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).