Factors controlling the effects of mutualistic bacteria on plants associated with fungi

Abstract

Plants interacting with mutualistic fungi (MF) or antagonistic fungi (AF) can form associations with bacteria. We assessed whether the performance gain conferred by mutualistic bacteria to fungal-associated plants is affected by the interaction between symbiont traits, type of bacterial-protective traits against AF and abiotic/biotic stresses. Results showed that (A) performance gain conferred by bacteria to MF-associated plants was greater when symbionts promoted distinct rather than similar plant functions, (B) bacterial-based alleviation of the AF's negative effect on plants was independent of the type of protective trait, (C) bacteria promoted a greater performance of symbiotic plants in presence of biotic, but not abiotic, stress compared to stress-free situations. The plant performance gain was not affected by any fungal-bacterial trait combination but optimised when bacteria conferred resistance traits in biotic stress situations. The effects of bacteria on fungal-associated plants were controlled by the interaction between the symbionts' functional traits and the relationship between bacterial traits and abiotic/biotic stresses.

Keywords: antagonistic symbionts; mutualistic symbionts; plant-associated fungi; plant-microbe interactions; tripartite plant symbiosis.

FIGURE 1

Predicted effects of three major factors on the performance gain conferred by bacteria to plants associated with Mutualistic Fungi (MF) or Antagonistic Fungi (AF). (a) Interaction between MF‐bacterial traits: Fungi and bacteria that confer traits promoting distinct plant functions may lead to a greater gain in plant performance than symbionts that confer traits enhancing similar/identical plant functions (i.e. functionally distinct MF‐bacteria vs. functionally equivalent MF‐bacteria). (b) Type of protection traits conferred by bacterial symbionts: bacteria that confer both pathogen resistance and tolerance traits to plants interacting with AF may alleviate to a greater degree the AF's negative effect on plant performance than bacteria that confer these trait types separately. (c) Abiotic/biotic environmental stresses: bacteria that confer stress‐protective traits to their MF‐associated plant hosts may lead to a greater gain in plant performance in the presence of abiotic/biotic stresses compared to those plants in the absence of any stress.

FIGURE 2

The effect of bacteria on the performance of plants associated with Mutualistic Fungi (MF). The overall effect of bacteria on plants associated with MF was categorised into three subgroups depending on the interaction between fungal and bacterial traits (i.e. functionally distinct group = bacteria that add traits promoting dissimilar plant functions than fungi, functionally equivalent group = bacteria that add traits promoting identical/similar plant functions than fungi, while the third group included symbiotic associations with an unknown relationship). The first two subgroups were further categorised according to the specific plant functions that bacteria and fungi promoted. Those plant functions that were exclusively promoted by bacteria are italicised. The effects of just MF and bacteria on performance of symbiont‐free plants are also shown. An effect size with a positive value (95% confidence interval (CI) not overlapping zero) indicates a positive or beneficial effect of bacteria (relative to MF‐plants or symbiont‐free plants) or MF (relative to symbiont‐free plants) on the performance of host plants. For simplicity, the 95% CI of ‘growth’ and ‘stress protection’ categories are not fully shown. We refer to plant performance as measures of fitness including biomass, survival and seed production. Values in parentheses indicate the number of studies analysed.

FIGURE 3

The effect of bacteria on the performance of plants associated with Antagonistic Fungi (AF). The overall effect of bacteria on plants associated with AF was categorised into four subgroups depending on the types of protective traits provided by bacteria to their host plant against AF (i.e. resistance and tolerance traits, only resistance traits, only tolerance traits and unknown). The effects of just AF and bacteria on performance of symbiont‐free are also shown. An effect size with a positive value (95% confidence interval (CI) not overlapping zero) indicates a positive or beneficial effect of bacteria (relative to AF‐plants or symbiont‐free plants) or AF (relative to symbiont‐free plants) on the performance of their host plants, whereas a negative value indicates the opposite. We refer to plant performance as measures of fitness including biomass and disease resistance. Values in parentheses indicate the number of studies analysed.

FIGURE 4

Relationships between performance gains conferred by bacteria to plants associated with fungi (either mutualistic or antagonistic) in the presence and absence of environmental stresses. (a) Abiotic/biotic environmental stresses: The effect of bacteria on plant performance gain was categorised into the type of stress (i.e. abiotic or biotic stress). (b) Within biotic stress: The effect of bacteria on the plant performance gain was categorised into three subgroups depending on the types of protective traits conferred by bacteria to their host plant against biotic stresses (i.e. resistance and tolerance traits, only resistance traits, only tolerance traits). Each dot represents a single study (for details see studies listed in Table S1). The discontinuous black line is a reference that indicates the 1:1 relationship between plant performance gains (the proportional effect conferred by bacteria on their plant hosts, which are associated with fungi in the presence and absence of abiotic/biotic stresses). The continuous lines represent the linear models inferred from the GLM analyses (abiotic: y = 0.43 ± 0.24 × X + 0.56 ± 0.84; biotic: y = 1.60 ± 0.25 × X + 0.31 ± 1.11; with resistance and tolerance traits: y = 0.16 ± 0.49 × X + 9.10 ± 3.79; with resistance traits: y = 1.81 ± 0.04 × X − 0.56 ± 0.43; with tolerance traits: y = 0.14 ± 0.51 × X + 4.96 ± 2.51).