Mechanism underlying potato spindle tuber viroid affecting tomato (Solanum lycopersicum): loss of control over reactive oxygen species production

Severe infection of the tomato cultivar ‘Rutgers’ with potato spindle tuber viroid (PSTVd) variants resulted in systemic stunting, leaf malformation, and vein necrosis; accompanied by a rapid increase in reactive oxygen species (ROS) and abnormally high expression of the stress-responsive microRNAs, miR398 and miR398a-3p. The severity of the symptoms, PSTVd accumulation, the high expression of miR398 and miR398a-3p, and the high level of ROS production were positively correlated with the pathogenesis of the PSTVd variants. In contrast, the cytosolic and chloroplast-localized Cu/Zn-superoxide dismutase genes SlSOD4 and SlSOD3, respectively that encode the ROS scavenging enzymes were down-regulated and negatively correlated with the severity of the symptoms. Conversely, in the PSTVd-infected, PSTVd-tolerant (almost asymptomatic) tomato cultivar ‘Moneymaker’ in which PSTVd accumulation was suppressed, the ROS production was as low as in the control, miR398 and miR398a-3p were down-regulated, and almost all the SOD genes were up-regulated. The results indicated that in the PSTVd-sensitive tomato cultivar ‘Rutgers’, infection with the severe PSTVd variant caused suppression of the cytosolic and chloroplast-localized Cu/Zn-SOD genes via PSTVd-induced overexpression of miR398 and miR398a-3, respectively. This condition significantly reduced or eliminated the normal ROS scavenging function and an excess of harmful ROS in cells and tissues seem to have caused severe pathological symptoms accompanied by necrosis.