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

Abstract

Rhizospheric microorganisms can alter plant physiology and morphology in many different ways including through the emission of volatile organic compounds (VOCs). Here we demonstrate that VOCs from beneficial root endophytic Serendipita spp. are able to improve the performance of in vitro grown Arabidopsis seedlings, with an up to 9.3-fold increase in plant biomass. Additional changes in VOC-exposed plants comprised petiole elongation, epidermal cell and leaf area expansion, extension of the lateral root system, enhanced maximum quantum efficiency of photosystem II (F v /F m ), and accumulation of high levels of anthocyanin. Notwithstanding that the magnitude of the effects was highly dependent on the test system and cultivation medium, the volatile blends of each of the examined strains, including the references S. indica and S. williamsii , exhibited comparable plant growth-promoting activities. By combining different approaches, we provide strong evidence that not only fungal respiratory CO 2 accumulating in the headspace, but also other volatile compounds contribute to the observed plant responses. Volatile profiling identified methyl benzoate as the most abundant fungal VOC, released especially by Serendipita cultures that elicit plant growth promotion. However, under our experimental conditions, application of methyl benzoate as a sole volatile did not affect plant performance, suggesting that other compounds are involved or that the mixture of VOCs, rather than single molecules, accounts for the strong plant responses. Using Arabidopsis mutant and reporter lines in some of the major plant hormone signal transduction pathways further revealed the involvement of auxin and cytokinin signaling in Serendipita VOC-induced plant growth modulation. Although we are still far from translating the current knowledge into the implementation of Serendipita VOCs as biofertilizers and phytostimulants, volatile production is a novel mechanism by which sebacinoid fungi can trigger and control biological processes in plants, which might offer opportunities to address agricultural and environmental problems in the future.

Fungal volatiles emitted by members of the microbiome of desert plants are diverse and capable of promoting plant growth

“…S3). Although most effects on plants in these systems had been considered to be mostly the result of the accumulation of carbon dioxide (Kai and Piechulla, 2009), recent studies have shown that both the organic and inorganic volatiles, including carbon dioxide, emitted by microorganisms are jointly responsible for these changes (García‐Gómez et al ., 2019; Moisan et al ., 2019; Venneman et al ., 2020). Thus, we analysed the organic compounds emitted by fungi that were linked to growth‐promotion phenotypes in Arabidopsis and that were commercially available (Fig.…”

“…Volatile organic compounds emitted by fungi (fVOCs) can activate defence responses in plants and prepare them against future pathogen attacks (Contreras- Cornejo et al, 2014;Naznin et al, 2014;Cellini et al, 2018;Quintana-Rodriguez et al, 2018). They can also promote the growth of plants and influence their tolerance to abiotic stress (Minerdi et al, 2011;Bitas et al, 2015;Lee et al, 2016;Venneman et al, 2020). Previously, we found that bacterial volatiles emitted by members of the prokaryotic microbiome of agaves and cacti, alone or in mixtures, displayed beneficial effects in A. thaliana, and improved growth and development of A. tequilana and A. salmiana (Camarena-Pozos et al, 2019).…”

Comment on acp-2020-1328

“…Both studies observed maximum fluxes during the grain-filling period, which showed large CO2 assimilation (Figure 5). To our knowledge, the only references reporting 530 emissions of this compound are from an orange orchard (Park et al, 2013b), biomass burning (Stockwell, 2016) and root endophytic fungi (Serendipita) (Venneman et al, 2020) studies, but also Gonzaga et al (2019) who found emissions of m/z 93.033 from oilseed rape plants. Park et al (2013b) report an average flux of 4.2 µg C m -2 h -1 over 24h, which is twice as low as the emissions reported here, when the measured three times larger methanol emissions.…”

“…Abis et al (2018) found indeed emissions from sieved soils, though small in magnitude. Furthermore, Venneman et al (2020) showed clear emissions of DMS from root endophytic Serendipita fungi. Clearly, DMS emissions by terrestrial ecosystems, and soils in particular should be 610 investigated further.…”

Mechanisms in Growth-Promoting of Cucumber by the Endophytic Fungus Chaetomium globosum Strain ND35

“…can increase the growth of Arabidopsis seedlings and plant biomass through the emission of volatile organic compounds (VOCs), such as methyl benzoate. The involvement of auxin and cytokinin signaling play important roles in Serendipita VOC-induced plant growth modulation [19]. The above mentioned studies demonstrated a strong change of hormonal and secondary metabolic pathways associated with growth stimulation in the plants following colonization by endophytic fungi.…”