Distance‐dependent effects of pathogenic fungi on seedlings of a legume tree: impaired nodule formation and identification of antagonistic rhizosphere bacteria

Abstract

1. The Janzen-Connell (JC) hypothesis proposes that diversity of tree communities is promoted by species-specific enemies that suppress seedling recruitment. Pathogenic soil-borne fungi are often responsible for JC effects. However, previous ecological studies have not placed JC effects in the context of beneficial soil bacteria. Using the JC effect surrounding a subtropical legume tree (Ormosia glaberrima) as a model, we characterized tripartite interactions between seedlings, soil fungi and plant-associated bacteria. 2. Survival of seedlings grown in soil inocula collected at close distances to focal adult trees was reduced. Half of the experimental units were treated with fungicides to confirm the presence of pathogenic fungi. In a parallel experiment, nitrogen-fixing rhizobia induced fewer nodules on O. glaberrima seedlings when soil inocula were collected closer to focal adult trees. An inoculation experiment with rhizobial isolates promoted nodulation of seedlings grown in soil taken at close distances to adult trees, suggesting that rhizobial densities are suboptimal at these locations. 3. Fusarium oxysporum, a pathogen of O. glaberrima seedlings, produced exudates that inhibited growth of most bacteria isolated from nodules. Accordingly, F. oxysporum negatively affected rhizosphere colonization of rhizobia in a co-inoculation experiment. Contrariwise, certain Burkholderia isolates (from nodules and the rhizosphere) were identified that possess the ability to inhibit growth of F. oxysporum. The majority of the antagonistic bacteria were isolated from locations with fungal pathogens, suggesting competition between fungi and rhizosphere bacteria. 4. Exclusion of pathogenic fungi by application of fungicides promoted nodulation of O. glaberrima seedlings under growth-room and field conditions. 5. Synthesis. Our findings indicate that soil-borne pathogens surrounding adult trees are microbial keystone species that locally influence interactions between seedlings and plant-associated bacteria.

Spatial patterns of pathogenic and mutualistic fungi across the elevational range of a host plant

“…The pH may potentially influence the pathogen through conditions favourable for spore germination (Land, Banhidi, & Albertsson, ; Magan & Lacey, ). Negative distance dependence supports the Janzen–Connell hypothesis, implying that high pathogen abundance could cause high seedling mortality close to conspecific adults (Liang et al., ; Liu, Yu, Xie, Staehelin, & van der Heijden, ; Packer & Clay, ). In the specialist ECM fungi, abiotic (i.e.…”

A native parasitic plant and soil microorganisms facilitate a native plant co‐occurrence with an invasive plant

“…Competitive interactions between fungi and soil bacteria have been observed (Fitter & Garbaye, ; Liu, Yu, Xie, & Staehelin, ). For instance, suppression of pathogenic fungi ( Fusarium oxysporum ) by application of fungicides promoted activities of nitrogen‐fixing bacteria in the roots of Ormosia glaberrima seedlings (Liu et al, ). Hence, it is likely that in our case, the fungicide suppressed soil fungi, which in turn freed the soil bacteria from fungal competition.…”

“…This may feedback on plant growth because different components of the microbial community may exert differential effects on plant growth (Bever, Platt, & Morton, 2012). Competitive interactions between fungi and soil bacteria have been observed (Fitter & Garbaye, 1994;Liu, Yu, Xie, & Staehelin, 2016). For instance, suppression of pathogenic fungi (Fusarium oxysporum) by application of fungicides promoted activities of nitrogen-fixing bacteria in the roots of Ormosia glaberrima seedlings (Liu et al, 2016).…”

Relationships between plant diversity and soil microbial diversity vary across taxonomic groups and spatial scales

“…Although soil microbial groups vary in their functional relationships with plants, they can promote plant community diversity through a variety of mechanisms. For example, symbiotic mutualists can promote plant community diversity by increasing nutrient availability or facilitating niche partitioning (Van Der Heijden et al 2006, Bever et al 2015, Van Der Putten 2017, while soil pathogens can infect and kill plant seedlings directly, or suppress beneficial microbial interactions with plant hosts, which both contribute to the survival of heterospecifics and lead to higher plant diversity (Mangan et al 2010, Liu et al 2016b). Plants also serve as the principal suppliers of energy for decomposers, symbionts, and pathogens, thereby governing the niche space for different soil microbes to persist (Facelli and Pickett 1991, Zak et al 2003, Berg and Smalla 2009, Bulgarelli et al 2013, Steinauer et al 2015.…”