Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis

Abstract

As sessile organisms, plants must sense environmental conditions and adjust their growth and development processes accordingly, through adaptive responses regulated by various internal factors, including hormones. A key environmental factor is temperature, but temperature-sensing mechanisms are not fully understood despite intense research. We investigated proteomic responses to temperature shocks (15 min cold or heat treatments) with and without exogenous applications of cytokinin in Arabidopsis. Image and mass spectrometric analysis of the two-dimensionally separated proteins detected 139 differentially regulated spots, in which 148 proteins were identified, most of which have not been previously linked to temperature perception. More than 70% of the temperature-shock response proteins were modulated by cytokinin, mostly in a similar manner as heat shock. Data mining of previous transcriptomic datasets supported extensive interactions between temperature and cytokinin signalling. The biological significance of this finding was tested by assaying an independent growth response of Arabidopsis seedlings to heat stress: hypocotyl elongation. This response was strongly inhibited in mutants with deficiencies in cytokinin signalling or endogenous cytokinin levels. Thus, cytokinins may directly participate in heat signalling in plants. Finally, large proportions of both temperature-shock and cytokinin responsive proteomes co-localize to the chloroplast, which might therefore host a substantial proportion of the temperature response machinery.

Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways

“…A rapid proteomic heat-shock response that could be mimicked to some extent by cytokinin treatment at standard temperature has also been reported [136], indicating that cytokinin may play a role in temperature perception. Moreover, the accumulation of cytokinin has been observed in Pinus radiata under prolonged heat stress and in recovered plants [137,138].…”

“…Accordingly, transgenic lines with inactivated components of cytokinin signalling pathways or reductions in pools of active cytokinin have displayed increased tolerance to high temperatures [141,142]. Further, analyses of temperature-induced hypocotyl growth in cytokinin-deficient transgenic plants and cytokinin receptor ahk double mutants have shown that impairment of the cytokinin pathway strongly inhibits growth at high temperatures [136]. This indicates that cytokinin could serve as a signal for thermomorphogenesis.…”

Heat Acclimation and Inhibition of Cytokinin Degradation Positively Affect Heat Stress Tolerance of Arabidopsis

“…In the case of heat stress, CK effect on stomata opening followed by stimulation of leaf transpiration was found to be crucial at the early phase of the stress response (Mackova et al, 2013;Dobra et al, 2015;Skalak et al, 2016). Further, a large number of heat stress affected genes are CK-responsive (Cerny et al, 2014). CKs stimulate the antioxidant system upon heat stress .…”

Low doses of triazine xenobiotics mobilize ABA and cytokinin regulations in a stress- and low-energy-dependent manner

“…may interfere with CK pathways involved in modulation of low and high temperature shocks [80,107], or directly with temperature-related perception and transduction [101].…”