Integrated Transcriptomic and Metabolomic Analysis Reveals Molecular Signatures Associated with Natural Degeneration of Puccinia striiformis f. sp. tritici

Stripe rust of wheat, caused by the obligate biotrophic fungus <i>Puccinia striiformis</i> f. sp. <i>tritici</i> (Pst), is a devastating disease. The natural degeneration and viability loss of Pst urediniospores directly impact its dispersal and epidemic potential, yet the underlying molecular mechanisms remain unclear. This study aimed to systematically decipher the key molecular changes during the natural degeneration of Pst urediniospores using a multi-omics approach. We performed integrated transcriptomic (RNA-seq) and metabolomic (LC-MS) analyses on relatively purified fresh urediniospores (CC group) and those undergoing room-temperature-induced degeneration (CM group) of the prevalent Pst race CYR34. A total of 1622 differentially expressed genes (DEGs) and 382 differentially accumulated metabolites (DAMs) were identified. Transcriptomic analysis revealed significant downregulation of core energy and biosynthetic pathways, including ribosome biogenesis and oxidative phosphorylation. Metabolomic profiling showed that lipids and lipid-like molecules, along with organic acids and derivatives, constituted the major classes of altered metabolites. DAMs were primarily enriched in pathways such as "Metabolic pathways" and "ABC transporters." Integrated analysis indicated a prevalent negative correlation pattern between gene expression levels and metabolite abundance. This study provides a systematic molecular landscape associated with Pst urediniospore degeneration, revealing characteristics concomitant with the suppression of energy metabolism and translation functions, thereby offering novel insights and a data foundation for understanding the mechanisms of viability maintenance and loss.