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Ethylene-mediated regulation of A2-type CYCLINs modulates hyponastic growth in arabidopsis

Polko, J.K., van Rooij, J.A., Vanneste, S., Pierik, R., Ammerlaan, A.M.H., Vergeer-Van Eijk, M.H., McLoughlin, F., Guhl, K., Van Isterdael, G., Voesenek, L.A.C.J., Millenaar, F.F., Beeckman, T., Peeters, A.J.M., Maree, A.F.M. and van Zanten, M. 2015. Ethylene-mediated regulation of A2-type CYCLINs modulates hyponastic growth in arabidopsis. Plant Physiology 169 (1) , pp. 194-208. 10.1104/pp.15.00343

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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. Plants have acquired mechanisms to adjust growth and secure reproduction under unfavorable environmental conditions. Among the strategies to avoid adverse conditions is upward leaf movement, called hyponastic growth. This leaf reorientation is driven by unequal growth rates between adaxial and abaxial sides of the petiole (Cox et al., 2004; Polko et al., 2012b). Arabidopsis (Arabidopsis thaliana) exhibits hyponasty upon several environmental signals (e.g. submergence, waterlogging, proximity of neighboring vegetation, low red:far-red light ratios, reduced blue light fluence rates, low light intensities, and high temperatures; Millenaar et al., 2005, 2009; Mullen et al., 2006; Koini et al., 2009; Moreno et al., 2009; Van Zanten et al., 2009; Keuskamp et al., 2010; Keller et al., 2011; Vasseur et al., 2011; De Wit et al., 2012; Rauf et al., 2013; Dornbusch et al., 2014). Hyponasty alleviates the impact of environmental stresses (Van Zanten et al., 2010b). During submergence, it allows reestablishment of gas exchange with the atmosphere (e.g. Cox et al., 2003); at high plant densities, it positions the leaves in better lit layers of the canopy to improve light interception (e.g. De Wit et al., 2012); and at high temperatures, it improves the cooling capacity of the leaves (Crawford et al., 2012; Bridge et al., 2013). The cellular basis of hyponastic growth in Rumex palustris (Cox et al., 2004) and Arabidopsis (Polko et al., 2012b; Rauf et al., 2013) has been characterized. Ethylene causes reorientation of cortical microtubules (CMTs) in the petiole, which leads to longitudinal cell expansion in an approximately 2-mm-long epidermal cell zone at the proximal part of the abaxial side of the organ (Polko et al., 2012b). The interactions between several hormones (e.g. ethylene, abscisic acid, GAs, and auxin) in controlling hyponasty under various conditions have been studied (Mullen et al., 2006; Benschop et al., 2007; Millenaar et al., 2009; Van Zanten et al., 2009, 2010b; Peña-Castro et al., 2011). The volatile phytohormone ethylene is a key component in the complex regulatory network of hyponastic growth. Ethylene is the trigger and a positive regulator of hyponastic growth in submerged and waterlogged Arabidopsis (Millenaar et al., 2005, 2009; Van Zanten et al., 2010b; Rauf et al., 2013) and a negative regulator of high temperature-induced hyponasty (Van Zanten et al., 2009), but is not involved in low light-induced hyponastic growth in this species (Millenaar et al., 2009). Abscisic acid antagonizes ethylene-induced hyponasty (Benschop et al., 2007) and is a positive regulator of high temperature-induced hyponastic growth (Van Zanten et al., 2009). The growth-promoting GAs positively regulate hyponastic response to all three environmental signals (Peña-Castro et al., 2011), whereas auxins promote low light and high temperature-induced hyponastic growth (Millenaar et al., 2005; Koini et al., 2009; Van Zanten et al., 2009), as well as low red:far-red- and low blue light-induced hyponasty (Moreno et al., 2009; Keller et al., 2011). Finally, brassinosteroids also positively regulate ethylene-induced hyponasty (Polko et al., 2013). Despite the extensive knowledge on hormonal regulation of hyponasty, little is known about the molecular genetic mechanisms that drive this response. One notable exception is the study by Rauf et al. (2013), who showed that hyponastic growth in Arabidopsis in response to root waterlogging is controlled by the NAC (for No Apical Meristem [NAM], Arabidopsis Transcription Activation Factor) transcription factor SPEEDY HYPONASTIC GROWTH that directly affects expression of the ethylene biosynthesis gene 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID (ACC) OXIDASE5. Here, we followed a forward genetic approach to identify unique components that control hyponastic growth in Arabidopsis. From a population of activation-tagged plants (Weigel et al., 2000), we isolated Enhanced Hyponasty-D (EHY-D), which showed exaggerated hyponasty under exogenous ethylene application, low light intensities, and high temperature. We found that ectopic expression of the core cell cycle regulator CYCLINA2;1 (CYCA2;1) caused the exaggerated ethylene-induced leaf movement of EHY-D. Mathematical analyses indicated that, besides promoting cell expansion, ethylene can also attenuate the amplitude of hyponasty by affecting differential cell proliferation in the petiole of wild-type plants. We suggest that this occurs through ethylene-dependent effects on CYCA2;1 levels, activity, or sensitivity in petioles of wild-type plants. The ethylene-mediated transcriptional regulation of CYCA2;1 observed here could contribute to this. In EHY-D, however, ethylene-mediated effects on cell proliferation are overruled by ectopic CYCA2;1 overexpression, which consequently results in enhanced hyponasty, in accordance with the predictions of our model. Correspondingly, cyca2;1 knockout lines where ethylene cannot affect CYCA2;1-mediated cell proliferation also exhibited enhanced hyponasty. Our data therefore describe a mechanism by which hyponastic growth is kept within limits, through a bipartite role for ethylene: within the same organ, ethylene initiates hyponastic growth by promoting cell elongation, while simultaneously attenuating the response by regulation of A2-type CYCLIN-mediated cell proliferation.

Item Type: Article
Date Type: Published Online
Status: Published
Schools: Biosciences
Publisher: American Society of Plant Biologists
ISSN: 0032-0889
Last Modified: 14 Feb 2019 08:30

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