Combined Small RNA and Degradome Sequencing Reveals Important Roles of Light-Responsive microRNAs in Wild Potato (Solanum chacoense)

Abstract

The accumulation of chlorophyll and antinutritional glycoalkaloids in potato tubers resulting from exposure to light has been widely recognized as a cause of unpredictable quality loss of potato tuber. While transcriptional regulation of light-induced chlorophyll and glycoalkaloids accumulation has been extensively investigated, the mechanisms of post-transcriptional regulation through miRNA remain largely unexplored. An experimental model, the tubers of Solanum chacoense, were used to identify light-responsive miRNA–target interactions (MTIs) related to tuber greening and glycoalkaloid biosynthesis by employing multi-omics approaches (miRNA-seq and degradome-seq). A total of 732 unique mature miRNAs have been identified in S. chacoense. In total, 6335 unique target transcripts were cleaved by 489 known miRNAs and 153 novel miRNAs. The results revealed that light-responsive miRNAs can be grouped into eight temporally related clusters and play important roles in various physiological processes such as plant growth, stress responses, and primary and secondary metabolism. Multi-omics analyses have revealed that the modulation of transcript abundance of MYB59, HSPs, and EBF1/EBF2 by light-responsive miRNAs is pivotal for their function in cross-tolerance responses to both abiotic and biotic stresses. Furthermore, our findings suggest that many light-responsive miRNAs are crucial regulators in various biosynthetic pathways, including tetrapyrrole biosynthesis, suberin biosynthesis, and steroid biosynthesis. These findings highlight the significant role of light-responsive miRNAs in secondary metabolic pathways, particularly in isoprenoid, terpenoid, and glycoalkaloid biosynthesis, and have implications for the precise manipulation of metabolic pathways to produce new potato varieties with improved resistance to greening and lower glycoalkaloid levels.