Transcriptome and metabolome analyses reveal the potential mechanism of root zone temperature regulates the growth rhythm of switchgrass (Panicum virgatum L.) seedlings

Switchgrass ( Panicum virgatum L.) is a perennial warm-season C₄ plant that is a vital resource for forage production, soil and water conservation, and renewable energy. However, its slow seedling growth limits its broader application, with the underlying reasons for this slow growth not being well understood. This study examined the growth patterns, physiological metrics, and transcriptomic and metabolic profiles of Alamo cultivar seedlings under simulated root-zone temperature conditions. A moderate increase in root-zone temperature could enhance seedling growth, as evidenced by increases in plant height, stem diameter, root length, and fresh weight. A 6 °C increase in root-zone temperature significantly elevated chlorophyll, starch, lignin, soluble sugars, and soluble proteins in leaves, along with root vitality. An integrated multi-omics analysis revealed that genes associated with the IAA, ABA, JA, BR, SA, ETH, and CTK signaling pathways were differentially expressed. Additionally, the hormone content varied across different temperature treatment groups. Notably, the ZOG gene, involved in cytokinin biosynthesis, was downregulated, whereas 21 genes related to the two-component system were consistently upregulated. Additionally, flavonoid metabolism and the expression of genes associated with their biosynthesis were identified as crucial pathways in response to changes in root-zone temperature. Notably, as root zone temperatures increase, enhanced leaf photosynthesis coupled with weakened root energy metabolism may represent a balancing mechanism by which seedlings respond to changes in root zone temperature. This phenomenon requires further investigation. We propose a molecular model to account for the growth rhythm of switchgrass seedlings induced by root zone temperature variations. These findings offer a reference for elucidating the molecular mechanisms underlying the slow development of switchgrass seedlings and offer valuable insights for the genetic improvement of switchgrass and other crops. • This study examined switchgrass seedling growth rhythms via simulated seasonal root-zone temperature changes. • A moderate root-zone temperature increase promoted switchgrass seedling growth, enhancing plant height, stem diameter, fresh weight, chlorophyll content, and other indicators. • Comparative analyses revealed that plant hormone pathways, flavonoid metabolism, photosynthesis, glycolysis, and the TCA cycle regulate switchgrass growth under varying root-zone temperatures. • Key metabolites and differentially expressed genes were identified, and a molecular network model for root-zone temperature regulation of switchgrass seedling growth was constructed.