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Plants have evolved shoot elongation mechanisms to escape from diverse environmental stresses such as flooding and vegetative shade. The apparent similarity in growth responses suggests a possible convergence of the signaling pathways. Shoot elongation is mediated by passive ethylene accumulating to high concentrations in flooded plant organs and by changes in light quality and quantity under vegetation shade. Here, we study hypocotyl elongation as a proxy for shoot elongation and delineate Arabidopsis (Arabidopsis thaliana) hypocotyl length kinetics in response to ethylene and shade. Based on these kinetics, we further investigated ethylene- and shade-induced genome-wide gene expression changes in hypocotyls and cotyledons separately. Both treatments induced a more extensive transcriptome reconfiguration in the hypocotyls compared with the cotyledons. Bioinformatics analyses suggested contrasting regulation of growth promotion- and photosynthesis-related genes. These analyses also suggested an induction of auxin, brassinosteroid, and gibberellin signatures and the involvement of several candidate regulators in the elongating hypocotyls. Pharmacological and mutant analyses confirmed the functional involvement of several of these candidate genes and physiological control points in regulating stress-escape responses to different environmental stimuli. We discuss how these signaling networks might be integrated and conclude that plants, when facing different stresses, utilize a conserved set of transcriptionally regulated genes to modulate and fine-tune growth., (© 2016 American Society of Plant Biologists. All Rights Reserved.)

We propose that the ability to synthesize ethylene was selectively lost in evolution when the ancestors of fully aquatic higher plants lost their terrestrial lifestyle. We suggest that there has been negative selection on ethylene in these submerged species because it might interfere with growth in permanently deluged environments., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Land plants have evolved adaptive regulatory mechanisms enabling the survival of environmental stresses associated with terrestrial life. Here, we focus on the evolution of the regulatory CONSTITUTIVE TRIPLE RESPONSE1 (CTR1) component of the ethylene signaling pathway that modulates stress-related changes in plant growth and development. First, we compare CTR1-like proteins from a bryophyte, Physcomitrella patens (representative of early divergent land plants), with those of more recently diverged lycophyte and angiosperm species (including Arabidopsis [Arabidopsis thaliana]) and identify a monophyletic CTR1 family. The fully sequenced P. patens genome encodes only a single member of this family (PpCTR1L). Next, we compare the functions of PpCTR1L with that of related angiosperm proteins. We show that, like angiosperm CTR1 proteins (e.g. AtCTR1 of Arabidopsis), PpCTR1L modulates downstream ethylene signaling via direct interaction with ethylene receptors. These functions, therefore, likely predate the divergence of the bryophytes from the land-plant lineage. However, we also show that PpCTR1L unexpectedly has dual functions and additionally modulates abscisic acid (ABA) signaling. In contrast, while AtCTR1 lacks detectable ABA signaling functions, Arabidopsis has during evolution acquired another homolog that is functionally distinct from AtCTR1. In conclusion, the roles of CTR1-related proteins appear to have functionally diversified during land-plant evolution, and angiosperm CTR1-related proteins appear to have lost an ancestral ABA signaling function. Our study provides new insights into how molecular events such as gene duplication and functional differentiation may have contributed to the adaptive evolution of regulatory mechanisms in plants., (© 2015 American Society of Plant Biologists. All Rights Reserved.)

Upward leaf movement (hyponastic growth) is frequently observed in response to changing environmental conditions and can be induced by the phytohormone ethylene. Hyponasty results from differential growth (i.e. enhanced cell elongation at the proximal abaxial side of the petiole relative to the adaxial side). Here, we characterize Enhanced Hyponasty-d, an activation-tagged Arabidopsis (Arabidopsis thaliana) line with exaggerated hyponasty. This phenotype is associated with overexpression of the mitotic cyclin CYCLINA2;1 (CYCA2;1), which hints at a role for cell divisions in regulating hyponasty. Indeed, mathematical analysis suggested that the observed changes in abaxial cell elongation rates during ethylene treatment should result in a larger hyponastic amplitude than observed, unless a decrease in cell proliferation rate at the proximal abaxial side of the petiole relative to the adaxial side was implemented. Our model predicts that when this differential proliferation mechanism is disrupted by either ectopic overexpression or mutation of CYCA2;1, the hyponastic growth response becomes exaggerated. This is in accordance with experimental observations on CYCA2;1 overexpression lines and cyca2;1 knockouts. We therefore propose a bipartite mechanism controlling leaf movement: ethylene induces longitudinal cell expansion in the abaxial petiole epidermis to induce hyponasty and simultaneously affects its amplitude by controlling cell proliferation through CYCA2;1. Further corroborating the model, we found that ethylene treatment results in transcriptional down-regulation of A2-type CYCLINs and propose that this, and possibly other regulatory mechanisms affecting CYCA2;1, may contribute to this attenuation of hyponastic growth., (© 2015 American Society of Plant Biologists. All Rights Reserved.)

In the natural environment, days are generally warmer than the night, resulting in a positive day/night temperature difference (+DIF). Plants have adapted to these conditions, and when exposed to antiphase light and temperature cycles (cold photoperiod/warm night [-DIF]), most species exhibit reduced elongation growth. To study the physiological mechanism of how light and temperature cycles affect plant growth, we used infrared imaging to dissect growth dynamics under +DIF and -DIF in the model plant Arabidopsis (Arabidopsis thaliana). We found that -DIF altered leaf growth patterns, decreasing the amplitude and delaying the phase of leaf movement. Ethylene application restored leaf growth in -DIF conditions, and constitutive ethylene signaling mutants maintain robust leaf movement amplitudes under -DIF, indicating that ethylene signaling becomes limiting under these conditions. In response to -DIF, the phase of ethylene emission advanced 2 h, but total ethylene emission was not reduced. However, expression analysis on members of the 1-aminocyclopropane-1-carboxylic acid (ACC) synthase ethylene biosynthesis gene family showed that ACS2 activity is specifically suppressed in the petiole region under -DIF conditions. Indeed, petioles of plants under -DIF had reduced ACC content, and application of ACC to the petiole restored leaf growth patterns. Moreover, acs2 mutants displayed reduced leaf movement under +DIF, similar to wild-type plants under -DIF. In addition, we demonstrate that the photoreceptor PHYTOCHROME B restricts ethylene biosynthesis and constrains the -DIF-induced phase shift in rhythmic growth. Our findings provide a mechanistic insight into how fluctuating temperature cycles regulate plant growth.

Upward leaf movement, called hyponastic growth, is employed by plants to cope with adverse environmental conditions. Ethylene is a key regulator of this process and, in Arabidopsis thaliana, hyponasty is induced by this phytohormone via promotion of epidermal cell expansion in a proximal zone of the abaxial side of the petiole. ROTUNDIFOLIA3/CYP90C1 encodes an enzyme which was shown to catalyse C-23 hydroxylation of several brassinosteroids (BRs) - phytohormones involved in, for example, organ growth, cell expansion, cell division, and responses to abiotic and biotic stresses. This study tested the interaction between ethylene and BRs in regulating hyponastic growth. A mutant isolated in a forward genetic screen, with reduced hyponastic response to ethylene treatment, was allelic to rot3. The cause of the reduced hyponastic growth in this mutant was examined by studying ethylene-BR interaction during local cell expansion, pharmacological inhibition of BR synthesis and ethylene effects on transcription of BR-related genes. This work demonstrates that rot3 mutants are impaired in local cell expansion driving hyponasty. Moreover, the inhibition of BR biosynthesis reduces ethylene-induced hyponastic growth and ethylene increases sensitivity to BR in promoting cell elongation in Arabidopsis hypocotyls. Together, the results show that ROT3 modulates ethylene-induced petiole movement and that this function is likely BR related.

Colonization of the land by multicellular green plants was a fundamental step in the evolution of life on earth. Land plants evolved from fresh-water aquatic algae, and the transition to a terrestrial environment required the acquisition of developmental plasticity appropriate to the conditions of water availability, ranging from drought to flood. Here we show that extant bryophytes exhibit submergence-induced developmental plasticity, suggesting that submergence responses evolved relatively early in the evolution of land plants. We also show that a major component of the bryophyte submergence response is controlled by the phytohormone ethylene, using a perception mechanism that has subsequently been conserved throughout the evolution of land plants. Thus a plant environmental response mechanism with major ecological and agricultural importance probably had its origins in the very earliest stages of the colonization of the land., (© 2012 The Authors. The Plant Journal © 2012 Blackwell Publishing Ltd.)

• Hyponastic growth is an upward petiole movement induced by plants in response to various external stimuli. It is caused by unequal growth rates between adaxial and abaxial sides of the petiole, which bring rosette leaves to a more vertical position. The volatile hormone ethylene is a key regulator inducing hyponasty in Arabidopsis thaliana. Here, we studied whether ethylene-mediated hyponasty occurs through local stimulation of cell expansion and whether this involves the reorientation of cortical microtubules (CMTs). • To study cell size differences between the two sides of a petiole in ethylene and control conditions, we analyzed epidermal imprints. We studied the involvement of CMT orientation in epidermal cells using the tubulin marker line as well as genetic and pharmacological means of CMT manipulation. • Our results demonstrate that ethylene induces cell expansion at the abaxial side of the- petiole and that this can account for the observed differential growth. At the abaxial side, ethylene induces CMT reorientation from longitudinal to transverse, whereas, at the adaxial side, it has an opposite effect. The inhibition of CMTs disturbed ethylene-induced hyponastic growth. • This work provides evidence that ethylene stimulates cell expansion in a tissue-specific manner and that it is associated with tissue-specific changes in the arrangement of CMTs along the petiole., (© 2011 The Authors. New Phytologist © 2011 New Phytologist Trust.)

Background and Aims: Complete submergence is an important stress factor for many terrestrial plants, and a limited number of species have evolved mechanisms to deal with these conditions. Rumex palustris is one such species and manages to outgrow the water, and thus restore contact with the atmosphere, through upward leaf growth (hyponasty) followed by strongly enhanced petiole elongation. These responses are initiated by the gaseous plant hormone ethylene, which accumulates inside plants due to physical entrapment. This study aimed to investigate the kinetics of ethylene-induced leaf hyponasty and petiole elongation., Methods: Leaf hyponasty and petiole elongation was studied using a computerized digital camera set-up followed by image analyses. Linear variable displacement transducers were used for fine resolution monitoring and measurement of petiole growth rates., Key Results: We show that submergence-induced hyponastic growth and petiole elongation in R. palustris can be mimicked by exposing plants to ethylene. The petiole elongation response to ethylene is shown to depend on the initial angle of the petiole. When petiole angles were artificially kept at 0 degrees, rather than the natural angle of 35 degrees, ethylene could not induce enhanced petiole elongation. This is very similar to submergence studies and confirms the idea that there are endogenous, angle-dependent signals that influence the petiole elongation response to ethylene., Conclusions: Our data suggest that submergence and ethylene-induced hyponastic growth and enhanced petiole elongation responses in R. palustris are largely similar. However, there are some differences that may relate to the complexity of the submergence treatment as compared with an ethylene treatment.

Plants modify growth in response to the proximity of neighbors. Among these growth adjustments are shade avoidance responses, such as enhanced elongation of stems and petioles, that help plants to reach the light and outgrow their competitors. Neighbor detection occurs through photoreceptor-mediated detection of light spectral changes (i.e. reduced red:far-red ratio [R:FR] and reduced blue light intensity). We recently showed that physiological regulation of these responses occurs through light-mediated degradation of nuclear, growth-inhibiting DELLA proteins, but this appeared to be only part of the full mechanism. Here, we present how two hormones, auxin and ethylene, coregulate DELLAs but regulate shade avoidance responses through DELLA-independent mechanisms in Arabidopsis (Arabidopsis thaliana). Auxin appears to be required for both seedling and mature plant shoot elongation responses to low blue light and low R:FR, respectively. Auxin action is increased upon exposure to low R:FR and low blue light, and auxin inhibition abolishes the elongation responses to these light cues. Ethylene action is increased during the mature plant response to low R:FR, and this growth response is abolished by ethylene insensitivity. However, ethylene is also a direct volatile neighbor detection signal that induces strong elongation in seedlings, possibly in an auxin-dependent manner. We propose that this novel ethylene and auxin control of shade avoidance interacts with DELLA abundance but also controls independent targets to regulate adaptive growth responses to surrounding vegetation.

The slow gas diffusion rate in flooded soil not only causes oxygen deficiency, but also favours the accumulation of ethylene in root systems to concentrations that may strongly affect root elongation. Previously published experiments showed that root elongation in rice is much less strongly inhibited by ethylene than in some other species less well adapted to wet conditions. Rice roots have also been reported to produce abnormally little ethylene. We tested if these traits are typical of wetland species and are thus likely to be widespread adaptive traits. Comparisons using 14 species indicated that insensitivity to the inhibiting effects of ethylene on root elongation is unlikely to be a common feature of temperate wetland species. However, resistance to longitudinal gas diffusion within roots of wetland species, which largely depends on diameter and the presence of gas-filled channels, was found to be less than in non-wetland species. We show that this can help maintain low internal ethylene concentrations by venting accumulated gas to the shoot and atmosphere.

The gaseous plant hormone ethylene modulates many internal processes and growth responses to environmental stimuli. Ethylene has long been recognized as a growth inhibitor, but evidence is accumulating that ethylene can also promote growth. Therefore, the concept of ethylene as a general growth inhibitor needs reconsideration: a close examination of recent literature can help to understand the two contrasting faces of growth control by ethylene. Here, we propose a hypothesis that integrates growth inhibition and growth stimulation into one biphasic ethylene response model. Focusing on photosynthesis and cell expansion, we highlight several mechanisms through which ethylene affects plant growth, thereby interacting with various other signal transduction routes.

Plants can reorient their organs in response to changes in environmental conditions. In some species, ethylene can induce resource-directed growth by stimulating a more vertical orientation of the petioles (hyponasty) and enhanced elongation. In this study on Arabidopsis (Arabidopsis thaliana), we show significant natural variation in ethylene-induced petiole elongation and hyponastic growth. This hyponastic growth was rapidly induced and also reversible because the petioles returned to normal after ethylene withdrawal. To unravel the mechanisms behind the natural variation, two contrasting accessions in ethylene-induced hyponasty were studied in detail. Columbia-0 showed a strong hyponastic response to ethylene, whereas this response was almost absent in Landsberg erecta (Ler). To test whether Ler is capable of showing hyponastic growth at all, several signals were applied. From all the signals applied, only spectrally neutral shade (20 micromol m(-2) s(-1)) could induce a strong hyponastic response in Ler. Therefore, Ler has the capacity for hyponastic growth. Furthermore, the lack of ethylene-induced hyponastic growth in Ler is not the result of already-saturating ethylene production rates or insensitivity to ethylene, as an ethylene-responsive gene was up-regulated upon ethylene treatment in the petioles. Therefore, we conclude that Ler is missing an essential component between the primary ethylene signal transduction chain and a downstream part of the hyponastic growth signal transduction pathway.

Plants respond to proximate neighbors with a suite of responses that comprise the shade avoidance syndrome. These phytochrome-mediated responses include hyponasty (i.e. a more vertical orientation of leaves) and enhanced stem and petiole elongation. We showed recently that ethylene-insensitive tobacco (Nicotiana tabacum) plants (Tetr) have reduced responses to neighbors, showing an important role for this gaseous plant hormone in shade avoidance. Here, we investigate interactions between phytochrome signaling and ethylene action in shade avoidance responses. Furthermore, we investigate if ethylene acts in these responses through an interaction with the GA class of hormones. Low red to far-red light ratios (R:FR) enhanced ethylene production in wild-type tobacco, resulting in shade avoidance responses, whereas ethylene-insensitive plants showed reduced shade avoidance responses. Plants with inhibited GA production showed hardly any shade avoidance responses at all to either a low R:FR or increased ethylene concentrations. Furthermore, low R:FR enhanced the responsiveness of hyponasty and stem elongation in both wild-type and Tetr plants to applied GA(3), with the stem elongation process being more responsive to GA(3) in the wild type than in Tetr. We conclude that phytochrome-mediated shade avoidance responses involve ethylene action, at least partly by modulating GA action.

Plant competition for light is a commonly occurring phenomenon in natural and agricultural vegetations. It is typically size-asymmetric, meaning that slightly larger individuals receive a disproportionate share of the light, leaving a limited amount of light for the initially smaller individuals. As a result, size inequalities of such stands increase with competition intensity. A plant's ability to respond morphologically to the presence of neighbour plants with enhanced shoot elongation, the so-called shade avoidance response, acts against the development of size inequalities. This has been shown experimentally with transgenic plants that cannot sense neighbours and, therefore, show no shade avoidance responses. Stands of such transgenic plants showed a much stronger development of size inequalities at high plant densities than did wild type (WT) stands. However, the transgenic plants used in these experiments displayed severely hampered growth rates and virtually no response to neighbours. In order to more precisely study the impact of this phenotypic plasticity on size inequality development, experiments required plants that have normal growth rates and reduced, but not absent, shade avoidance responses. We made use of an ethylene-insensitive, transgenic tobacco genotype (Tetr) that has wild type growth rates and moderately reduced shade avoidance responses to neighbours. Here, we show that the development of size inequalities in monocultures of these plants is not affected unambiguously different from wild type monocultures. Plots of Tetr plants developed higher inequalities for stem length than did WT, but monocultures of the two genotypes had identical CV (Coefficient of Variance) values for shoot biomass that increased with plant density. Therefore, even though reduced shade avoidance capacities led to the expected higher size inequalities for stem length, this does not necessarily lead to increased size inequalities for shoot biomass.