Abstract
Serendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to understand if the free-living stage growth conditions (namely C availability) regulate S. indica’s phenotype, and its potential as plant-growth-promoting-microbe (PGPM). We grew S. indica in its free-living stage under increasing C availabilities (2–20 g L–1 of glucose or sucrose). We first characterised the effect of C availability during free-living stage growth on fungal phenotype: colonies growth and physiology (plasma membrane proton pumps, stable isotopic signatures, and potential extracellular decomposing enzymes). The effect of the C availability during the free-living stage of the PGPM was evaluated on wheat. We observed that C availability during the free-living stage regulated S. indica’s growth, ultrastructure and physiology, resulting in two distinct colony phenotypes: compact and explorer. The compact phenotype developed at low C, used peptone as the major C and N source, and displayed higher decomposing potential for C providing substrates; while the explorer phenotype developed at high C, used glucose and sucrose as major C sources and casein and yeast extract as major N sources, and displayed higher decomposing potential for N and P providing substrates. The C availability, or the C/N ratio, during the free-living stage left a legacy to the symbiosis stage, regulating S. indica’s potential to promote plant growth: wheat growth promotion by the explorer phenotype was ± 40% higher than that by the compact phenotype. Our study highlights the importance of considering microbial ecology in designing PGPM/biofertilizers. Further studies are needed to test the phenotypes under more extreme conditions, and to understand if the in vitro acquired characteristics persist under field conditions.
Highlights
To maintain the current human population growth and consumption patterns, food demand is forecasted to double by 2050 (Rockström et al, 2009), while its environmental footprint must be reduced
When grown under C availability < 10 g L−1, S. indica cultures tended to present a smaller proportion of small spores (16–45 μm) when compared with cultures grown under higher C availability (Supplementary Figure S1)
This means that in our study, the sporulation process started earlier when S. indica was grown under lower C availability, and at the same time point, spores formed under low C availability are older and more mature, bigger, than those formed at higher C availability which is supported by our observation of lower proportion of small spores under low C availability (Supplementary Figure S1)
Summary
To maintain the current human population growth and consumption patterns, food demand is forecasted to double by 2050 (Rockström et al, 2009), while its environmental footprint must be reduced (for the European Union, see Directive 2009/128/EC regarding the sustainable use of pesticides). This creates the need for cleaner farming practices capable of boosting crop yields while decreasing environmental impacts (Dias et al, 2015, 2018). Non-obligate biotroph fungi that confer benefits to the plant host similar to those conferred by AMF, are especially attractive as plant-growth-promoting-microbes (PGPM) and potential biofertilizers
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