Transcriptome Analysis Reveals Co-Expression Regulation of Sugar Transport and Signaling Networks in Initiating Stolon-to-Tuber Transition in Potato

The network regulatory mechanism governing the dynamics of plant maturity and tuber development in potatoes (<i>Solanum tuberosum</i> L.) has remained a major focus in potato molecular biology research. In this study, three potato cultivars with different maturity periods ('Shishu 2', 'Zhongshu 3', and 'Zhongshu 49') were examined. RNA sequencing was performed on samples from five tissues, including the leaves, stems, stolon (T0), sub-apical swellings (T1), and initiation stage (T2), to reveal the co-expression regulatory network involved in leaf, stem, and tuber development. <i>StSWEET11</i> and <i>StSP6A</i> were significantly upregulated in the early-maturing cultivar 'Shishu 2'. Differentially expressed genes were classified into 18 modules (ME) using weighted gene co-expression network analysis (WGCNA). Among these, ME1, ME3, and ME13 showed significant positive correlations with leaf tissue, ME2, ME4, and ME15 with stem tissue, and ME7, ME8, and ME14 with T1 and T2 tissues. <i>StSP5G</i> was identified as the core hub gene of ME4. Genes such as <i>StCOL1</i>, <i>StSWEET11</i>, and <i>StSP6A</i> exhibited significant co-expression in leaf-related modules. <i>StGIGANTEA</i> and <i>StGIGANTEA-like</i> played important regulatory roles in linking the expression networks of stems and tubers. Metabolism-related genes, including <i>StSUSⅠc</i>/<i>StSuSy4</i> and <i>StDPE1</i>, were also found to be crucial in mediating interactions between leaf and tuber tissues. Therefore, this study provides new insights into the regulatory network governing tuberous signal transmission from leaves and stems to tubers.