Synergism between feremycorrhizal symbiosis and free-living diazotrophs leads to improved growth and nutrition of wheat under nitrogen deficiency conditions

Abstract

A controlled-environment study was conducted to explore possible synergistic interactions between the feremycorrhizal (FM) fungus Austroboletus occidentalis and soil free-living N2-fixing bacteria (diazotrophs). Wheat (Triticum aestivum) plants were grown under N deficiency conditions in a field soil without adding microbial inoculum (control: only containing soil indigenous microbes), or inoculated with a consortium containing four free-living diazotroph isolates (diazotrophs treatment), A. occidentalis inoculum (FM treatment), or both diazotrophs and A. occidentalis inoculums (dual treatment). After 7 weeks of growth, significantly greater shoot biomass was observed in plants inoculated with diazotrophs (by 25%), A. occidentalis (by 101%), and combined inoculums (by 106%), compared to the non-inoculated control treatment. All inoculated plants also had higher shoot nutrient contents (including N, P, K, Mg, Zn, Cu, and Mn) than the control treatment. Compared to the control and diazotrophs treatments, significantly greater shoot N content was observed in the FM treatment (i.e., synergism between the FM fungus and soil indigenous diazotrophs). Dually inoculated plants had the highest content of nutrients in shoots (e.g., N, P, K, S, Mg, Zn, Cu, and Mn) and soil total N (13–24% higher than the other treatments), i.e., synergism between the FM fungus and added diazotrophs. Root colonization by soil indigenous arbuscular mycorrhizal fungi declined in all inoculated plants compared to control. Non-metric multidimensional scaling (NMDS) analysis of the bacterial 16S rRNA gene amplicons revealed that the FM fungus modified the soil microbiome. Our in vitro study indicated that A. occidentalis could not grow on substrates containing lignocellulosic materials or sucrose, but grew on media supplemented with hexoses such as glucose and fructose, indicating that the FM fungus has limited saprotrophic capacity similar to ectomycorrhizal fungi. The results revealed synergistic interactions between A. occidentalis and soil free-living diazotrophs, indicating a potential to boost microbial N2 fixation for non-legume crops.

Diazotrophic abundance and community structure associated with three meadow plants on the Qinghai-Tibet Plateau

“…Similarly, Proteobacteria and Actinobaceria were the most abundant diazotrophs in switchgrass ( Bahulikar et al, 2014 ), rhizosphere soil and the roots of Lasiurus sindicus grass in ( Chowdhury et al, 2009 ). Diazotrophs have widely been observed in non-legume plants, including maize ( Bloch et al, 2020 ; Wang et al, 2020 ), rice ( Wang et al, 2020 ; Mir et al, 2022 ), wheat ( Kariman et al, 2022 ) and sorghum ( Barros et al, 2020 ), grasses ( Pankievicz al., 2015 ) and sugarcane ( Matoso et al, 2020 ). Furthermore, Proteobacteria were dominant diazotrophs in non-legume plant species, such as Panicum coloratum , Chloris gayana and Digitaria eriantha ( Gupta et al, 2019 ).…”

Characterization of arbuscular mycorrhizal fungal species associating with Zea mays

“…Sorghum bicolor was chosen as the symbiotic partner because of its high mycorrhizal dependency, wide adaptability, and high resistance to abiotic stresses, including drought, salinity, waterlogging, and heavy metals ( Dar et al., 2018 ). A non-soil clay substrate was sterilized at 121°C for 15 min ( Getenga et al., 2004 ; Kariman et al., 2022 ) and, when cooled, was placed in 9.5 × 6.5 × 9.5 cm plastic pots (until they were two-thirds filled). A soil sample from the field (5 g each; from four different treatments, MO, MS, MM, MP, and under two different agriculture management practices) was used as inoculum and placed (2 cm deep) in the pots below the seeds (approximately three disinfected seeds of sorghum per pot).…”

Response to “Feremycorrhizal fungi: A confusing and erroneous term”: Feremycorrhiza means ‘nearly mycorrhiza’; hence, it is a clear and correct term because the fungal partner has mycorrhizal traits and lineage

“…The feremycorrhizal fungus does not grow on complex organic matter and lignocellulosic substrates and it only consumes hexoses such as glucose as a carbon source (Kariman et al, 2022), similar to ECM fungi (Shah et al, 2016;Zak et al, 2019). Therefore, it is not comparable to saprotrophs because saprotrophic fungi such as Aspergillus and Penicillium utilize organic matter, and may grow extensively in soil, leading to boosted mycelial biomass and competition with plants for nutrients; hence, they have limited use as bioinoculants and have not been successful biofertilisers in practice.…”

“…; see below), but it lacks the root colonization trait. Moreover, A. occidentalis effectively competes with other soil microbes, as growth/nutritional benefits were observed in inoculated plants grown in natural field soils containing indigenous microorganisms (Kariman et al, 2020(Kariman et al, , 2022. We accordingly hypothesize that A. occidentalis has developed stronger organic acid anion exudation and/or more effective capacity to capture organic molecules (e.g.…”

“…otherwise, and explain why here. Austroboletus occidentalis Watling & N.M. Greg (Boletaceae, Boletales, Basidiomycota) establishes the feremycorrhizal (FM) symbiosis, conferring significant growth and nutritional benefits to diverse host plants, including woody species such as jarrah (Eucalyptus marginata) (Kariman et al, 2014), arbuscular mycorrhizal (AM) crops such as wheat and barley as well as the non-mycorrhizal canola (Brassica napus) growing in natural field soils containing indigenous microorganisms (Kariman et al, 2020(Kariman et al, , 2022. 'Fere' means 'nearly' in Latin; hence, the term 'feremycorrhiza' means 'nearly mycorrhiza' (Kariman et al, 2018).…”