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.
Agriculture touches all aspects of society and global environmental health. Dwindling phosphorous reserves are a looming crisis for civilization, and soil erosion typically far outpaces pedogenesis. Improving plant–mycorrhizal symbioses can enhance sustainable agriculture because mycorrhizas typically improve host‐plant nutrition and stabilize soils. Selective breeding of plants that gain greater benefits from mycorrhizas can provide considerable economic and environmental benefits. Our assessments demonstrate switchgrass genetic improvement increased or maintained production of two populations, and low‐input breeding increased mycorrhizal responsiveness, compared to parent lines. Selecting for increased mycorrhizal reliance may be an effective strategy for more sustainable and economical agricultural production.
Plant–mycorrhizal interactions are not typically assessed in crop breeding programs. Our experiment addresses this by determining host‐plant outcomes of newly developed synthetic (agronomic) populations compared with parent lines, following low‐input selective breeding. Assessing the potential of low‐input breeding to enhance crop mycorrhizal benefits is a critical step toward more sustainable agricultural production. We compared four synthetic populations of We assessed shoot and root biomass, shoot P concentration and P content, mycorrhizal growth response (MGR), and mycorrhizal phosphorous response (MPR). Importantly, we provide novel evidence that low‐input selective breeding increased mycorrhizal reliance of switchgrass synthetics compared to parent lines, with implications for global agricultural systems. There are substantial opportunities for plant traits associated with increased MGR and MPR to be transferred to a wide array of crops. Our findings indicate low‐input selective breeding can improve MGR and MPR. We propose these traits serve as a useful proxy for host‐plant mycorrhizal reliance, facilitating successful hologenome breeding to reduce fertilizer requirements.
- Award ID(s):
- 1946093
- NSF-PAR ID:
- 10449324
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- PLANTS, PEOPLE, PLANET
- Volume:
- 3
- Issue:
- 5
- ISSN:
- 2572-2611
- Page Range / eLocation ID:
- p. 578-587
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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