Nucleic acid damage and DNA damage repair are affected by freezing stress in annual wheat (Triticum aestivum) and by both plant age and freezing in its perennial relative (Thinopyrum intermedium)

Authors: JAIKUMAR, NIKHIL - University Of Illinois; Dorn, Kevin; BAAS, DEAN - Michigan State University; WILKE, BROOK - Michigan State University; KAPP, CHRISTIAN - Michigan State University; SNAPP, SIEGLINDE - Michigan State University

Submitted to: American Journal of Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/28/2020
Publication Date: 12/19/2020
Citation: Jaikumar, N.S., Dorn, K.M., Baas, D., Wilke, B., Kapp, C., Snapp, S. 2020. Nucleic acid damage and DNA damage repair are affected by freezing stress in annual wheat (Triticum aestivum) and by both plant age and freezing in its perennial relative (Thinopyrum intermedium). American Journal of Botany. 107(12):1693-1709. https://doi.org/10.1002/ajb2.1584.
DOI: https://doi.org/10.1002/ajb2.1584

Interpretive Summary: Many crop plants are exposed to cold and freezing temperatures throughout their life cycles, which can cause significant damage. Overwintering annual crops and perennial crops have varying levels of resistance to cold or freezing damage, derived from several different molecular adaptations in response to these conditions. In this study, the expression of a set of genes encoding DNA repair and antioxidative enzymes was examined in two annual cereal crops (winter wheat and barley) and one perennial relative (Thinopyrum intermedium, also known as intermediate wheatgrass) between intermittent freezing stress and non-freezing conditions. We found that freezing stress caused changes in expression of genes that encode several DNA repair and antioxidative proteins. In the perennial species, Thinopyrum intermedium, that lives for several years, younger plants exhibited a higher level of oxidative damage to RNA. Overall, the control of DNA repair genes seems to influence cold acclimation and resistance to cold and freezing damage in the species studied here.

Technical Abstract: Premise of the study: Few previous studies have considered how nucleic acid damage and damage repair processes may play a role in cold stress adaptation. A further under-explored question concerns how age affects tolerance to cold stress among mature cohorts of perennials. Methods: Oxidative damage to RNA, and expression of genes involved in DNA repair were compared in multiple mature cohorts of of Thinopyrum intermedium plants (an emerging perennial cereal), as well as in two annual cereals (winter wheat and barley) under intermittent freezing stress and under non-freezing conditions. Thinopyrum cohorts were of similar size and reproductive status. Activity of five antioxidative enzymes was also measured under freezing and non-freezing conditions: catalase, superoxide dismutase, ascorbate peroxidase, glutathione peroxidase (GPX), and glutathione reductase (GR). DNA repair genes considered included photolyases involved in repairing ultraviolet-induced damage (PHR1A, PHR1B) and two genes involved in repairing oxidatively induced damage (ERCC1, RAD23). Results: • Freezing stress was accompanied by large increases in photolyase expression and in GPX activity (in all three species) and in ERCC1 expression (in Thinopyrum). • This is the first report of DNA photolyases being overexpressed under freezing stress. • Older Thinopyrum had lower expression of PHR1A, and lower expression of ERCC1 and higher GPX activity (under cold stress). • Younger Thinopyrum sustained more oxidative damage to RNA. Conclusions: Overexpression of DNA repair genes appears to be an important aspect of cold acclimation. When comparing adult cohorts, aging was associated with changes in the freezing stress response, but not with overall increases or decreases in stress tolerance.