Plant Phenotypic and Transcriptional Changes Induced by Volatiles from the Fungal Root Pathogen Rhizoctonia solani.

Viviane Cordovez,Kay Moisan,Dani Lucas-Barbosa,Jos M Raaijmakers,Victor J Carrion,Liesje Mommer,Roland Mumm,Ronald Pierik

doi:10.3389/fpls.2017.01262

Abstract

Beneficial soil microorganisms can affect plant growth and resistance by the production of volatile organic compounds (VOCs). Yet, little is known on how VOCs from soil-borne plant pathogens affect plant growth and resistance. Here we show that VOCs released from mycelium and sclerotia of the fungal root pathogen Rhizoctonia solani enhance growth and accelerate development of Arabidopsis thaliana. Seedlings briefly exposed to the fungal VOCs showed similar phenotypes, suggesting that enhanced biomass and accelerated development are primed already at early developmental stages. Fungal VOCs did not affect plant resistance to infection by the VOC-producing pathogen itself but reduced aboveground resistance to the herbivore Mamestra brassicae. Transcriptomics of A. thaliana revealed that genes involved in auxin signaling were up-regulated, whereas ethylene and jasmonic acid signaling pathways were down-regulated by fungal VOCs. Mutants disrupted in these pathways showed similar VOC-mediated growth responses as the wild-type A. thaliana, suggesting that other yet unknown pathways play a more prominent role. We postulate that R. solani uses VOCs to predispose plants for infection from a distance by altering root architecture and enhancing root biomass. Alternatively, plants may use enhanced root growth upon fungal VOC perception to sacrifice part of the root biomass and accelerate development and reproduction to survive infection.

Highlights

Plants interact with a multitude oforganisms, including beneficial symbionts, fungal pathogens and insects
Seedlings exposed to volatile organic compounds (VOCs) from R. solani grown on 1/5th PDA medium showed an increase in shoot and root dry weight of 150% (Mann–Whitney U test, P = 0.008) and 265% (Mann–Whitney U test, P = 0.008), respectively, compared to seedlings not exposed to the fungal VOCs (Figure 1B)
Higher concentrations (10 μg, 100 μg and 1 mg) of 1-octen3-ol, 3-octanone and the mix even inhibited plant growth. These results indicate that other concentrations or other mixtures of the tested VOCs, or other VOCs not detected by the analytical method used here are involved in plant growth promotion by R. solani

Summary

Introduction

Plants interact with a multitude of (micro)organisms, including beneficial symbionts, fungal pathogens and insects. In the chemical interplay between microorganisms and plants, a wide range of compounds play a significant role. In this context, specific emphasis is given to volatile organic compounds (VOCs). Specific emphasis is given to volatile organic compounds (VOCs) This chemically diverse group of compounds can travel longer distances than other metabolites, facilitating a multitude of interactions with other organisms both below- and aboveground (Schulz and Dickschat, 2007; Das et al, 2012; Junker and Tholl, 2013). Plants use VOCs during resource limitation to detect the presence of proximate competitors, such as neighboring plants, and to inhibit the competitors’ growth and development (Kegge and Pierik, 2010)

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