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

Abstract

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 gas chromatography-mass spectrometry-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 (Put) induced most significantly in roots during the interaction. Further, our results indicated that P. indica modulates the arginine decarboxylase (ADC)-mediated Put biosynthesis pathway via induction of SlADC1 in tomato. Piriformospora indica did not promote growth in Sladc1-(virus-induced gene silencing of SlADC1) lines of tomato and showed less colonization. Furthermore, using LC–MS/MS we showed that Put promoted growth by elevation of auxin (indole-3-acetic acid) and gibberellin (GA4 and GA7) levels in tomato. In Arabidopsis (Arabidopsis thaliana) adc knockout mutants, P. indica colonization also decreased and showed no plant growth promotion, and this response was rescued upon exogenous application of Put. Put 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 Put is an essential metabolite and its biosynthesis in plants is crucial for P. indica-mediated plant growth promotion and fungal growth.

Effect of Piriformospora indica-Induced Systemic Resistance and Basal Immunity Against Rhizoctonia cerealis and Fusarium graminearum in Wheat

“…In addition, our results proved that P. indica treatment was able to promote plant growth parameters, stimulating root biomass and fresh weight. Consistent with our data, colonization of P. indica has been confirmed to be able to increase the growth parameters of various plants ( Deshmukh and Kogel, 2007 ; Waller et al, 2008 ; Sun et al, 2014 ; Nassimi and Taheri, 2017 ; Kundu et al, 2021 ; Liu et al, 2021 ), which undoubtedly makes us believe that P. indica can be considered as a biological fertilizer to improve plant yields. Several hypotheses have been formulated about the mechanisms of growth promotion of P. indica , which suggested that P. indica may actively promote auxin-regulated genes through the production of indole-3-acetic acid-like compounds ( Lee et al, 2011 ; Franken, 2012 ).…”

“…The P. indica is well-known to be able to establish beneficial interactions with many different hosts, including monocotyledons such as barley, wheat, rice, corn, and dicotyledons, such as Arabidopsis and tobacco ( Qiang et al, 2012 ). The P. indica serves as an excellent model for beneficial microbes since it: (1) is genetically transformable and culturable in axenic conditions ( Zuccaro et al, 2009 ); (2) promotes plant growth and yield ( Kundu et al, 2021 ); (3) enhances plant tolerance against abiotic stress ( Li et al, 2021a ); and (4) primes plants for disease resistance against biotrophic and necrotrophic fungi ( Stein et al, 2008 ), oomycetes ( Trzewik et al, 2020 ), and viruses ( Fakhro et al, 2010 ).…”

Molecular mechanisms of Piriformospora indica mediated growth promotion in plants

“…Growth promotion with P. indica was found to be impaired in SlADC1 -suppressed or -mutant lines of tomato and/or Arabidopsis, and the growth promotion was restored by complementation with exogenous putrescine supplementation. Exogenous putrescine treatment also elevates auxin (indole-3-acetic acid) and specific gibberellins (GA 4 and GA 7 ) in tomato, which suggests that P. indica induces putrescine to elevate growth phytohormone levels, which finally results in plant’s growth promotion 10 ( Figure 1 ).…”

“… 34 In a recent study, it has been elucidated that P. indica employs putrescine for plant’s growth promotion. 10 P. indica induces putrescine biosynthesis in tomato ( Solanum lycopersicum ) through the ARGININE DECARBOXYLASE 1 ( Sl ADC1)-mediated pathway, as metabolomics and gene expression data indicated that P. indica induces putrescine content and SlADC1 transcript level in tomato upon colonization. Growth promotion with P. indica was found to be impaired in SlADC1 -suppressed or -mutant lines of tomato and/or Arabidopsis, and the growth promotion was restored by complementation with exogenous putrescine supplementation.…”

Reprogramming of Fundamental miRNA and Gene Expression during the Barley-Piriformospora indica Interaction

“…Piriformospora indica ( P. indica ) is an endophytic fungus, belonging to the order Sebacinales that colonizes the roots of both monocotyledons and dicotyledons plants [ 5 ]. P. indica serves as an excellent model for beneficial microbes as it can form a mutually beneficial symbiosis with a series of crops such as Chinese cabbage, rice, wheat, cucumber, onion and banana, which can effectively promote their growth, nutrient absorption, accumulation of secondary metabolites, and resistance to disease damage [ 6 , 7 , 8 , 9 , 10 , 11 , 12 ]. P. indica has great potential in biological control and soil improvement and thus can play a positive role in agricultural production.…”