Integration of metabolome and transcriptome analyses highlights soybean roots responding to phosphorus deficiency by modulating phosphorylated metabolite processes

Abstract

Phosphorus (P) is a major constituent of biomolecules in plant cells, and is an essential plant macronutrient. Low phosphate (Pi) availability in soils is a major constraint on plant growth. Although a complex variety of plant responses to Pi starvation has been well documented, few studies have integrated both global transcriptome and metabolome analyses to shed light on molecular mechanisms underlying metabolic responses to P deficiency. This study is the first time to investigate global profiles of metabolites and transcripts in soybean (Glycine max) roots subjected to Pi starvation through targeted liquid chromatography electrospray ionization mass spectrometry (LC-ESI-MS/MS) and RNA-sequencing analyses. This integrated analysis allows for assessing coordinated transcriptomic and metabolic responses in terms of both pathway enzyme expression and regulatory levels. Between two Pi availability treatments, a total of 155 metabolites differentially accumulated in soybean roots, of which were phosphorylated metabolites, flavonoids and amino acids. Meanwhile, a total of 1644 differentially expressed genes (DEGs) were identified in soybean roots, including 1199 up-regulated and 445 down-regulated genes. Integration of metabolome and transcriptome analyses revealed Pi starvation responsive connection between specific metabolic processes in soybean roots, especially metabolic processes involving phosphorylated metabolites (e.g., phosphorylated lipids and nucleic acids). Taken together, this study suggests that complex molecular responses scavenging internal Pi from phosphorylated metabolites are typical adaptive strategies soybean roots employ as responses to Pi starvation. Identified DEGs will provide potential target region for future efforts to develop P-efficient soybean cultivars.