Abstract
In natural and agricultural ecosystems, survival and growth of plants depend substantially on residing microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to understand how sets of microbial species positively or negatively affect plants’ performance. By conducting a series of single- and dual-inoculation experiments of 13 plant-associated fungi targeting a Brassicaceae plant species (Brassica rapa var. perviridis), we here systematically evaluated how microbial effects on plants depend on presence/absence of co-occurring microbes. The comparison of single- and dual-inoculation experiments showed that combinations of the fungal isolates with the highest plant-growth promoting effects in single inoculations did not have highly positive impacts on plant performance traits (e.g., shoot dry weight). In contrast, pairs of fungi with small/moderate contributions to plant growth in single-inoculation contexts showed the greatest effects on plants among the 78 fungal pairs examined. These results on the offset and synergistic effects of pairs of microbes suggest that inoculation experiments of single microbial species/isolates can result in the overestimation or underestimation of microbial functions in multi-species contexts. Because keeping single-microbe systems under outdoor conditions is impractical, designing sets of microbes that can maximize performance of crop plants is an important step for the use of microbial functions in sustainable agriculture.
Highlights
Plants in natural and agricultural ecosystems are associated with diverse taxonomic groups of microbes, forming both positive and negative interactions with the microbiomes (Lundberg et al, 2012; Peay et al, 2016; Busby et al, 2017; Toju et al, 2018b)
Various taxonomic groups of fungal isolates were retrieved from the ca. 3,500 fungal isolates maintained in the culture collection of Centre for Ecological Research, Kyoto University (Supplementary Data 1)
We examined how the nonlinearity measures of fungal pairs are associated with the abovementioned index values representing deviations of observed dual-inoculation results from those expected as intermediate results of single inoculations (DIAB)
Summary
Plants in natural and agricultural ecosystems are associated with diverse taxonomic groups of microbes, forming both positive and negative interactions with the microbiomes (Lundberg et al, 2012; Peay et al, 2016; Busby et al, 2017; Toju et al, 2018b). Bacteria and fungi found within and around root systems have been reported as key determinants of plants’ survival and growth (Hiruma et al, 2016, 2018; Castrillo et al, 2017; Trivedi et al, 2020). A growing number of studies have shown that diverse clades of endophytic and soil fungi support host plants by provisioning inorganic/organic forms of nutrients (Usuki and Narisawa, 2007; Newsham, 2011; Hiruma et al, 2016), activating plant immune systems (van Wees et al, 2008; Pieterse et al, 2014), and suppressing populations of pathogens/pests in the rhizosphere (Narisawa et al, 2004; Khastini et al, 2012; Gu et al, 2020). Developing scientific bases for maximizing the benefits from those plant-associated microbiomes is an essential step for fostering sustainable crop production and restoring forest/grassland ecosystems (Bulgarelli et al, 2013; Carlström et al, 2019; Wagg et al, 2019; Saad et al, 2020)
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