The Arbuscular Mycorrhizal Symbiosis: Origin and Evolution of a Beneficial Plant Infection

Arbuscular mycorrhizal fungi (AMF) represent a monophyletic fungal lineage (Glomeromycota) that benefits terrestrial ecosystems worldwide by establishing an intimate association with the roots of most land plants: the mycorrhizal symbiosis. This relationship results in an improved acquisition of nutrients (e.g., phosphate and nitrates) from the soil by the plant partners and, in exchange, allows the AMF to obtain the photosynthetically fixed carbon sources (e.g., sugars) necessary for their survival and propagation [1,2] (Figure 1). This fungal lineage is known to impact the function and biodiversity of entire ecosystems by producing extensive underground networks, composed of hyphae and spores, that interconnect a number of unrelated individual plant species [1,2]. These networks also function as a significant sink for atmospheric carbon dioxide, and represent significant underground ‘‘nutrient highways’’ that benefit entire plant and microbial communities. Indeed, AMF spores and hyphae are also a valuable source of food for many soil microorganisms (i.e., bacteria, other fungi, and nematodes), and because of their many beneficial effects on terrestrial ecosystems, AMF are widely used in organic agriculture and plant nurseries to improve the growth of economically important species. Besides their enormous benefits for terrestrial ecosystems around the globe, AMF are also known for their atypical evolutionary history and cellular features. For instance, it is currently thought that this intimate fungal–plant association has evolved over at least 500 million years—an extremely long-term co-evolutionary history, which has led many to suggest that AMF could have played a major role in the colonization of land by plants [3]. This hypothesis is also consistent with recent reports describing the capacity of some AMF species to infect the most ancient plant lineages (e.g., liverworts) and improve their overall fitness [4]. From a cellular point of view, AMF cells are at odds with those of many other eukaryotes, harbouring hundreds of haploid nuclei within one cytoplasm throughout their entire life cycle (i.e., septa are absent). The genetic structure of these co-existing nuclei has sparked a long-standing and intense scientific debate, and it is currently unclear whether such nuclei are genetically similar (e.g., homokaryons) [5] or divergent (e.g., heterokaryons) [6,7]. Nevertheless, it is now generally accepted by the mycorrhizal research community that genes isolated from one spore are often characterized by an atypically high degree of intra-individual sequence polymorphism.