Combined drought and salinity trigger unique lncRNA regulatory signatures in sweet sorghum (Sorghum bicolor L. Moench) compared to individual stress responses

Climate change has driven rapid environmental shifts, exposing crop plants to a myriad of stressors, including drought and salinity, which frequently co-occur in natural environments. To thrive, the host must exhibit enough plasticity to adapt to this challenging habitat, or else confront an inevitable decline. While long non-coding RNAs (lncRNAs) are crucial mediators of post-transcriptional gene regulation, they have rarely been associated with co-occurring stresses. Here, lncRNA transcriptome of sweet sorghum was analyzed to discern its potential role in drought and salinity, either alone or in combination, aiming to establish a foundational understanding of its contribution in stress resilience. The simultaneous occurrence of the stressors prompted the host to elicit differential expression (DE) of 349 lncRNAs, surpassing the number observed when the stressors were applied individually. Notably, lncRNA signatures under dual stress exhibited a greater resemblance to the impacts induced by salinity rather than drought, as evidenced by the abundance of shared and stress-specific lncRNA transcripts. WGCNA analysis highlighted modules with co-expressed gene clusters, revealing strong correlation between dysregulated lncRNAs and stress-responsive genes linked to ion transport, phytohormone signalling, stress and defence response, photosynthesis, oxidative stress and abiotic stress signalling. qPCR validation of certain candidate lncRNAs associated with these pathways revealed significant differences in expression levels when assessed individually compared to in combination. Moreover, four sweet sorghum lncRNAs were identified as endogenous target mimics (eTM), potentially acting as decoys to counter the transcriptional repression activity of miRNAs. Capitalizing on this regulatory interplay, expression patterns of two eTMs, MSTRG.13861.4-miR169d-RAP2.6 and MSTRG.15003.1-miR5565e-PSAN, were scrutinized and quantitatively validated under the concurrent exposure of stress factors. Together, this pioneering work has uncovered lncRNA signatures that give crucial insights about interactions to cope with the impacts of co-occurring drought and salinity.