Dark septate endophytes: mutualism from by-products?

Plant roots are abundantly colonized by DSE fungi in virtually all ecosystems, but the biology and ecological roles of these ubiquitous fungi are poorly understood. Development of genomics and other molecular methods has made research of root-associated fungal communities (including DSE symbiosis) timely. Understanding DSE symbiosis requires holistic evolutionary ecological approach. We consider by-product mutualism (sensu Connor Biol Rev. 1995;70:427–457) as a framework and present a schematic hypothesis of evolution of plant‐symbiont interactions. By-product mutualisms may be an important step between free-living saprotrophs and mutualistic mycorrhizal symbioses. Plant roots are abundantly colonized by dark septate endophytic (DSE) fungi in virtually all ecosystems. DSE fungi are functionally heterogeneous and their relationships with plants range from antagonistic to mutualistic. Here, we consider the role of by-product benefits in DSE and other root–fungal symbioses. We compared host investments against symbiont-derived benefits for the host plant and categorized these benefits as by-products or benefits requiring reciprocal investment from the host. By-product benefits may provide the variability required for the evolution of invested mutualisms between the host and symbiont. We suggest that DSE could be considered as ‘a by-product mutualist transitional phase’ in the evolution of cooperative mycorrhizal symbionts from saprotrophic fungi. Plant roots are abundantly colonized by dark septate endophytic (DSE) fungi in virtually all ecosystems. DSE fungi are functionally heterogeneous and their relationships with plants range from antagonistic to mutualistic. Here, we consider the role of by-product benefits in DSE and other root–fungal symbioses. We compared host investments against symbiont-derived benefits for the host plant and categorized these benefits as by-products or benefits requiring reciprocal investment from the host. By-product benefits may provide the variability required for the evolution of invested mutualisms between the host and symbiont. We suggest that DSE could be considered as ‘a by-product mutualist transitional phase’ in the evolution of cooperative mycorrhizal symbionts from saprotrophic fungi. organism feeding on other organism. mutually beneficial interaction between individual organisms equipped with traits that primarily benefit the bearer and benefit the other individual only as a side effect [35.Connor R.C. The benefits of mutualism: a conceptual framework.Biol. Rev. 1995; 70: 427-457Crossref Scopus (197) Google Scholar,41.Leimar O. Connor R. By-product benefits, reciprocity and pseudo–reciprocity in mutualism.in: Hammerstein P. Genetic & Cultural Evolution of Cooperation, Dahlem Workshop Report 90. MIT Press, 2003: 203-222Google Scholar]. mutually beneficial interactions between two organisms. symbiosis between plant roots and fungi, in which the fungus facilitates nutrient uptake from soil into the plant and receives carbon in return. self-investment by an organism benefits another organism as a by-product. Insect mating gifts, in which the male investment in their own reproduction benefits female mating behavior is an example of pseudoreciprocity [35.Connor R.C. The benefits of mutualism: a conceptual framework.Biol. Rev. 1995; 70: 427-457Crossref Scopus (197) Google Scholar,41.Leimar O. Connor R. By-product benefits, reciprocity and pseudo–reciprocity in mutualism.in: Hammerstein P. Genetic & Cultural Evolution of Cooperation, Dahlem Workshop Report 90. MIT Press, 2003: 203-222Google Scholar]. continuous reciprocal investments between individual organisms. Investment can come in many forms, for example (i) improving physical access to partners and their resources/services; (ii) improving/manipulation of the ability of the partner to provide beneficial services/resources; and (iii) improving the ability of an organism to effectively use the services/resources received for own survival and reproduction [35.Connor R.C. The benefits of mutualism: a conceptual framework.Biol. Rev. 1995; 70: 427-457Crossref Scopus (197) Google Scholar,41.Leimar O. Connor R. By-product benefits, reciprocity and pseudo–reciprocity in mutualism.in: Hammerstein P. Genetic & Cultural Evolution of Cooperation, Dahlem Workshop Report 90. MIT Press, 2003: 203-222Google Scholar] ability to feed on dead organic material. a close interaction between two organisms. The outcome of the interaction can be positive (mutualism), neutral (commensalism), or negative (parasitism).