Proteomic, transcriptomic, biochemical, and physio-anatomical analyses provide insights into energy metabolism, light usage, and photosynthesis in cigar tobacco under different light intensities

Low light (LL) resulting in shading are among the detrimental abiotic stresses limiting plant growth and suppressing crop productivity. Shading is a key cultivation technique in cigar wrapper tobacco production but little is known about its impact on transcriptional and translational regulatory networks. Here, we integrate transcriptomic and proteomic profiling with physio-biochemical and anatomical analyses under different light intensities [T200 (200 μmol m−2 s−1), T100 (100 μmol m−2 s−1), and T50 (50 μmol m−2 s−1)] to uncover the underlying molecular response mechanisms of tobacco plants. We found that the leaf anatomical structure impacts photosynthetic capacity and that LL intensities (particularly T50) decrease leaf and palisade thickness (42%) and spongy tissues (16%), which leads to a lower photosynthetic rate (84%) compared with T200. Furthermore, we identified 3045 and 590 significantly differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) in the transcriptome and proteome of cigar tobacco, respectively. A total of 110 pairs were correlated which were upregulated in photosynthesis-antenna proteins, photosynthesis, and defense/detoxification-related pathways, according to integrated omics analyses, and downregulated in tyrosine metabolism, starch and sucrose metabolism, mitochondrial electron transport chain, and glycolysis pathways; and associated with decreased activities of glyceraldehyde-3-phosphate dehydrogenase (31%), starch phosphorylase (25%), and pyruvate kinase (24%) enzymes related to glycolysis. Our results show that cigar tobacco efficiently utilizes low light to reconfigure its energy metabolism, and offer profound insights into the response mechanisms at the physio-biochemical, anatomical, and molecular levels. This study thus represents a valuable resource of genes and proteins for future functional studies underlying LL response. [Display omitted] •Shading or LL is one of the key cultivation techniques in cigar tobacco production.•LL decreased LT, PCL, and STT which resulted in lower photosynthesis and biomass.•DEGs and DEPs related to photosynthesis and defense are upregulated under LL.•DEGs and DEPs related to glycolysis and sugar metabolism are repressed under LL.•Plant energy metabolism is interrupted and alternatively efficiently utilized LL.