Abstract

Changes in the stomatal aperture in response to CO2 levels allow plants to manage water usage, optimize CO2 uptake and adjust to environmental stimuli. The current study reports that sub-ambient CO2 up-regulated the low temperature induction of the C-repeat Binding Factor (CBF)-dependent cold signaling pathway in Arabidopsis (Arabidopsis thaliana) and the opposite occurred in response to supra-ambient CO2. Accordingly, cold induction of various downstream cold-responsive genes was modified by CO2 treatments and expression changes were either partially or fully CBF-dependent. Changes in electrolyte leakage during freezing tests were correlated with CO2′s effects on CBF expression. Cold treatments were also performed on Arabidopsis mutants with altered stomatal responses to CO2, i.e., high leaf temperature 1-2 (ht1-2, CO2 hypersensitive) and β-carbonic anhydrase 1 and 4 (ca1ca4, CO2 insensitive). The cold-induced expression of CBF and downstream CBF target genes plus freezing tolerance of ht1-2 was consistently less than that for Col-0, suggesting that HT1 is a positive modulator of cold signaling. The ca1ca4 mutant had diminished CBF expression during cold treatment but the downstream expression of cold-responsive genes was either similar to or greater than that of Col-0. This finding suggested that βCA1/4 modulates the expression of certain cold-responsive genes in a CBF-independent manner. Stomatal conductance measurements demonstrated that low temperatures overrode low CO2-induced stomatal opening and this process was delayed in the cold tolerant mutant, ca1ca4, compared to the cold sensitive mutant, ht1-2. The similar stomatal responses were evident from freezing tolerant line, Ox-CBF, overexpression of CBF3, compared to wild-type ecotype Ws-2. Together, these results indicate that CO2 signaling in stomata and CBF-mediated cold signaling work coordinately in Arabidopsis to manage abiotic stress.

Highlights

  • Cold stress is one of the significant environmental stresses that can severely impact crop yields and limit plant species’ geographical distribution.many terrestrial plants have developed strategies to survive prolonged exposures to low and freezing temperatures [1]

  • The current study reports that sub-ambient CO2 up-regulated the low temperature induction of the C-repeat Binding Factor (CBF)-dependent cold signaling pathway in Arabidopsis (Arabidopsis thaliana) and the opposite occurred in response to supra-ambient CO2

  • These results indicate that CO2 signaling in stomata and CBF-mediated cold signaling work coordinately in Arabidopsis to manage abiotic stress

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Summary

Introduction

Cold stress (freezing or chilling temperatures) is one of the significant environmental stresses that can severely impact crop yields and limit plant species’ geographical distribution.many terrestrial plants have developed strategies to survive prolonged exposures to low and freezing temperatures [1]. Cold acclimation in higher plants involves various physiological and molecular changes that enhance freezing tolerance regulated by both CBF (C-repeat-binding factors)-dependent and -independent pathways [2]. In Arabidopsis and other plant species, cold stress induces the expression of CBF transcription factors, which subsequently activate downstream molecular cascades of COR genes [9,10,11]. More than 3000 COR genes displayed a significant change in their expression levels in the mutants of CBF1 to CBF3 compared to the wild-type plants after being treated at 4 ◦C for 12 h [12]. Proteins synthesized from COR genes act as cryoprotectants and enhance low temperature tolerance, and the ability of plants to survive episodes of frost [3,4,17,18,19,20]

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