Morphological and physiological traits
Arbuscular mycorrhizal fungal traits, including for example hyphal length, arbuscule morphology, or the robustness of spore walls, can modulate key functions/processes with ramifications not only to the health of the fungus itself but also the associated plant and the soil environment (see Table 1 for detailed descriptions of key traits, their hypothesized function, and methods for trait measurement). Here we define AM fungal traits primarily as “functional markers”, which are indicators of mycorrhizal function and are dependent on the morphological, physiological, or phenological characteristics of the fungal partner (Chaudhary et al. , 2022). In this context, AM fungal traits are most likely instrumental in defining ecosystem resilience and adaptability to environmental fluctuations, as certain fungal isolates with specific traits may demonstrate superior robustness or flexibility under changing conditions.
Conceptualizing the form and function of AM fungal traits becomes clearer when contextualized within the lifecycle of the fungal organism. We can broadly categorize the lifecycle of an AM fungus into two phases: (1) the asymbiotic phase, in which the dispersed spores are activated, germinate and explore the soil for a compatible host, and (2) the symbiotic phase, which includes the four following stages: a) the initiation of root colonization; b) the formation of structures within the root cortex; 3) the extension of mycelium into the soil matrix and possibly other hosts; and (4) spore production and dispersal. Briefly, spores, hyphal networks, and colonized root fragments, identified as the three principal types of propagules, remain dormant until the proper abiotic/biotic conditions emerge (Lanfranco et al. , 2018). Hyphae emerging from these propagules identify a host root, adhere to its surface, and commence root colonization. A swollen hyphopodium forms subsequently, from which a single hypha penetrates the root epidermis to access the root cortex. A series of morphogenetic and molecular processes come into play at these initial stages, enabling the plant to identify the presence of the fungus (as reviewed by (Bonfante & Perotto, 1995; Gianinazzi-Pearson et al. , 2007; Bonfante & Genre, 2010; Luginbuehl & Oldroyd, 2017). Upon reaching the root cortex, the fungus colonizes intercellular spaces, forming the intraradical mycelium (IRM). This mycelium then differentiates into structures such as arbuscules or coils, and, in some taxa, vesicles/ spores and the extraradical mycelium (ERM) which consists of runner hyphae, branched absorbing structures (BAS), spore associated BAS, and ”asexual” spores. Upon attaining a certain threshold of root colonization, hyphae extend beyond the root system into the soil matrix, forming the extraradical mycelium (ERM) and generating asexual spores. The expansive hyphal network, comprising IRM and ERM and spores, embodies the traits that underpin several ecosystem-level processes attributed to AM fungi. These traits impact not just the host plants and soil environment, but also the fungal organism itself.
AM fungal spores
Arbuscular mycorrhizal fungal spores are among the largest (Aguilar-Trigueros et al. , 2023) and most multinucleated spores (Kokkoris et al., 2020) known in the kingdom Fungi and exhibit the phenotypic characteristics that enable species identification. Three types of spore formation are recognized (Walker et al. , 2018). Glomoid spores are formed blastically at the tip of a hyphae or by intercalary inflation of a hypha. Acaulosporoid spores involve the blastic formation of a sporiferous saccule with a neck, followed by the differentiation of spores laterally or inside the neck, or inside the sporiferous saccule. Gigasporoid spores are differentiated at the tip of a small bulb or suspensor cell.
Spores range widely in their traits including size, shape, color, and wall thickness (see (Morton, 1988) for a review) across and within species. In fact, single isolates of some species are known to produce more than one type of spores (even the model fungus, Rhizophagus irregularis (Kokkoris et al. , 2023)). It has been reported that spores can be produced singly in the soil, in loose aggregates and in small or large sporocarps. The cytoplasm of the spores contains not only the nuclei (ranging from hundreds to thousands) but also lipid reserves that assist the germination and early colonization. Based on spore ontogeny, three main phenotypic characters are observed in AM fungal spores: spore wall, germinal walls, and germination structure - with the latter two not present in many species. In addition, the spore walls of many species show appendages and indentations. Some AM fungi produce sporocarps (i.e., aggregations of spores), which are called “glomerocarps” (Jobim et al. , 2019). Sporocarps have functions in reproduction (Yamato et al. , 2022) and dispersal, including dispersal by mammals (Mangan & Adler, 2002). Overall, variation in spore traits across species are hypothesized to reflect differences in reproduction (investing in fewer larger spores or many small spores), dispersal (long or short, different dispersal vector), survival in the absence of the host (e.g., resistance to desiccation and pathogenesis) and early colonization strategies (Chaudhary et al. , 2018).