Metabolic changes in Avena sativa crowns recovering from freezing

Authors: Henson, Cynthia; DUKE, STANLEY - University Of Wisconsin; Livingston, David

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2014
Publication Date: 3/27/2014
Citation: Henson, C.A., Duke, S., Livingston, D.P. 2014. Metabolic changes in Avena sativa crowns recovering from freezing. PLoS One. 9(3):e93085. DOI:10.1371/journal.pone.0093085.

Interpretive Summary: The ability of plants to recover from freezing is one of the most crucial aspects of successfully growing winter crops such as wheat barley oats and rye in northern regions of the US. Most research studying winter hardiness in crops has focused on the adaptation of plants in the fall prior to freezing, a period called cold-acclimation. The ability of plants to recover from freezing stress in the spring is an important aspect of overall winter hardiness which has received very little attention from stress physiologists. We investigated the most freezing sensitive winter cereal, oat by looking at the crown from a metabolic point of view. We froze plants and then at specific time periods while they were recovering took samples from crown tissue (the region where new growth is initiated after freezing). A previous study indicated that at day 7 a distinct region of cells forming a rough spherical shape had developed. This region of cells formed a barrier that separated living from dead tissue. To see if we could determine a metabolic reason for this barrier, we analyzed crown tissue of frozen and unfrozen plants during recovery from freezing for changes in a battery of metabolites. Significant differences between frozen and unfrozen plants confirmed that plants which had been frozen had a distinctly different pattern of metabolism than those which had not frozen. Several of the pathways we identified were involved in stress response and cell repair mechanisms. This means that much of the energy stored in the fall is likely necessary for rebuilding cellular structures that have been damaged or destroyed by freezing. This research will help breeders identify individual genes that may be important to incorporate into existing cultivars to help survive winter and to grow winter crops further north.

Technical Abstract: Extensive research has been conducted on cold acclimation and freezing tolerance of fall-sown cereal plants due to their economic importance; however, little has been reported on the biochemical changes occurring over time after the freezing conditions are replaced by conditions favorable for recovery and growth such as would occur during spring. In this study, GC-MS was used to detect metabolic changes in the overwintering crown tissue of oat (Avena sativa L.) during a fourteen day time-course after freezing. Metabolomic analysis revealed increases in most amino acids, particularly proline, 5-oxoproline and arginine, which increased greatly in crowns that were frozen compared to controls and correlated very significantly with days after freezing. In contrast, sugar and sugar related metabolites were little changed by freezing, except sucrose and fructose which decreased dramatically. In frozen tissue all TCA cycle metabolites, but especially citrate and malate, decreased in relation to unfrozen tissue. Alterations in some amino acid pools after freezing were similar to those observed in cold acclimation whereas most changes in sugar pools after freezing were not. These similarities and differences suggest that there are common as well as unique genetic mechanisms between these two environmental conditions that are crucial to the winter survival of plants.