Abstract

BackgroundCold 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.ResultsThe 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.ConclusionsA 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.

Highlights

  • 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

  • Photosynthesis and respiration The vast majority of responsive genes associated with chloroplast function were down-regulated after the time point 2 (TP2) and remained in that state for the duration of the time course (Figure 1 and Additional file 1: Table S1)

  • A spruce homolog of the disulfide oxidoreductase ROXY1, which has a regulatory role in angiosperm flower development, was highly up-regulated at the later time points

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Summary

Introduction

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. The photosynthetic apparatus is prone to oxidative damage as temperatures drop due to energetic and metabolic imbalance [8] This imbalance is a result of the temperature dependency of metabolic processes, including photochemistry. Highenergy electrons produced in excess reduce molecular oxygen to generate ROS causing photosystem damage [9] In evergreen conifers, such oxygen reduction in a Mehlertype reaction is coupled to antioxidant defenses and represents an important mechanism of dissipating excess energy absorbed by photosystem I at low temperatures [8,10]

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