Time-course transcriptome and WGCNA reveal tissue-specific genes in ‘White BK-1’ rye during early cold acclimation stage

Introduction The early stage of cold acclimation (CA) is a critical period during which plants gradually transition from cold sensing to the establishment of acquired freezing tolerance. Winter rye ( Secale cereale L.) is a cereal crop with superior cold hardiness. However, the temporal transcriptional dynamics during early CA and the tissue-specific expression patterns between leaves and roots remain poorly understood. Methods We evaluated the growth and freezing survival of ‘White BK-1’ during long-term CA and profiled leaf and root transcriptomes at multiple time points during the first 48 h of CA. Results Following CA, enhanced freezing tolerance in rye was associated with growth inhibition. Time-course transcriptome analysis of leaves and roots during early CA (0-48 h) revealed distinct transcriptional reprogramming patterns. At 2 h, 2,585 and 137 DEGs (Differentially expressed genes) were identified in roots and leaves, respectively. DEG numbers peaked at 48 h in both tissues, reaching 8,795 in leaves and 8,984 in roots. The leaf responses were initially dominated by photosynthesis-related pathways, followed by the upregulation of protective metabolism, such as trehalose biosynthesis, glutathione metabolism, and phenylpropanoid biosynthesis. The response in roots was characterized by rapid transcriptional reprogramming, followed by plant hormone signal transduction and damage clearance mechanisms, including ABA/ethylene responses, autophagy, and linoleic acid metabolism, several genes associated with ABA signaling pathways, as well as a gene encoding the DELLA inhibitor RHT1 ( SECCE4Rv1G0219050 ), were significantly upregulated. In total, 764 DETFs (Differentially Expressed Transcription Factors) were identified, mainly from the ERF, MYB, WRKY, bHLH, and NAC families. Moreover, SECCE5Rv1G0340400 ( DREB1H , ERF family), SECCE5Rv1G0304800 ( CPRF2 , bZIP family), and SECCE3Rv1G0171840 ( CDF2 , Dof family) were upregulated in both tissues. WGCNA (Weighted gene co-expression network analysis) identified modules closely associated with 48 h cold treatment in ‘White BK-1’ leaves and roots. Within the ICE-CBF-COR signaling pathway, SECCE7Rv1G0464580 ( COR27 ) and SECCE5Rv1G0354870 ( COR413PM1 ) exhibited the highest connectivity in the leaf and root subnetworks, respectively. Discussion Our study provides insight into tissue-specific transcriptional responses in rye leaves and roots during early CA, identifying candidate genes and co-expression modules potentially relevant to cereal cold tolerance.