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

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.

Understanding developmental and adaptive cues in pine through metabolite profiling and co-expression network analysis

“…These genes may participate in the maintenance of basal cellular functions when photosynthetic rates are low, or in general adaptations to cold conditions, as previously reported in stems of P. glauca during preparation for overwintering ( Galindo-González et al , 2012 ) or in P. sitchensis ( Grene et al , 2012 ; Collakova et al , 2013 ). Upregulation of glycolysis, the TCA cycle, oxidative phosphorylation, and other energy-generating pathways during winter is essential for plants to survive the reductions in photosynthetic generation of ATP ( Ophir et al , 2009 ; Grene et al , 2012 , Galindo-González et al , 2012 ; Collakova et al , 2013 ). Functional enrichment in the turquoise module suggests that it is involved in associated metabolic reorganization during the winter ( Supplementary Data S7 ), including adaptation of carbohydrate metabolism and oxidative phosphorylation ( Supplementary Data S7 and Fig.…”

“…Essential responses to these environmental changes include accumulation of ‘compatible solutes’ to maintain protein stability and cellular integrity under frost stress ( Galindo-González et al , 2012 ; Simard et al , 2013 ), with adjustments of membrane lipid composition to maintain their fluidity ( Roden et al , 2009 ). Clearly, when photosynthesis is reduced cell energy requirements must be met through metabolic pathways such as glycolysis or oxidative phosphorylation ( Ophir et al , 2009 ; Grene et al , 2012 ; Galindo-González et al , 2012 ; Collakova et al , 2013 ). Accordingly, photosynthetic rates and capacities of adult needles are temperature- and/or photoperiod-dependent, peaking in the summer ( Öquist and Huner, 2003 ).…”

Biochemical analysis on crop shoots of Camellia sinensis (L.) O. Kuntze tea from the selected UPASI-16 clone.

“…Peroxidase helps in the conversion of Theaflavins (TF) to Thearubigins (TR) by utilizing H 2 O 2 as an electron acceptor using catechin as a substrate (28). The peroxidase activity increased/decreased in the following order: first internode > bud > first leaf > second leaf > third leaf ( ity was maximum in the first internode (729.72 µM of O 2 formed min -1 g -1 dry weight) followed by bud (727.00 µM of O 2 formed min -1 g -1 dry weight) than the other parts (first leaf, second leaf and third leaf) in UPASI-16.…”

Mutation of the rice TCM12 gene encoding 2,3‐bisphosphoglycerate‐independent phosphoglycerate mutase affects chlorophyll synthesis, photosynthesis and chloroplast development at seedling stage at low temperatures

“…The energy requirements for plant development and growth must be met through metabolic pathways such as glycolysis or oxidative phosphorylation in cool conditions or when photosynthesis is reduced (Collakova et al . ; Cañas et al . ).…”