Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta‐analysis

Abstract

Many plant species simultaneously interact with multiple symbionts, which can, but do not always, generate synergistic benefits for their host. We ask if plant life history (i.e. annual vs perennial) can play an important role in the outcomes of the tripartite symbiosis of legumes, arbuscular mycorrhizal fungi (AMF), and rhizobia.We performed a meta-analysis of 88 studies examining outcomes of legume-AMF-rhizobia interactions on plant and microbial growth.Perennial legumes associating with AMF and rhizobia grew larger than expected based on their response to either symbiont alone (i.e. their response to co-inoculation was synergistic). By contrast, annual legume growth with co-inoculation did not differ from additive expectations. AMF and rhizobia differentially increased phosphorus (P) and nitrogen (N) tissue concentration. Rhizobium nodulation increased with mycorrhizal fungi inoculation, but mycorrhizal fungi colonization did not increase with rhizobium inoculation. Microbial responses to co-infection were significantly correlated with synergisms in plant growth.Our work supports a balanced plant stoichiometry mechanism for synergistic benefits. We find that synergisms are in part driven by reinvestment in complementary symbionts, and that time-lags in realizing benefits of reinvestment may limit synergisms in annuals. Optimization of microbiome composition to maximize synergisms may be critical to productivity, particularly for perennial legumes.

The effects of arbuscular mycorrhizal fungal species and taxonomic groups on stressed and unstressed plants: a global meta‐analysis

“…Mixed‐effect models allow the specification of fixed effects and of random terms. To avoid the nonindependence of the data we included the study identifier (ID), the experiment ID nested within study ID and host ID as random terms in order to contemplate and control the random variation of several outcomes from a single study, treatment or host identity (Tuck et al ., 2014; Ramírez‐Viga et al ., 2018; Primieri et al ., 2022). Moderator levels with three or fewer outcomes (i.e.…”

Nitrogen but not phosphorus addition affects symbiotic N2 fixation by legumes in natural and semi-natural grasslands located on four continents

“…We observed a higher N 2 fixation per unit biomass in the grasslands dominated by perennial legumes compared to the sites dominated by annual legumes. The reason for this could be that perennials can build up a symbiosis with N 2 fixation that last for several years, whereas annuals have to establish a new symbiosis with N 2 fixing microorganisms every year which makes this symbiosis likely less effective (Primieri et al 2022). The differences in N 2 fixation per unit biomass between annual and perennial legume sites disappeared in the N treatment (Fig.…”

Nitrogen-fixing symbiotic bacteria act as a global filter for plant establishment on islands

“…Synergistic limitation, where plant species that associate with both types of symbionts are less likely to colonize islands than expected from the two filters individually, may occur given that synergistic effects on plant growth has been found for co-inoculation with mycorrhizal fungi and N-fixing bacteria [19][20][21] . However, meta-analyses suggest that synergistic impacts on plant growth may be limited to perennial plants 22,23 , which may reduce the likelihood of finding synergistic limitations on island colonization. To date, the possibility of a plant island colonization filter strengthened by multiple mutualisms has not been tested.…”