Coexpression Regulation of New and Ancient Genes in the Dynamic Transcriptome Landscape of Stem and Rhizome Development in “Bainianzhe”—An Ancient Chinese Sugarcane Variety Ratooned for Nearly 300 Years

The sucrose yield in sugarcane largely depends on stem morphology, including length, diameter and sugar content, making sugarcane stem a key trait in breeding. The "Bainianzhe" variety from Songxi County, Fujian Province, possesses both aerial stems and rhizomes, providing a unique model for studying stem development. We performed a spatiotemporal transcriptomic analysis of the base, middle and apical sections of both aerial stems and rhizomes. The analysis categorized transcriptomes by developmental stage-base, middle and apical-rather than environmental differences. Apical segments were enriched with genes related to cell proliferation, while base segments were linked to senescence and fibrosis. Gene regulatory networks revealed key TFs involved in stem development. Orphan genes may be involved in rhizome development through coexpression networks. Plant hormones, especially genes involved in ABA and GAs synthesis, were highly expressed in rhizomes. Thiamine-related genes were also more prevalent in rhizomes. Furthermore, the apical segments of rhizomes enriched in photosynthesis-related genes suggest adaptations to light exposure. Low average temperatures in Songxi have led to unique cold acclimation in Bainianzhe, with rhizomes showing higher expression of genes linked to unsaturated fatty acid synthesis and cold-responsive calcium signalling. This indicates that rhizomes may have enhanced cold tolerance, aiding in the plant's overwintering success.