During the independent process of evolution in plants, photosynthesis appears to have been under convergent evolution to adapt to specific selection pressure in their geographical regions. However, it is unclear how lncRNA regulation and DNA methylation are involved in the phenotypic convergence in distinct lineages. Here, we present a large-scale comparative study of lncRNA transcription profile and whole-genome bisulfite sequencing (WGBS) data in two unrelated Populus species, selected from three relatively overlapping geographical regions. The results indicated that 39.75% lncRNAs of Populus tomentosa were shown to have homologous sequences in the 46.99% lncRNA of Populus simonii. Evolutionary analysis revealed that lncRNAs showed a rapid gain rate in the Populus lineage. Furthermore, co-expression networks in two Populus species identified eight lncRNAs that have the potential to simultaneously cis- or trans-regulate eight photosynthetic-related genes. These photosynthetic lncRNAs and genes were predominantly expressed in accessions from the southern region, indicating a conserved spatial expression in photosynthetic pathways in Populus. We also detected that most lncRNA targeted photosynthetic genes hypomethylated in promoter regions of Southern accessions compared with Northern accessions. Geographical DMRs correlated with genetic SNP variations in photosynthetic genes among Populus from the three geographic regions, indicating that DNA methylation coordinated with lncRNAs in convergent evolution of photosynthesis in Populus. Our results shed light on the evolutionary forces acting on patterns of lncRNA and DNA methylation, and provide a better understanding of the genetic and epigenetic mechanism in photosynthetic convergence evolution.
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