Objectives We explored the physiological metabolism and transcriptional changes of switchgrass (Panicum virgatum L.) under different phosphorus levels, aiming to understand the phosphorus response of root morphology and growth of switchgrass.

Methods A hydroponics experiment of switchgrass was carried out, based on the Hoagland nutrient solution, 4 KH₂PO₄ supply levels: 20, 100, 200, 500 μmol/L were setup (recorded as P20, P100, P200, P500). After 45 days of treatment, the seedlings were harvested for determination of physiological, root phenotype indexes and antistress enzyme activities, and transcriptome sequencing of leaves and roots was performed to identify the differentially expressed genes (DEGs) in leaves and roots. Some high expressed DEGs from glycolysis and phenylpropyl biosynthesis pathways were selected for qRT-PCR analysis to confirm the accuracy of transcriptome sequencing.

Results With the increase of P supply level, the activities of SOD, POD, and CAT in the leaves showed a trend of initially decreasing and then increasing; the total length, total area, and vitality of the roots increased first and then decreased; the acid phosphatase activities and phosphorus contents in both leaves and roots showed an initial increase followed by a decrease trend. There were 1091 and 1762 commonly expressed genes in the leaves and roots under all the phosphorus levels. GO enrichment annotation showed that the DEGs in leaves were mainly enriched in ion transmembrane transport and oxidoreductase, and the DEGs in roots were mainly enriched in specific DNA sequence binding, active transmembrane transport and lyase, and the DEGs in both the two organs in antioxidant enzyme, transferase and inorganic molecular transmembrane transporter. KEGG enrichment analysis showed that there were 9 common metabolic pathways in switchgrass leaves and roots, the DEGs were significantly enriched in amino sugar and nucleoside glucose metabolism, glycolysis/gluconeogenesis, phenylpropanoid biosynthesis, sucrose and starch metabolism pathways, and both glycolysis and phenylpropanoid biosynthesis pathways were enriched 16 DEGs each, and a total of 20 DEGs involved in phosphorus uptake transportion. The differential expression of AE, PGM, HK, PFK in key enzyme genes of glycolysis pathway, that of PAL, CCR, CAD, C4H, 4CL in key enzyme genes in the phenylpropanoid biosynthesis pathway, and GPT2, PHT2;1, TPT, PPT1, PPT2, PPT3, PiC3, APC2 in phosphorus uptake and absorption transporter explained the metabolic response differences of switchgrass to phosphorus nutrition.

Conclusions The suitable phosphorus supply level is conducive to good switchgrass root morphology, low anti-stress enzyme activities in leaves, and high acid phosphatase activity in leaves and roots, and high dry matter weight, as a result. The number and levels of differentially expressed genes related to glycolysis, phenylpropanoid biosynthesis and phosphorus absorption and transport in leaves and roots, which are caused by the P supply levels, could partially explain the mechanism.