Comparative transcriptome analysis of respiration-related genes in nodules of phosphate-deficient soybean (Glycine max cv. Williams 82)

Abstract

A transcriptome analysis was used to compare the nodule transcriptomes of the model soybean ‘Williams 82’ inoculated with two Bradyrhizobium diazoefficiens strains (USDA110 vs. CB1809) under phosphate (Pi) deficiency. The entire dataset revealed a core set of low-Pi-responsive genes and recognized enormous differential transcriptional changes between the Pi-deprived USDA110-nodules and CB1809-nodules. The lower symbiotic efficiency of the Pi-starved USDA110 nodules was ascribed to the downregulation of an F1-ATPase gene engaged in oxidative phosphorylation, more likely contributing to diminished ATP production. To cope with energy shortage caused by Pi stress, the Pi-deprived USDA110-nodules preferentially upregulated the expression of a large number of genes encoding enzymes implicated in specialized energy-demanding pathways, such as the mitochondrial respiratory chain (i.e., cytochrome c oxidase), alcoholic fermentation (i.e., pyruvate decarboxylase and alcohol dehydrogenase) and glycolysis (e.g., hexokinase, phosphofructokinase, glyceraldehyde‐3‐phosphate dehydrogenase and pyruvate kinase). These respiratory adjustments were likely associated with higher metabolic cost and redox imbalance, thereby, negatively affecting nodule symbiosis under Pi deprivation. In contrast, the Pi-starved CB1809-nodules reduced the metabolic cost by regulating a lower number of genes and increasing the expression of genes encoding proteins implicated in non-phosphorylating bypasses (e.g., flavoprotein alpha and flavoprotein:ubiqionone oxidoreductase), which could promote the carbohydrate utilization efficiency and energy metabolism. Notably, the upregulation of a transcript encoding a malate dehydrogenase could boost the CB1809-nodules under Pi stress. The dynamic shifts in energy metabolism in the Pi-deprived USDA110-nodules and CB1809-nodules could be transformative to upgrade the mechanistic/conceptual understandings of soybean adaptation to Pi deficiency at the transcriptional level.