Fungi Indirectly Affect Plant Root Architecture by Modulating Soil Volatile Organic Compounds

Abstract

The plant-growth modulating effect of microbial volatile organic compounds (VOCs) has been demonstrated repeatedly. This has most often been performed by exposing plants to VOC released by microbes grown on nutrient rich media. Here, we used soil instead to grow fungi of the Fusarium genus and investigate how VOCs emitted by this system influenced the development of Arabidopsis plants. The volatile profiles of Fusarium strains grown in soil and malt extract were also compared. Our results demonstrate that distinct volatile signatures can be attributed to different Fusarium genetic clades but also highlight a major influence of the growth medium on volatile emission. Furthermore, all soil-grown Fusarium isolates increased primary root length in Arabidopsis by decreasing VOC concentrations in soil. This result represents a major paradigm shift in plant-microbe interactions since growth modulating effects have been attributed so far to the emission and not the consumption of volatile signals.

The role of volatiles in plant communication

“…Others can induce resistance and tolerance in plants such as acetoin, dimethyl disulfide, 3‐pentanol and 6‐pentyl‐α‐pyrone (Fincheira and Quiroz, ) (Figure d). This shows that plants do not only produce volatiles, but also perceive them, and respond to them with altered growth or defence signalling (Schenkel et al ., ). This is further discussed below under ‘Molecular mechanisms underlying VOC perception’.…”

“…The field of VOC research is going through an exciting phase. We are seeing intriguing new developments such as the role of micro‐organisms in VOC communication, producing volatiles themselves (Lemfack et al ., ; Schenkel et al ., ), affecting the induction of HIPVs as endosymbionts of herbivorous insects (Frago et al ., ) or changing the flower VOC blend because they colonize nectar (Vannette and Fukami, ; Rering et al ., ). Also the elucidation of VOC transport, emission and accumulation and their perception in the receiver organism are hot topics in research and we are only just beginning to understand how specific volatiles and their blends convey information from one organism to the other and how flexible this process is.…”

Boreal forest soil is a significant and diverse source of volatile organic compounds

“…Although the quantities and functions of compounds in soils are largely unknown, the VOCs in soils have also been suggested to have an effect on biological interactions as infochemicals by transmitting messages between soil organisms (Tholl et al 2006;Schulz and Dickschat 2007;Insam and Seewald 2010;Wenke et al 2010;Schenkel et al 2018). VOCs may promote plant growth, control the nitrogen cycle, affect microbial metabolism and transmit long-distance communication between different decomposers (Insam and Seewald 2010;Asensio et al 2012;Peñuelas et al 2014;Tahir et al 2017).…”

“…Studies exist on the potentially high releases of VOCs from litter during biotic and abiotic processes and VOCs associated with multitrophic interactions between roots and microbes (Hayward et al 2001;Isidorov and Jdanova 2002;Gray et al 2010;Isidorov et al 2010;Wenke et al 2010;Ditengou et al 2015;Schenkel et al 2018). We hypothesized that belowground VOC concentrations are highest in the organic soil layer (the O-horizon) and the top mineral soil (the A-horizon) as the O-horizon contains isoprenoid-rich litter, and as fine roots and root-associated microbes are concentrated in the top horizon of the mineral soil.…”

Linking soil's volatilome to microbes and plant roots highlights the importance of microbes as emitters of belowground volatile signals

“…For instance, the volatile profile of the plant pathogen Gibberella avenacea, (teleomorph of Fusarium avenaceum) has been investigated during infection of maize ears (Becker et al, 2014). Additionally, the volatile profiles of other Fusarium species have been characterized in numerous other studies (Bitas and Kang, 2015;Lemfack et al, 2018;Schenkel et al, 2018;Wang et al, 2018). Two unidentified OTUs belonging to the Glomeromycota phylum known for its ability to form arbuscular mycorrhizae with plants were also put forward as possible emitter of volatiles (Table 2).…”