Abstract
Chilling stress can cause cellular DNA damage, affecting the faithful transmission of genetic information. Cold acclimation enhances chilling tolerance, but it is not clear that the process of cold adaption involves DNA damage responses, as cold acclimation does not form real chilling stress. Here we showed with cucumber fruit that pre-storage cold acclimation (PsCA) reduces chilling injury and upregulates DNA damage inducible protein1 (CsDDI1), suggesting that the chilling tolerance induced by cold acclimation involves CsDDI1 transcription. Application of nitric oxide (NO), abscisic acid (ABA) or H2O2 biosynthesis inhibitor before PsCA treatment downregulates CsDDI1 and aggravates chilling injury, while H2O2 generation inhibition plus exogenous NO or ABA application before PsCA treatment restores chilling tolerance, but does not restore CsDDI1 expression, suggesting H2O2 plays a crucial role in triggering cold adaption. CsDDI1 overexpression Arabidopsis lines show faster growth, stronger chilling tolerance, lower reactive oxygen species levels, enhanced catalase and superoxide dismutase activities and higher expression of nine other Arabidopsis defense genes under chilling stress, suggesting CsDDI1 strengthens defenses against chilling stress by enhancing antioxidant defense system. Taken together, CsDDI1 positively regulates chilling tolerance induced by cold acclimation in cucumber. In addition, H2O2 is involved in initiation of cold acclimation. While CsDDI1 upregulation requires H2O2 as a key signaling molecule, the upregulation of CsDDI1 activates an antioxidant system to reduce biotoxic accumulation of H2O2 and helps in DNA repair.
Highlights
Plants have evolved the ability to cope with various environmental stresses to ensure survival and proliferation, including solar UV and ionizing radiation, chemical mutagens, heavy metals, droughts, heat, pathogenic attacks, and chilling
We investigated expression patterns during pre-storage cold acclimation (PsCA) treatment and cold storage for DDI1, DDR1 and DDB1, which are all involved in DNA repair responses (Al Khateeb and Schroeder, 2009; Fujimori et al, 2014; Maric et al, 2017)
In fruit exposed to cold stress from the very beginning, CsDDI1 expression remained almost unchanged until 6 d, while that of the PsCA-treated cucumber significantly increased following 3 d of cold acclimation and kept increasing even after the fruit were placed in chilling stress condition (Figure 1A)
Summary
Plants have evolved the ability to cope with various environmental stresses to ensure survival and proliferation, including solar UV and ionizing radiation, chemical mutagens, heavy metals, droughts, heat, pathogenic attacks, and chilling. DNA damage may result in changes to both the chemical and physical structures of DNA, which can seriously threaten the survival and the faithful transmission of genetic information in plants (Zhang et al, 2015a; Ding et al, 2016). DNA damage-inducible (DDI) proteins are usually related to plant defense responses and play important roles in DNA repair pathways (Maric et al, 2017). Arabidopsis DNA damage-inducible protein 1 (AtDDI1) participates in plant defense responses against abiotic stresses such as drought and salt by regulating the expression of defense genes (Ding et al, 2016)
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