Piriformospora indica recruits host-derived putrescine for growth promotion in plants.

Growth promotion induced by the endosymbiont Piriformospora indica has been observed in various plants; however, except growth phytohormones, specific functional metabolites involved in P. indica-mediated growth promotion are unknown. Here, we used a GC-MS based untargeted metabolite analysis to identify tomato (Solanum lycopersicum) metabolites whose levels were altered during P. indica-mediated growth promotion. Metabolomic multivariate analysis revealed several primary metabolites with altered levels, with putrescine induced most significantly in roots during the interaction. Further, our results indicated that P. indica modulates the arginine decarboxylase (ADC)-mediated putrescine biosynthesis pathway via induction of SlADC1 in tomato. P. indica did not promote growth in Sladc1-VIGS (virus-induced gene silencing of SlADC1) lines of tomato tomato and showed less colonization. Furthermore, using LC-MS/MS we showed that putrescine promoted growth by elevation of auxin (indole-3-acetic acid) and gibberellin (GA4, GA7) levels in tomato. In Arabidopsis (Arabidopsis thaliana) adc knock-out mutants, P. indica colonization also decreased and showed no plant growth promotion, and this response was rescued upon exogenous application of putrescine. Putrescine is also important for hyphal growth of P. indica, indicating that it is co-adapted by both host and microbe. Taken together, we conclude that putrescine is an essential metabolite and its biosynthesis in plants is crucial for P. indica-mediated plant growth promotion and fungal growth.