Multi‐symbiotic systems: functional implications of the coexistence of grass–endophyte and legume–rhizobia symbioses

Abstract

The coexistence of symbionts with different functional roles in co‐occurring plants is highly probable in terrestrial ecosystems. Analyses of how plants and microbes interact above‐ and belowground in multi‐symbiotic systems are key to understand community structure and ecosystem functioning. We performed an outdoor experiment in mesocosms to investigate the consequences of the interaction of a provider belowground symbiont of legumes (nitrogen‐fixing bacteria) and a protector aerial fungal symbiont of grasses (Epichloё endophyte) on nitrogen dynamics and aboveground net primary productivity. Four plants of Trifolium repens (Trifolium, a perennial legume) either inoculated or not with Rhizobium leguminosarum, grew surrounded by 16 plants of Lolium multiflorum (Lolium, an annual grass), with either low or high levels of the endophyte Neotyphodium occultans. After five months, we quantified the number of nodules in Trifolium roots, shoot biomass of both plant species, and the contribution of atmospheric nitrogen fixation vs. soil nitrogen uptake to above ground nitrogen in each plant species. The endophyte increased grass biomass production (+ 16%), and nitrogen uptake from the soil – the main source for the grass. Further, it reduced the nodulation of neighbour Trifolium plants (−50%). Notably, due to a compensatory increase in nitrogen fixation per nodule, this reduced neither its atmospheric nitrogen fixation – the main source of nitrogen for the legume – nor its biomass production, both of which were doubled by rhizobial inoculation. In consequence, the total amount of nitrogen in aboveground biomass and aboveground productivity were greatest in mesocosms with both symbionts (i.e. high rhizobia + high endophyte). These results show that, in spite of the deleterious effect of the endophyte on the establishment of the rhizobia–legume symbiosis, the coexistence of these symbionts, leading to additive effects on nitrogen capture and aboveground productivity, can generate complementarity on the functioning of multi‐symbiotic systems.

Fungal endophyte symbiosis alters nitrogen source of tall fescue host, but not nitrogen fixation in co-occurring red clover

“…Schipanski and Drinkwater (2012) estimated that in red clover-orchardgrass mixtures, N fixation activity increased by 15 % due to transfer of fixed N between species. García Parisi et al (2014) also found that asexual Epichloë spp. infection of annual ryegrass almost doubled N fixation activity and biomass in neighboring white clover despite a reduction in nodulation.…”

Removal of Soil Microbes Alters Interspecific Competitiveness of Epichloë Endophyte-Infected over Endophyte-Free Leymus chinensis

“…In a recent study, we found that Epichloë endophyte colonization significantly inhibited AMF colonization of the host grass Achnatherum sibiricum, and the effects of AMF on host competition were variable and depended on the identity of the AMF species [18]. As AMF diversity is high in natural grasslands, and Epichloë endophyte colonization can affect AMF as well as other microbes [32][33][34], we hypothesized that Epichloë endophyte colonization could not only affect the competitive ability of the host directly by changing its growth and resistance, but also indirectly by changing soil microbes.…”

“…Epichloë endophytes may not only affect the growth and resistances of host grasses, but may also affect soil microbes, such as nitrogen-fixing bacteria, phosphorus-solubilizing rhizospheric fungi, arbuscular mycorrhizal fungi (AMF) and other microbial communities [30][31][32][33]. Can Epichloë endophyte-mediated modification of soil microbes affect the competitive ability of host grasses indirectly?…”

The Inhibitory Effect of Endophyte-Infected Tall Fescue on White Clover Can Be Alleviated by Glomus mosseae Instead of Rhizobia

“…Omacini et al [79] reported that rhizobia were sensitive to endophytic fungi. García Parisi et al [80] found that endophytic fungi could inhibit the number of nodules in leguminous plants but did not affect their growth. Our study found that rhizobia inoculation could significantly increase clover biomass when mixed with E− tall fescue; however, when mixed with E+ plants, the beneficial effect of rhizobia inoculation on clover disappeared.…”