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Open Access Research article

Evidence for extensive heterotrophic metabolism, antioxidant action, and associated regulatory events during winter hardening in Sitka spruce

Eva Collakova1, Curtis Klumas2, Haktan Suren23, Elijah Myers2, Lenwood S Heath4, Jason A Holliday3 and Ruth Grene1*

Author Affiliations

1 Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA, 24061, USA

2 Genetics, Bioinformatics and Computational Biology Program, Virginia Tech, Blacksburg, VA, 24061, USA

3 Department of Forest Resources and Environmental Conservation, Virginia Tech, Blacksburg, VA, 24061, USA

4 Department of Computer Science, Virginia Tech, Blacksburg, VA, 24061, USA

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BMC Plant Biology 2013, 13:72  doi:10.1186/1471-2229-13-72

Published: 30 April 2013

Abstract

Background

Cold acclimation in woody perennials is a metabolically intensive process, but coincides with environmental conditions that are not conducive to the generation of energy through photosynthesis. While the negative effects of low temperatures on the photosynthetic apparatus during winter have been well studied, less is known about how this is reflected at the level of gene and metabolite expression, nor how the plant generates primary metabolites needed for adaptive processes during autumn.

Results

The MapMan tool revealed enrichment of the expression of genes related to mitochondrial function, antioxidant and associated regulatory activity, while changes in metabolite levels over the time course were consistent with the gene expression patterns observed. Genes related to thylakoid function were down-regulated as expected, with the exception of plastid targeted specific antioxidant gene products such as thylakoid-bound ascorbate peroxidase, components of the reactive oxygen species scavenging cycle, and the plastid terminal oxidase. In contrast, the conventional and alternative mitochondrial electron transport chains, the tricarboxylic acid cycle, and redox-associated proteins providing reactive oxygen species scavenging generated by electron transport chains functioning at low temperatures were all active.

Conclusions

A regulatory mechanism linking thylakoid-bound ascorbate peroxidase action with “chloroplast dormancy” is proposed. Most importantly, the energy and substrates required for the substantial metabolic remodeling that is a hallmark of freezing acclimation could be provided by heterotrophic metabolism.

Keywords:
Microarray; Sitka spruce; Carbon metabolism; Cell walls; Adaptation mechanisms; Visualization