Integrated Transcriptomic and Phytohormone Metabolomic Analyses Reveal Distinct Molecular States Associated with PSTVd-Induced Potato Tuber Cracking and Knob-like Protuberances at Tuber Eyes

Potato spindle tuber viroid (PSTVd) infection can induce tuber cracking and knob-like protuberances at tuber eyes, but the molecular differences between these two localized symptoms remain unclear. In this study, smooth surface regions and normal eye tissues were collected from mock-inoculated tubers of the potato cultivar ‘Kexin 18’, whereas crack regions and regions of knob-like protuberances at tuber eyes were collected from PSTVd-infected tubers. RNA sequencing and targeted phytohormone quantification were combined with weighted gene co-expression network analysis, infection × region interaction analysis, and gene-hormone association analysis. PSTVd infection markedly inhibited plant growth and tuber development, and 2972 genes with significant infection × region interaction effects were identified. Crack regions were characterized primarily by enhanced defense and oxidative stress related transcriptional responses, remodeling of cell wall and surface barrier related processes, and accumulation of several cytokinin (CK) metabolites, salicylic acid/salicylic acid glucoside (SA/SAG), and 12-oxo-phytodienoic acid (OPDA); CRK2, RBOHA, and CSLG2 were among the representative candidate genes. Regions of knob-like protuberances at tuber eyes showed pronounced reprogramming of processes related to DNA replication, the cell cycle, chromosome maintenance, and chromatin organization, together with decreases in several CK metabolites, a downward trend in jasmonate-related oxylipins, and an increase in indole-3-butyric acid; ACL5-like, PILS7-like, CYCA3;1, and MCM4 were identified as candidate genes. Gene-hormone association analysis further revealed distinct molecular association patterns in the two regions. Collectively, the two symptomatic regions exhibited distinct region-dependent transcriptomic and phytohormone metabolic states after symptom development.