Morphophysiological disorders and metabolic reprogramming in Physalis peruviana infected with the physalis rugose mosaic virus

Physalis peruviana L. (Cape gooseberry) is susceptible to several pathogens, among which the sobemovirus physalis rugose mosaic virus (PhyRMV) is most prominent. This study investigated the anatomical, morphophysiological, and metabolic responses of P. peruviana to PhyRMV over the course of the infection cycle. P. peruviana plants were grown under greenhouse conditions (24 ± 2 ℃) and mechanically inoculated with buffer (mock) or PhyRMV inoculum. The local and systemic leaves were collected at 0, 3, 7, 14, 21, and 42 days after inoculation (DAI) and viral infection was confirmed by RT-qPCR. Morphological traits, including plant height, symptoms, and the Falker chlorophyll index, and histological changes were evaluated in PhyRMV-infected plants and compared to mock-inoculated controls. To characterize and compare their metabolic profile, the collected leaves were processed and subjected to gas chromatography-mass spectrometry (GC-MS). Yield was also assessed by quantifying the number and weight of fruits. PhyRMV could be detected in systemic leaves from 14 DAI onward, accompanied by an increase in viral load and the intensification of the symptoms, including mosaic, chlorosis, and leaf deformation from 21 DAI onward, which were associated with reduced plant height and chlorophyll contents. At 42 DAI, histological changes and increased starch accumulation were observed in the infected leaves, suggesting impaired photoassimilate transport. GC-MS revealed an accumulation of sucrose, pyruvate, and tricarboxylic acid (TCA) cycle metabolites, possibly due to the high energy demand associated with viral replication, indicating significant alterations in the functioning of the central metabolic pathways in systemic leaves in the late stage of infection at 42 DAI. Compounds such as glutamate, isoleucine, and malonate could potentially be involved in the activation of defense pathways, including the shikimic acid pathway. Metabolic networks demonstrated a loss of complexity in the infected plants, indicating a redirection of resources from primary metabolism to defense-associated mechanisms. Thus, fruit production was reduced by 31% in the infected plants, highlighting a negative impact of infection on the production potential. These results support management strategies based on the induction of plant defense mechanisms and reinforce the importance of the use of integrative approaches to understanding the physiological and biochemical impacts of viruses on crops.