynthesis-promoting effects and elicited shade avoidance responses. We conclude that FR photons can have a dual role, where effects depend on the environmental context: in addition to being an environmental signal, they are also a potent source of harvestable energy.

A low-cost open-source imaging platform reveals spatiotemporal insight into leaf elongation and movement.

Plant organs move throughout the diurnal cycle, changing leaf and petiole positions to balance light capture, leaf temperature, and water loss under dynamic environmental conditions. Upward movement of the petiole, called hyponasty, is one of several traits of the shade avoidance syndrome (SAS). SAS traits are elicited upon perception of vegetation shade signals such as far-red light (FR) and improve light capture in dense vegetation. Monitoring plant movement at a high temporal resolution allows studying functionality and molecular regulation of hyponasty. However, high temporal resolution imaging solutions are often very expensive, making this unavailable to many researchers. Here, we present a modular and low-cost imaging set-up, based on small Raspberry Pi computers, that can track leaf movements and elongation growth with high temporal resolution. We also developed an open-source, semi-automated image analysis pipeline. Using this setup we followed responses to FR enrichment, light intensity, and their interactions. Tracking both elongation and the angle of the petiole, lamina, and entire leaf in Arabidopsis (Arabidopsis thaliana) revealed insight into R:FR sensitivities of leaf growth and movement dynamics and the interactions of R:FR with background light intensity. The detailed imaging options of this system allowed us to identify spatially separate bending points for petiole and lamina positioning of the leaf.

Mechanodetection of neighbor plants elicits adaptive leaf movements through calcium dynamics.

Plants detect their neighbors via various cues, including reflected light and touching of leaf tips, which elicit upward leaf movement (hyponasty). It is currently unknown how touch is sensed and how the signal is transferred from the leaf tip to the petiole base that drives hyponasty. Here, we show that touch-induced hyponasty involves a signal transduction pathway that is distinct from light-mediated hyponasty. We found that mechanostimulation of the leaf tip upon touching causes cytosolic calcium ([Ca2+]cyt induction in leaf tip trichomes that spreads towards the petiole. Both perturbation of the calcium response and the absence of trichomes reduce touch-induced hyponasty. Finally, using plant competition assays, we show that touch-induced hyponasty is adaptive in dense stands of Arabidopsis. We thus establish a novel, adaptive mechanism regulating hyponastic leaf movement in response to mechanostimulation by neighbors in dense vegetation.

Plant signaling: The sugar-coated story of root growth.

A new study draws attention to photosynthetically produced sucrose as a major shoot-derived and auxin-dependent regulator of root growth and development in plants.

Local light signaling at the leaf tip drives remote differential petiole growth through auxin-gibberellin dynamics.

Although plants are immobile, many of their organs are flexible to move in response to environmental cues. In dense vegetation, plants detect neighbors through far-red light perception with their leaf tip. They respond remotely, with asymmetrical growth between the abaxial and adaxial sides of the leafstalk, the petiole. This results in upward movement that brings the leaf blades into better lit zones of the canopy. The plant hormone auxin is required for this response, but it is not understood how non-differential leaf tip-derived auxin can remotely regulate movement. Here, we show that remote signaling of far-red light promotes auxin accumulation in the abaxial petiole. This local auxin accumulation is facilitated by reinforcing an intrinsic directionality of the auxin transport protein PIN3 on the petiole endodermis, as visualized with a PIN3-GFP line. Using an auxin biosensor, we show that auxin accumulates in all cell layers from endodermis to epidermis in the abaxial petiole, upon far-red light signaling in the remote leaf tip. In the petiole, auxin elicits a response to both auxin itself as well as a second growth promoter; gibberellin. We show that this dual regulation is necessary for hyponastic leaf movement in response to light. Our data indicate that gibberellin is required to permit cell growth, whereas differential auxin accumulation determines which cells can grow. Our results reveal how plants can spatially relay information about neighbor proximity from their sensory leaf tips to the petiole base, thus driving adaptive growth.

Mechanisms of far-red light-mediated dampening of defense against Botrytis cinerea in tomato leaves.

Plants detect neighboring competitors through a decrease in the ratio between red and far-red light (R:FR). This decreased R:FR is perceived by phytochrome photoreceptors and triggers shade avoidance responses such as shoot elongation and upward leaf movement (hyponasty). In addition to promoting elongation growth, low R:FR perception enhances plant susceptibility to pathogens: the growth-defense tradeoff. Although increased susceptibility in low R:FR has been studied for over a decade, the associated timing of molecular events is still unknown. Here, we studied the chronology of FR-induced susceptibility events in tomato (Solanum lycopersicum) plants pre-exposed to either white light (WL) or WL supplemented with FR light (WL+FR) prior to inoculation with the necrotrophic fungus Botrytis cinerea (B.c.). We monitored the leaf transcriptional changes over a 30-h time course upon infection and followed up with functional studies to identify mechanisms. We found that FR-induced susceptibility in tomato is linked to a general dampening of B.c.-responsive gene expression, and a delay in both pathogen recognition and jasmonic acid-mediated defense gene expression. In addition, we found that the supplemental FR-induced ethylene emissions affected plant immune responses under the WL+FR condition. This study improves our understanding of the growth-immunity tradeoff, while simultaneously providing leads to improve tomato resistance against pathogens in dense cropping systems.

The role of seasonality in reproduction of multiannual delayed gametophytes of Saccharina latissima.

Delayed gametophytes are able to grow vegetatively for prolonged periods of time. As such, they are potentially very valuable for kelp aquaculture given their great promise in opening up novel opportunities for kelp breeding and farming. However, large-scale application would require more in-depth understanding of how to control reproduction in delayed gametophytes. For newly formed gametophytes, many environmental factors for reproduction have been identified, with key drivers being light intensity, temperature, and the initial gametophyte density. However, the question of whether delayed gametophytes react similarly to these life cycle controls remains open for exploration. In this study, we performed a full factorial experiment on the influences of light intensity, temperature, and density on the reproduction of multiannual delayed gametophytes of Saccharina latissima, during which the number of sporophytes formed was counted. We demonstrate that delayed gametophytes of S. latissima can reliably reproduce sexually after more than a year of vegetative growth, depending on the effects between light intensity and temperature. Under higher light intensities (≥29 µmol photons · m-2 · s-1 ), optimal reproduction was observed at lower temperatures (10.2°C), while at lower light intensities (≤15 µmol photons · m-2 · s-1 ), optimal reproduction was observed at higher temperatures (≥12.6°C). Given the seasonal lag between solar radiation and sea surface temperature in natural systems, these conditions resemble those found during spring (i.e., increasing light intensity with low temperatures) and autumn (i.e., decreasing light intensity with higher temperatures). Seasonality can be used as an aquaculture tool to better control the reproduction of delayed gametophytes.

Regulation of Lateral Root Development by Shoot-Sensed Far-Red Light via HY5 Is Nitrate-Dependent and Involves the NRT2.1 Nitrate Transporter.

Plants are very effective in responding to environmental changes during competition for light and nutrients. Low Red:Far-Red (low R:FR)-mediated neighbor detection allows plants to compete successfully with other plants for available light. This above-ground signal can also reduce lateral root growth by inhibiting lateral root emergence, a process that might help the plant invest resources in shoot growth. Nitrate is an essential nutrient for plant growth and Arabidopsis thaliana responds to low nitrate conditions by enhancing nutrient uptake and reducing lateral and main root growth. There are indications that low R:FR signaling and low nitrate signaling can affect each other. It is unknown which response is prioritized when low R:FR light- and low nitrate signaling co-occur. We investigated the effect of low nitrate conditions on the low R:FR response of the A. thaliana root system in agar plate media, combined with the application of supplemental Far-Red (FR) light to the shoot. We observed that under low nitrate conditions main and lateral root growth was reduced, but more importantly, that the response of the root system to low R:FR was not present. Consistently, a loss-of-function mutant of a nitrate transporter gene NRT2.1 lacked low R:FR-induced lateral root reduction and its root growth was hypersensitive to low nitrate. ELONGATED HYPOCOTYL5 (HY5) plays an important role in the root response to low R:FR and we found that it was less sensitive to low nitrate conditions with regards to lateral root growth. In addition, we found that low R:FR increases NRT2.1 expression and that low nitrate enhances HY5 expression. HY5 also affects NRT2.1 expression, however, it depended on the presence of ammonium in which direction this effect was. Replacing part of the nitrogen source with ammonium also removed the effect of low R:FR on the root system, showing that changes in nitrogen sources can be crucial for root plasticity. Together our results show that nitrate signaling can repress low R:FR responses and that this involves signaling via HY5 and NRT2.1.

Light signalling shapes plant-plant interactions in dense canopies.

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.

Control of Plant Growth and Defense by Photoreceptors: From Mechanisms to Opportunities in Agriculture.

Plants detect and respond to the proximity of competitors using light signals perceived by photoreceptor proteins. A low ratio of red to far-red radiation (R:FR ratio) is a key signal of competition that is sensed by the photoreceptor phytochrome B (phyB). Low R:FR ratios increase the synthesis of growth-related hormones, including auxin and gibberellins, promoting stem elongation and other shade-avoidance responses. Other photoreceptors that help plants to optimize their developmental configuration and resource allocation patterns in the canopy include blue light photoreceptors, such as cryptochromes and phototropins, and UV receptors, such as UVR8. All photoreceptors act by directly or indirectly controlling the activity of two major regulatory nodes for growth and development: the COP1/SPA ubiquitin E3 ligase complex and the PIF transcription factors. phyB is also an important modulator of hormonal pathways that regulate plant defense against herbivores and pathogens, including the jasmonic acid signaling pathway. In this Perspective, we discuss recent advances on the studies of the mechanisms that link photoreceptors with growth and defense. Understanding these mechanisms is important to provide a functional platform for breeding programs aimed at improving plant productivity, stress tolerance, and crop health in species of agronomic interest, and to manipulate the light environments in protected agriculture.

Reducing shade avoidance can improve Arabidopsis canopy performance against competitors.

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.

A Gas-and-Brake Mechanism of bHLH Proteins Modulates Shade Avoidance.

Plants detect proximity of competitors through reduction in the ratio between red and far-red light that triggers the shade avoidance syndrome, inducing responses such as accelerated shoot elongation and early flowering. Shade avoidance is regulated by PHYTOCHROME INTERACTING FACTORs, a group of basic helix-loop-helix (bHLH) transcription factors. Another (b)HLH protein, KIDARI (KDR), which is non-DNA-binding, was identified in de-etiolation studies and proposed to interact with LONG HYPOCOTYL IN FAR-RED1 (HFR1), a (b)HLH protein that inhibits shade avoidance. Here, we established roles of KDR in regulating shade avoidance in Arabidopsis (Arabidopsis thaliana) and investigated how KDR regulates the shade avoidance network. We showed that KDR is a positive regulator of shade avoidance and interacts with several negative growth regulators. We identified KDR interactors using a combination of yeast two-hybrid screening and dedicated confirmations with bimolecular fluorescence complementation. We demonstrated that KDR is translocated primarily to the nucleus when coexpressed with these interactors. A genetic approach confirmed that several of these interactions play a functional role in shade avoidance; however, we propose that KDR does not interact with HFR1 to regulate shade avoidance. Based on these observations, we propose that shade avoidance is regulated by a three-layered gas-and-brake mechanism of bHLH protein interactions, adding a layer of complexity to what was previously known.

Far-red light promotes Botrytis cinerea disease development in tomato leaves via jasmonate-dependent modulation of soluble sugars.

Plants experience a decrease in the red:far-red light ratio (R:FR) when grown at high planting density. In addition to eliciting the shade avoidance response, low R:FR also enhances plant susceptibility to pathogens via modulation of defense hormone-mediated responses. However, other mechanisms, also affected by low R:FR, have not been considered as potential components in FR-induced susceptibility. Here, we identify FR-induced accumulation of leaf soluble sugars as a novel component of FR-induced susceptibility. We observed that phytochrome inactivation by FR or phytochrome B mutation was associated with elevated leaf glucose and fructose levels and enhanced disease severity caused by Botrytis cinerea. By experimentally manipulating internal leaf sugar levels, we found that the FR-induced susceptibility in tomato was partly sugar-dependent. Further analysis revealed that the observed sugar accumulation in supplemental FR occurred in a jasmonic acid (JA)-dependent manner, and the JA biosynthesis mutant def1 also displayed elevated soluble sugar levels, which was rescued by exogenous methyl jasmonate (MeJA) application. We propose that the reduced JA responsiveness under low R:FR promotes disease symptoms not only via dampened induction of defense responses, but also via increased levels of soluble sugars that supports pathogen growth in tomato leaves.

Photoreceptors Regulate Plant Developmental Plasticity through Auxin.

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.