Varying Atmospheric CO2 Mediates the Cold-Induced CBF-Dependent Signaling Pathway and Freezing Tolerance in Arabidopsis

Jinyoung Y Barnaby; Joonyup Kim; Mura Jyostna Devi; David H Fleisher; Mark L Tucker; Vangimalla R Reddy; Richard C Sicher

doi:10.3390/ijms21207616

Varying Atmospheric CO₂ Mediates the Cold-Induced CBF-Dependent Signaling Pathway and Freezing Tolerance in Arabidopsis

Int J Mol Sci. 2020 Oct 15;21(20):7616. doi: 10.3390/ijms21207616.

Authors

Jinyoung Y Barnaby^{1

2}, Joonyup Kim³, Mura Jyostna Devi¹, David H Fleisher¹, Mark L Tucker³, Vangimalla R Reddy¹, Richard C Sicher¹

Affiliations

¹ Adaptive Cropping Systems Laboratory, Agricultural Research Service, USDA, Building 001, 10300 Baltimore Ave., Beltsville, MD 20705, USA.
² Dale Bumpers National Rice Research Center, Agricultural Research Service, USDA, Building 001, 10300 Baltimore Ave., Beltsville, MD 20705, USA.
³ Soybean Genomics and Improvement Laboratory, Agricultural Research Service, USDA, Building 006, 10300 Baltimore Ave., Beltsville, MD 20705, USA.

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 CO_2'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.

Keywords: C-repeat binding factor; abiotic stress; atmospheric CO2; carbon dioxide; cold-responsive gene; freezing tolerance; stomatal regulation.

MeSH terms

Acclimatization / drug effects*
Arabidopsis
Arabidopsis Proteins / genetics
Arabidopsis Proteins / metabolism
Atmosphere / chemistry
Carbon Dioxide / analysis
Carbon Dioxide / pharmacology*
Cold-Shock Response / drug effects*
Freezing
Signal Transduction*
Transcription Factors / genetics
Transcription Factors / metabolism

Substances

Arabidopsis Proteins
DREB1A protein, Arabidopsis
Transcription Factors
Carbon Dioxide