Why did glutamate, GABA, and melatonin become intercellular signalling molecules in plants?

Intercellular signalling is an indispensable part of multicellular life. Understanding the commonalities and differences in how signalling molecules function in two remote branches of the tree of life may shed light on the reasons these molecules were originally recruited for intercellular signalling. Here we review the plant function of three highly studied animal intercellular signalling molecules, namely glutamate, γ-aminobutyric acid (GABA), and melatonin. By considering both their signalling function in plants and their broader physiological function, we suggest that molecules with an original function as key metabolites or active participants in reactive ion species scavenging have a high chance of becoming intercellular signalling molecules. Naturally, the evolution of machinery to transduce a message across the plasma membrane is necessary. This fact is demonstrated by three other well-studied animal intercellular signalling molecules, namely serotonin, dopamine, and acetylcholine, for which there is currently no evidence that they act as intercellular signalling molecules in plants

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

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

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

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

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 (PIFs), a group of 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-RED 1 (HFR1), a (b)HLH protein that inhibits shade avoidance. Here we established roles of KDR in regulating shade avoidance in 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

Why did glutamate, GABA, and melatonin become intercellular signalling molecules in plants?

Intercellular signalling is an indispensable part of multicellular life. Understanding the commonalities and differences in how signalling molecules function in two remote branches of the tree of life may shed light on the reasons these molecules were originally recruited for intercellular signalling. Here we review the plant function of three highly studied animal intercellular signalling molecules, namely glutamate, γ-aminobutyric acid (GABA), and melatonin. By considering both their signalling function in plants and their broader physiological function, we suggest that molecules with an original function as key metabolites or active participants in reactive ion species scavenging have a high chance of becoming intercellular signalling molecules. Naturally, the evolution of machinery to transduce a message across the plasma membrane is necessary. This fact is demonstrated by three other well-studied animal intercellular signalling molecules, namely serotonin, dopamine, and acetylcholine, for which there is currently no evidence that they act as intercellular signalling molecules in plants

Mechanodetection of neighbor plants elicits adaptive leaf movements through calcium dynamics

Abstract 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

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 (PIFs), a group of 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-RED 1 (HFR1), a (b)HLH protein that inhibits shade avoidance. Here we established roles of KDR in regulating shade avoidance in 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

Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics

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