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. 2016 Jul 1;16(1):149.
doi: 10.1186/s12870-016-0839-8.

Integrated analysis of gene expression from carbon metabolism, proteome and metabolome, reveals altered primary metabolism in Eucalyptus grandis bark, in response to seasonal variation

Ilara Gabriela Frasson Budzinski  1 , David H Moon  1 , Júlia Silva Morosini  1 , Pernilla Lindén  2 , Juliano Bragatto  1 , Thomaz Moritz  2 , Carlos Alberto Labate  3
Affiliations

Integrated analysis of gene expression from carbon metabolism, proteome and metabolome, reveals altered primary metabolism in Eucalyptus grandis bark, in response to seasonal variation

Ilara Gabriela Frasson Budzinski et al. BMC Plant Biol. .

Abstract

Background: Seasonal variation is presumed to play an important role in the regulation of tree growth, especially for Eucalyptus grandis, a fast-growing tree. This variation may induce changes in the whole tree at transcriptional, protein and metabolite levels. Bark represents an important group of tissues that protect trees from desiccation and pathogen attack, and it has been identified as potential feedstock for lignocellulosic derived biofuels. Despite the growing interest, little is known about the molecular mechanisms that regulates bark metabolism, particularly in tropical countries.

Results: In this study we report the changes observed in the primary metabolism of E. grandis bark during two contrasting seasons in Brazil, summer (wet) and winter (dry), through the combination of transcripts (RT-qPCR), proteome (2-DE gels) and metabolome (GC-MS) analysis, in an integrated manner. Twenty-four genes, involved in carbon metabolism, were analyzed in the two seasons. Eleven were up-regulated in summer, three were up-regulated in winter and ten did not show statistical differences in the expression pattern. The proteomic analysis using 2-DE gels showed 77 proteins expressing differences in abundance, with 38 spots up-regulated in summer and 37 in winter. Different metabolites significantly accumulated during winter.

Conclusions: This study revealed a metabolic reconfiguration in the primary metabolism of E. grandis bark, triggered by seasonal variation. Transcripts and protein data suggests that during winter carbohydrate formation seems to be favored by tree metabolism. Glucose, fructose and sucrose accumulated at significant levels during the winter.

Keywords: Eucalyptus grandis; Metabolomics; Primary metabolism; Proteomics; RT-qPCR.

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Figures

Fig. 1
Fig. 1
Seasonal variation of transcripts involved in primary metabolism (a–d), in E. grandis bark, by RT-qPCR. Data are expressed as log fold change and winter values were used as a control. Expression was determined relative to α-tubulin and MDHc (Material and Methods). Asterisks indicates genes that are significantly expressed (P ≤ 0,05). Abbreviations: FBAcyt (fructose bisphosphate aldolase cytoplasmatic); GPI (glucose-6-phosphate isomerase); PGK (phosphoglycerate kinase); PK (pyruvate kinase); PEPC (phosphoenolpyruvate carboxylase); PFK (ATP-dependent phosphofructokinase); ENO (enolase); PGM (phosphoglucomutase); PGAM (phosphoglyceratemutase); PDH (pyruvate dehydrogenase); SuSy1 (sucrose synthase 1); SuSy3 (sucrose synthase 3); PFP (PPi-dependent phosphofructokinase); ADH2 (alcohol dehydrogenase 2); ADH3 (alcohol dehydrogenase 3); PDC (pyruvate decarboxylase); IDH (isocitrate dehyidrogenase); SCL (succinyl-coa ligase); NADP-ME (NADP malic enzyme); CA (carbonic anhydrase); RbcL (rubisco large subunit); RbcS (rubisco small subunit); FBAcl (fructose bisphosphate aldolase chloroplastidial) and RPI (ribose-5-phosphateisomerase). Three biological replicates, each with three technical replicates were analyzed per sample and error bars are standard errors of mean
Fig. 2
Fig. 2
Categorization of differentially expressed proteins in E. grandis bark in two contrasting seasons
Fig. 3
Fig. 3
Soluble sugar content of E. grandis bark during summer and winter. Soluble sugars were quantified by HPLC (Material and Methods). Three biological replicates with three technical replicates were performed for each season. Bars with same letter are not significantly different, based on Tukey’s test (P ≤ 0.05). Error bars are standard errors of mean
Fig. 4
Fig. 4
PLS-DA scores plot showing a significant separation (R 2 = 0.95 and Q 2 = 0.96) between E. grandis summer and winter barks. Component 1 and 2 contributes with 33.3 % and 30.9 %, respectively, of the total variance. Three biological replicates, each with three technical replicates were analyzed per sample
Fig. 5
Fig. 5
Differentially expressed transcripts, proteins and metabolites involved in the bark primary metabolism. The transcripts (square), proteins (circles) and metabolites (boxes) shown in white were up-regulated in summer, and those in gray were up-regulated in winter. Metabolites in dashed boxes were detected but were not significantly affected by seasonal changes (summer/winter). 1- Ribose-5-phosphate isomerase (RPI), 2- Rubisco large subunit (RbcL), 3- Sucrose synthase (SuSy), 4- Phosphoglucomutase (PGM), 5- ATP-dependent phosphofructokinase (PFK), 6- Fructose bisphosphate aldolase (FBAcyt), 7- Phosphoglycerate kinase (PGK), 8-Phosphoglycerate mutase (PGAM), 9- Enolase (ENO), 10-Phosphoenolpyruvate carboxylase (PEPC), 11- Pyruvate kinase (PK), 12- Pyruvate decarboxilase (PDC), 13- Alcohol dehydrogenase (ADH), 14- Isocitrate dehydrogenase (IDH) and 15- Succinyl-CoA ligase (SCL)
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