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 (Fv/Fm), 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 CO2 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.
Highlights
In search of sustainable alternatives for chemical fertilizers and plant protection products, the use of beneficial rhizosphere microorganisms and/or their bioactive compounds as potential biofertilizers, phytostimulants, and biocontrol agents has been widely explored
To assess the impact of Serendipita volatile production on Arabidopsis, a Petri-dish-in-box co‐cultivation assay was established (Supplementary Figure S1A) in which the fungus was cultured on potato dextrose agar (PDA) while the seedlings were grown on 1⁄2 Murashige and Skoog (MS) medium supplemented with sucrose (0%, 1% and 3%)
Isolate 30 was chosen as test organism because of its high growth rate and its strong plant growth-promoting (PGP) abilities in previous direct contact assays (Venneman et al, 2017)
Summary
In search of sustainable alternatives for chemical fertilizers and plant protection products, the use of beneficial rhizosphere microorganisms and/or their bioactive compounds as potential biofertilizers, phytostimulants, and biocontrol agents has been widely explored (reviewed, e.g., in Ahmad et al, 2018). In this context, the endophyte Serendipita indica (formerly Piriformospora indica) and its close relatives within the Serendipitaceae (Sebacinales, Agaricomycetes, Basidiomycota) have attracted attention because of their broad host spectrum and positive influence on diverse aspects of plant development. The cis-zeatin- and isopentenyladenine-type cytokinins that are produced by S. indica may play an important role in the beneficial interaction with Arabidopsis, they are not the elusive bioactive compounds responsible for the observed plant growth effects (Vadassery et al, 2008)
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