Spatiotemporal transcriptome dynamics elucidate sucrose accumulation in modern sugarcane

Modern sugarcane cultivar XTT22 is characterized by high sucrose content and favorable agronomic traits and is widely cultivated as well as extensively used as a backbone parental line in sugarcane breeding. However, the molecular regulation of sucrose accumulation remains poorly understood due to its complex polyploid genome. Recently, our team successfully assembled and resolved the XTT22 genome, providing a robust foundation to explore these complex regulatory mechanisms. Here, we quantified sucrose content across six key developmental stages and profiled gene expression in leaf, upper stem, central stem, and lower stem tissues. Multivariate and pairwise analyses revealed pronounced expression divergence between the upper stem and the central/lower stem during the rapid sucrose accumulation. Integration of spatiotemporal transcriptome profiling with weighted gene co-expression network analysis (WGCNA) identified three region-specific modules comprising 19 candidate genes with putative roles in sucrose accumulation. Functional annotation indicated spatial specialization: the upper stem was enriched for genes associated with sucrose biosynthesis, transport, and auxin-mediated regulation; the central stem for stress responses and auxin signaling/transport; and the lower stem for stress-response pathways. Four hub genes, including IAA30 and ARF2 , were identified, highlighting the central role of auxin signaling. Beyond the predominant negative correlations, two positive correlations emerged between photosynthesis-related genes and hub genes, suggesting a more complex source-sink relationship during sucrose accumulation than previously appreciated. Haplotype-resolved mapping showed that upper-stem candidates predominantly originated from the high-sucrose S. officinarum , whereas central/lower-stem candidates were mainly derived from the stress-tolerant S. spontaneum , reflecting their ancestral contributions. Overall, our results demonstrate spatiotemporal specialization of gene expression underlying sucrose accumulation in XTT22 and highlight auxin signaling potentially serving as a key regulatory module. These findings provide new insights into the molecular basis of sucrose accumulation and offer candidate genes with potential for targeted improvement of sugarcane cultivars. • A comprehensive spatiotemporal transcriptome atlas of sucrose accumulation in the modern sugarcane cultivar XTT22 is presented. • Distinct gene expression patterns are observed between the upper and lower stem regions during sucrose accumulation. • Identification of three region-specific gene modules and four hub genes reveals auxin signaling as a key regulator of sucrose metabolism. • A negative correlation is found between photosynthetic gene activity in leaves and sucrose-related hub genes in stems, supporting feedback regulation. • Subgenomic ancestry reveals distinct S. officinarum and S. spontaneum roles in sucrose accumulation pathways.