Ecologically Different Fungi Affect Arabidopsis Development: Contribution of Soluble and Volatile Compounds

Abstract

Plant growth and development can be influenced by mutualistic and non-mutualistic microorganisms. We investigated the ability of the ericoid endomycorrhizal fungus Oidiodendron maius to influence growth and development of the non-host plant Arabidopsis thaliana. Different experimental setups (non-compartmented and compartmented co-culture plates) were used to investigate the influence of both soluble and volatile fungal molecules on the plant phenotype. O. maius promoted growth of A. thaliana in all experimental setups. In addition, a peculiar clumped root phenotype, characterized by shortening of the primary root and by an increase of lateral root length and number, was observed in A. thaliana only in the non-compartmented plates, suggesting that soluble diffusible molecules are responsible for this root morphology. Fungal auxin does not seem to be involved in plant growth promotion and in the clumped root phenotype because co-cultivation with O. maius did not change auxin accumulation in plant tissues, as assessed in plants carrying the DR5::GUS reporter construct. In addition, no correlation between the amount of fungal auxin produced and the plant root phenotype was observed in an O. maius mutant unable to induce the clumped root phenotype in A. thaliana. Addition of active charcoal, a VOC absorbant, in the compartmented plates did not modify plant growth promotion, suggesting that VOCs are not involved in this phenomenon. The low VOCs emission measured for O. maius further corroborated this hypothesis. By contrast, the addition of CO2 traps in the compartmented plates drastically reduced plant growth, suggesting involvement of fungal CO2 in plant growth promotion. Other mycorrhizal fungi, as well as a saprotrophic and a pathogenic fungus, were also tested with the same experimental setups. In the non-compartmented plates, most fungi promoted A. thaliana growth and some could induce the clumped root phenotype. In the compartmented plate experiments, a general induction of plant growth was observed for most other fungi, especially those producing higher biomass, further strengthening the role of a nonspecific mechanism, such as CO2 emission.

Respiratory CO2 Combined With a Blend of Volatiles Emitted by Endophytic Serendipita Strains Strongly Stimulate Growth of Arabidopsis Implicating Auxin and Cytokinin Signaling

“…A recurring enigma in studies examining plant responses under microbial VOC exposure is the relative importance of CO 2 versus other volatiles emitted by the microorganisms. Whereas some studies provided strong evidence for the contribution of respiratory CO 2 to the microbial VOC-elicited plant growth effects ( Kai and Piechulla, 2009 ; Casarrubia et al, 2016 ), other reports have implied the involvement of volatile compounds other than CO 2 , for instance in lateral root stimulation induced by L. bicolor volatiles ( Ditengou et al, 2015 ) or increased shoot FW triggered by VOCs of Escherichia coli ( Bailly et al, 2014 ), F. oxysporum ( Bitas et al, 2015 ), and Ampelomyces and Phoma strains ( Naznin et al, 2013 ). The positive correlation between the mycelial biomass, the plant responsiveness, and the level of generated CO 2 provided strong evidence for a major role of CO 2 in the Serendipita -mediated growth enhancement of Arabidopsis .…”

Volatile compounds other than CO2 emitted by different microorganisms promote distinct posttranscriptionally regulated responses in plants

“…A number of studies on plant's responses to microbial VCs have largely relied on the use of sealed dual cocultivation systems in which plants are exposed to complex mixtures of VICs and VOCs released by nearby microbial cultures (Blom et al, ; Casarrubia et al, ; Cordovez et al, ; Ditengou et al, ; Ezquer et al, ; Ryu et al, ; Sánchez‐López, Bahaji, et al, ; Sánchez‐López, Baslam, et al, ; Zhang et al, ). All currently known microorganisms that produce plant growth‐promoting volatiles are heterotrophic and thus emit respiratory CO 2 and consume O 2 when grown under aerobic conditions.…”

“…Elevated CO 2 and strong reduction of O 2 levels enhance photosynthesis, reduce photorespiration, and promote plant growth, flowering, starch accumulation, and changes in root architecture (Ainsworth & Rogers, ; Hachiya et al, ; Makino & Mae, ; Niu et al, ; Quebedeaux & Hardy, ; Ramonell et al, ; Song, Kristie, & Reekie, ; Thompson, Gamage, Hirotsu, Martin, & Seneweera, ). Therefore, several authors have argued that the responses of plants grown in closely proximity to microbial cultures in sealed containers could be largely due to accumulation of elevated levels of CO 2 from microbial respiration, which calls into question past interpretations of results obtained using sealed cocultivation systems (Casarrubia et al, ; Kai, Effmert, & Piechulla, ; Kai & Piechulla, ). Consequently, studies using sealed cocultivation systems should include appropriate CO 2 controls and online monitoring of the levels of this gas in the growth containers.…”

Volatile organic compounds stimulate plant growing and seed germination of Lactuca sativa

“…Bacterial species have been intensively studied for their ability to increase plant growth by emission of non-volatile compounds, but recent studies have discussed strongly the relevant ecological role of volatiles by their ability to induce growth without physical contact (Casarrubia et al, 2016;Tyc et al, 2016). In the last decade, Ryu et al (2003) so many studies have focused on these parameters (Salazar-henao et al, 2016).…”