Volatiles of pathogenic and non-pathogenic soil-borne fungi affect plant development and resistance to insects

Kay Moisan,Els M Van De Zande,Dani Lucas-Barbosa,Jos M Raaijmakers,Marcel Dicke,Viviane Cordovez

doi:10.1007/s00442-019-04433-w

Kay Moisan, Els M Van De Zande + Show 4 more

Open Access

https://doi.org/10.1007/s00442-019-04433-w

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Abstract

Plants are ubiquitously exposed to a wide diversity of (micro)organisms, including mutualists and antagonists. Prior to direct contact, plants can perceive microbial organic and inorganic volatile compounds (hereafter: volatiles) from a distance that, in turn, may affect plant development and resistance. To date, however, the specificity of plant responses to volatiles emitted by pathogenic and non-pathogenic fungi and the ecological consequences of such responses remain largely elusive. We investigated whether Arabidopsis thaliana plants can differentiate between volatiles of pathogenic and non-pathogenic soil-borne fungi. We profiled volatile organic compounds (VOCs) and measured CO2 emission of 11 fungi. We assessed the main effects of fungal volatiles on plant development and insect resistance. Despite distinct differences in VOC profiles between the pathogenic and non-pathogenic fungi, plants did not discriminate, based on plant phenotypic responses, between pathogenic and non-pathogenic fungi. Overall, plant growth was promoted and flowering was accelerated upon exposure to fungal volatiles, irrespectively of fungal CO2 emission levels. In addition, plants became significantly more susceptible to a generalist insect leaf-chewing herbivore upon exposure to the volatiles of some of the fungi, demonstrating that a prior fungal volatile exposure can negatively affect plant resistance. These data indicate that plant development and resistance can be modulated in response to exposure to fungal volatiles.

Highlights

Plants are exposed to diverse communities of insects and microorganisms, ranging from beneficial organisms, such as natural enemies of herbivores and plant growth-promoting rhizobacteria, to deleterious organisms such as pests and pathogens (Raaijmakers et al 2009; Bardgett and van der Putten 2014; Stam et al 2014)
58% of the compounds were unique to a fungal species, and 42% of the compounds were detected in the volatile organic compounds (VOCs) profiles of at least two different species (Fig. S2b)
The VOC profiles of the pathogenic fungi separated from the profiles of the non-pathogenic fungi: 18% and 13% of the total variance were explained by the first and second principal components, respectively (Fig. 1; Projection to Latent Structures Discriminant Analysis (PLS-DA); R2 = 0.6; Q2= 0.6, PCV ANOVA < 0.001)

Summary

Introduction

Plants are exposed to diverse communities of insects and microorganisms, ranging from beneficial organisms, such as natural enemies of herbivores and plant growth-promoting rhizobacteria, to deleterious organisms such as pests and pathogens (Raaijmakers et al 2009; Bardgett and van der Putten 2014; Stam et al 2014). Upon recognition of pathogenic microbes colonising the roots, local and systemic responses are induced in the plant which may affect plant development and resistance (Chagas et al 2018). Some non-pathogenic microorganisms can promote plant growth through facilitation of nutrient uptake or hormone production, and via symbiotic interactions such as nitrogen fixation (van Loon 2007; Bhattacharyya and Jha 2012). Plants colonised by these beneficial soil microorganisms may accelerate flowering, promoting their reproductive output (Koide and Dickie 2002; Wolfe et al 2005). Both pathogens and non-pathogenic microorganisms can affect plant fitness

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