Ethylene-Mediated Regulation of A2-Type CYCLINs Modulates Hyponastic Growth in Arabidopsis  

Abstract

(S.V., G.V.I., T.B.)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.

Interregulation of CDKA/CDK1 and the Plant-Specific Cyclin-Dependent Kinase CDKB in Control of the Chlamydomonas Cell Cycle

“…The various cyclins are expressed in distinct but overlapping patterns in different tissues and developmental stages. Some A-type cyclins respond specifically to certain hormones or developmental transitions (Vanneste et al 2011;Polko et al 2015). A-type cyclins also regulate transitions from mitotic cycles to endocycles of DNA replication (Imai et al 2006).…”

Ethylene and Hormonal Cross Talk in Vegetative Growth and Development

“…In leaves, ethylene was shown to cause cell cycle arrest upon mild osmotic stress, through the inhibition of CYCLIN-DEPENDENT KINASE A activity and independently from EIN3 transcriptional control (Skirycz et al, 2011). Ethylene also inhibits the mitotic cell cycle in the abaxial cells of the leaf petiole through the down-regulation of CYCLIN2A;1 expression, partially contributing to the hyponastic response (Polko et al, 2015).…”

Transcriptomic analysis of submergence-tolerant and sensitive Brachypodium distachyon ecotypes reveals oxidative stress as a major tolerance factor

“…Recently, it has been shown that the gaseous hormone ethylene, which accumulates around submerged tissues, coordinates cell expansion and division to promote the hyponastic response through the inhibition of CYCLINA2;1 expression ( CYCA2 )24.…”

“…The management of low light accessibility is achieved through a set of molecular events leading to increased angle (hyponastic) repositioning of the leaves outside the water level, thus raising the possibility of sustaining photosynthetic activity under stress 7 . Recently, it has been shown that the gaseous hormone ethylene, which accumulates around submerged tissues, coordinates cell expansion and division to promote the hyponastic response through the inhibition of CYCLINA2;1 expression ( CYCA2 ) 24 .…”