Auxin and Ethylene Regulate Elongation Responses to Neighbor Proximity Signals Independent of Gibberellin and DELLA Proteins in Arabidopsis      

Abstract

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.

Local auxin production underlies a spatially restricted neighbor-detection response inArabidopsis

“…In addition, the petiole vasculature also corresponds to a site of strong shade-induced IAA19/MSG2 expression ( Fig. S8 A and B) (38). Finally, the msg2 mutant expressing a stable form of the IAA19 protein has a reduced hyponastic response in low R/FR (Fig.…”

“…Low R/FR enhanced the GUS signal, particularly in the petiole vasculature of expanding leaves (Fig. S8 A and B) (38). To determine the functional importance of IAA19 in this process, we used the massugu2 (msg2) allele expressing a stabilized IAA19 auxin-signaling inhibitor (39).…”

Contributions of green light to plant growth and development

“…A low red to far-red ratio can dramatically stimulate ethylene biosynthesis in both tobacco and Arabidopsis plants ( Pierik et al, 2004a( Pierik et al, , 2009. Increased levels of gaseous ethylene promote stem and petiole elongation, but have little effect on leaf hyponastic growth.…”

“…The depletion of blue light by canopy or neighboring plants can induce SAS-like responses ( Ballaré et al, 1991a ;Ballaré et al, 1991b ;Pierik et al, 2004b ;Keuskamp et al, 2011 ). The responses to low blue light are dependent upon ethylene and mediated by cryptochromes ( Pierik et al, 2009 ).…”

Neighbor Detection Induces Organ-Specific Transcriptomes, Revealing Patterns Underlying Hypocotyl-Specific Growth

“…In particular, brassinosteroids, gibberellic acid (GA), and jasmonic acid have been shown to function in growth regulation in shaded environments (DjakovicPetrovic et al, 2007;Kozuka et al, 2010;Robson et al, 2010;Keller et al, 2011;Keuskamp et al, 2011;Cifuentes-Esquivel et al, 2013;Bou-Torrent et al, 2014;Moreno and Ballaré, 2014;Nozue et al, 2015;Das et al, 2016;Procko et al, 2016). Abscisic acid (ABA), cytokinins, and ethylene have also been linked to a subset of shaderegulated responses (Carabelli et al, 2007;Pierik et al, 2009;Reddy et al, 2013;Zheng et al, 2013;Pierik and Testerink, 2014). A recurrent problem with many transcriptional studies is that shaderegulated growth is most often measured in hypocotyls but is being correlated with gene expression analyzed in whole seedlings/ plants.…”