Review

Tansley review
The mycorrhizal symbiosis: research frontiers in
genomics, ecology, and agricultural application

Authors for correspondence: Francis M. Martin1,2 and Marcel G. A. van der Heijden3,4
Francis Martin 1
Email: [email protected] Universit
e de Lorraine, INRAE, UMR IAM, Champenoux, 54280, France; 2Institute of Applied Mycology, College of Plant Science
and Technology, Huazhong Agricultural University, Wuhan, Hubei, 430070, China; 3Department of Agroecology & Environment,
Marcel G. A. van der Heijden
urich, 8046, Switzerland; 4Department of Plant and Microbial Biology, University of Z€
Plant-Soil Interactions, Agroscope, Z€ urich,
Email: marcel.vanderheijden@agroscope.
admin.ch Z€
urich, 8057, Switzerland

Received: 14 August 2023

Accepted: 7 December 2023

Contents

Summary 1486 VI. Mycorrhizal symbiosis and plant community dynamics 1496

I. Introduction 1487 VII. Mycorrhiza applications 1497

II. Harnessing genomics to enhance our understanding of the VIII. Future directions 1497
development, evolution, and functioning of mycorrhizal
symbioses 1488
IX. Conclusion 1498

III. Mycorrhizal networks 1493

Acknowledgements 1498

IV. Mapping mycorrhizal diversity 1494

References 1498

V. Mycorrhizal symbiosis in ecosystems 1495

Summary
New Phytologist (2024) 242: 1486–1506 Mycorrhizal symbioses between plants and fungi are vital for the soil structure, nutrient
doi: 10.1111/nph.19541 cycling, plant diversity, and ecosystem sustainability. More than 250 000 plant species are
associated with mycorrhizal fungi. Recent advances in genomics and related approaches
Key words: arbuscular mycorrhizal fungi, have revolutionized our understanding of the biology and ecology of mycorrhizal
biodiversity, ectomycorrhizal fungi, ericoid associations. The genomes of 250+ mycorrhizal fungi have been released and hundreds
mycorrhizal fungi, mutualism, orchid of genes that play pivotal roles in regulating symbiosis development and metabolism have
mycorrhizal fungi, plant–microbe interactions, been characterized. rDNA metabarcoding and metatranscriptomics provide novel insights
population genetics.
into the ecological cues driving mycorrhizal communities and functions expressed by these
associations, linking genes to ecological traits such as nutrient acquisition and soil organic
matter decomposition. Here, we review genomic studies that have revealed genes involved
in nutrient uptake and symbiosis development, and discuss adaptations that are
fundamental to the evolution of mycorrhizal lifestyles. We also evaluated the ecosystem
services provided by mycorrhizal networks and discuss how mycorrhizal symbioses hold
promise for sustainable agriculture and forestry by enhancing nutrient acquisition and stress
tolerance. Overall, unraveling the intricate dynamics of mycorrhizal symbioses is paramount

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for promoting ecological sustainability and addressing current pressing environmental

concerns. This review ends with major frontiers for further research.

phosphorus (P), as well as a wide range of micro-elements (e.g. Fe,

I. Introduction
Cu, Zn, and Mn). Certain mycorrhizal fungi, including ECM and
It is widely acknowledged that mycorrhizal associations are ERM, also acquire organically bound N and P. Mycorrhizal fungi
prevalent in almost all terrestrial ecosystems, ranging from deserts receive carbon (C) compounds and vitamins from their host plants
and tropical forests to savannahs and arable land (Tedersoo in return for these nutrients and other benefits (van der Heijden
et al., 2014; van der Heijden et al., 2015). Over 80% of land plants et al., 2015; Martin et al., 2017).
(>250 000 plant species) form symbiotic associations with Mycorrhizal symbioses are of immense significance for biologists
mycorrhizal fungi (van der Heijden et al., 2008, 2015; Tedersoo and ecologists because of their profound influence on plant and
et al., 2014). Based on their structure and function, four major fungal growth, fitness, and diversity (van der Heijden et al., 2015;
types of mycorrhizal symbioses have been recognized: arbuscular Brundrett & Tedersoo, 2018). Moreover, these mutualistic relation-
mycorrhiza (AM), ectomycorrhiza (ECM), orchid mycorrhiza ships play a pivotal role in the N and P cycles within ecosystems (Saito
(ORM), and ericoid mycorrhiza (ERM; Fig. 1). Mycorrhizal fungi & Ezawa, 2016; Nehls & Plassard, 2018; Pellitier & Zak, 2018).
reside within the root cortex and rhizodermis. Fungal hyphae Numerous studies have demonstrated that AMF and ECM
extend from the roots into the soil, actively exploring for limited mycorrhizal symbionts can drain a substantial proportion of host
nutrients essential for plant growth, such as nitrogen (N) and C compounds, accounting for 5–30% of C flow. Globally, the flux of

(a) (b) (c) (d)

(e) (f) (g) (h)

Fig. 1 Typical structures of various types of mycorrhizal symbioses. (a) Arbuscular mycorrhizal fungi (AMF) spores of Rhizophagus irregularis containing
hundreds of stained nuclei; photo courtesy of Vasilis Kokkoris (Vrije Universeit, Amsterdam). Nuclei are visible due to staining with SYTO 13 Green Fluorescent
nucleic acid dye. Each image is the result of c. 300 z stacks (0.35-lm intervals) visualized using confocal laser scanning microscopy. Bar, 20 lm. (b) AMF
arbuscules in lettuce root cells colonized by an unknown species of native AMF. Hyphal threads were stained with WGA-Alexa Fluor 488, a chitin stain, and
visualized using confocal laser scanning microscopy; photo courtesy of Jen McGaley and Uta Paszkowski (University of Cambridge). (c) Fruiting body of the
ectomycorrhizal fly agaric Amanita muscaria; photo courtesy of Marcel van der Heijden. (d) Ectomycorrhizal roots formed between the ectomycorrhizal mate
bolet Xerocomellus pruinatus and pine (940 magnification); photo courtesy of Marc Bu
ee (INRAE). (e) Protocorms of the germinating orchid Serapias
vomeracea colonized by hyphae of the mycorrhizal fungus Tulasnella calospora. Only the plant cells in the basal part of the orchid protocorm (left) contain
mycorrhizal fungal coils, whereas the apical part of the protocorm (right) with the plant apical meristem is not colonized. The dark blue structures in some
of the colonized protocorm cells correspond to partially collapsed (and consumed) fungal coils that deliver carbon and nutrients to the orchid protocorm (Perotto
& Balestrini, 2023). Bar, 250 lm. Photo courtesy of Silvia Perotto (Universita di Torino). (f) Cross-section of a root of Pinus sylvestris colonized by the
ectomycorrhizal fungus Cenococcum geophilum. All typical features of the ectomycorrhizal symbiosis are shown, including a loose external mantle, aggregated
internal mantle, and Hartig net encasing epidermal and cortical root cells. Fungal hyphae are stained in green with WGA-Alexafluor 488, while root cells are
stained in red by propidium iodide (Bar, 50 lm; photo courtesy of Maira de Freitas Pereira (INRAE)). (g) Ascocarp of the truffle Tuber macrosporum; photo
courtesy of Janis Rogenmoser (University of Zurich). (h) Overview of root cells of Erica carnea colonized by hyphae of an ericoid mycorrhizal fungus stained in
blue (top panel), and an electron micrograph showing Pyrola minor cells containing a large number of fungal hyphae forming pelotons; photo courtesy of
Rosmarie Honegger (University of Zurich).

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plant-fixed C entering the living mycelium is equivalent to c. 36% of Basidiomycota, and 181 to Mucoromycota (including 13 to
annual CO2 emissions from fossil fuels (Hawkins et al., 2023). Glomeromycotina).
Therefore, it is important to investigate whether mycorrhizal fungi The release of the genomes of the ECM fungi Laccaria bicolor
influence soil organic C formation, especially the more persistent and Tuber melanosporum (Martin et al., 2008, 2010) and the AM
mineral-associated organic C pool, which is thought to be important fungi Rhizophagus irregularis (Tisserant et al., 2013) has opened up
for long-term C sequestration (Clemmensen et al., 2021; Hicks Pries new avenues for geneticists to compare the mycorrhizal genomic
et al., 2023; Horsch et al., 2023; Wu et al., 2023). In the context of blueprint with those of saprotrophic and pathogenic species,
ongoing global change, it is also crucial to investigate the role of thereby advancing our understanding of mycorrhizal symbiont
mycorrhizal associations in sustainable ecosystem functioning evolution. The current selection of sequenced mycorrhizal fungi is
(Angulo et al., 2022; Trivedi et al., 2022; Wang et al., 2022; Allsup based on their ability to establish different mycorrhizal associations,
et al., 2023). their ecological significance, phylogenetic relationships, and
Over the past two decades, genomics, as a tool for analyzing the practical considerations. This array of available genome sequences
genetic information of organisms, has emerged as a fundamental provides opportunities to investigate the evolutionary patterns and
approach for understanding the biology, evolution, and ecology of functional attributes of mycorrhizal symbioses across dozens of
mycorrhizal symbioses. In addition to providing critical mechan- fungal families (Wolfe et al., 2012; Kohler et al., 2015; Peter
istic insights, genetic information also identifies targets that can be et al., 2016; Murat et al., 2018; Miyauchi et al., 2020; Marqu
es-
prioritized for the application of mycorrhizal symbioses in G
alvez et al., 2021; Lebreton et al., 2022; Looney et al., 2022;
agriculture and forestry. In this review, we discuss recent studies Kobayashi et al., 2023; Plett et al., 2023). For several families, such
that illustrate the impact of genomics and related approaches (e.g. as Boletales, the data highlighted not only which areas of the
DNA metabarcoding and transcriptomics) on our understanding genomes were similar between the different species but also when
of mycorrhizal associations. First, we summarize the current their sequences diverged on a scale of millions of years (Miyauchi
knowledge on mycorrhizal fungal genomes and their implications et al., 2020; Lofgren et al., 2021; Wu et al., 2022). The primary
for understanding the transition from saprotrophism to symbiosis objectives of these genome-based studies were to (1) monitor the
across the fungal tree of life. Second, we examine how the genomes various independent lifestyle transitions from saprotrophism to
of mycorrhizal fungi and their host trees have been utilized to mutualism in fungal lineages (e.g. Agaricales, Boletales, and
understand the molecular mechanisms underlying the establish- Russulales), (2) establish connections between genome character-
ment and function of symbiosis. These resources have facilitated istics and important ecological traits, such as nutrient uptake and
the identification of the genes and pathways involved in symbiotic soil organic matter (SOM), and (3) identify gene sets involved in
development, nutrient exchange, and stress tolerance. Third, we the development and functioning of mycorrhizal associations.
discuss how high-throughput metabarcoding tools have unraveled In the following sections, we provide a summary of the key findings
the remarkable biodiversity of soil fungi, revealing their distribu- of these studies regarding the major types of mycorrhizal symbioses.
tion from small soil cores to the entire continent. In our discussion,
we emphasize the significance of mycorrhizal networks in natural
1. Arbuscular mycorrhizal fungi
ecosystems and highlight their roles in providing various ecosystem
services. We also briefly discuss the potential applications of Arbuscular mycorrhizal fungi (AMF) have captivated evolutionary
mycorrhizal symbiosis in sustainable agriculture and ecosystem biologists because of their ancient origins, which date back to c.
restoration, underscoring the importance of understanding the 500 million years (Fig. 2; Simon et al., 1993; Brundrett &
functional traits and ecological roles of mycorrhizal fungi. By Tedersoo, 2018). Their long evolutionary history and distinctive
synthesizing the latest research findings, this review aims to identify biological characteristics make them fascinating subjects of study.
knowledge gaps and propose future directions for mycorrhizal Ambiguity remained concerning the evolutionary history of
research to address the global challenges in agriculture, forestry, and Glomeromycota, either as sister to Mucoromycota and Mortier-
environmental sustainability. ellomycota, or as sister to Dikarya (Ascomycota and Basidiomy-
cota). Although it is generally thought that Mucoromycota
comprises three subphyla, Glomeromycotina, Mortierellomyco-
II. Harnessing genomics to enhance our
tina, and Mucoromycotina, and is sister to Dikarya (Spatafora
understanding of the development, evolution, and
et al., 2016), it is worth noting that some authors have re-elevated
functioning of mycorrhizal symbioses
Glomeromycotina to a phylum (Strassert & Monaghan, 2022).
The Joint Genome Institute (JGI) MycoCosm database currently Arbuscular mycorrhizal fungi possess coenocytic hyphae that
contains 2701 fungal genomes (as of November 2023), including contain thousands of nuclei and reproduce as large multinucleated
220+ mycorrhizal fungi, and the National Center for Biotechnol- spores (Fig. 1). To date, nuclear genome assemblies have been
ogy Information GenBank has annotations for 4770 genomes (as of released from representative species of different AMF orders, from
November 2023), demonstrating the enormous progress made in Glomerales to Diversisporales, and Archaeosporales. They have
the field (Martin et al., 2011; Grigoriev et al., 2014). The fungal unusually large genomes: c. 150 Mb for Rhizophagus species to
species that have been sequenced are highly diverse and comprise 784 Mb for Gigaspora species (Tisserant et al., 2013; Kobayashi
major clades of Mycota. Among the genomes available in the et al., 2018; Morin et al., 2019; Venice et al., 2020), which are rich
MycoCosm database, 1693 belonged to Ascomycota, 696 to in repetitive sequences. The early diverging AMF Paraglomus

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Antiquity of genomic traits related Ma Oldest known fossils

to mycorrhizal evolution based on 23
molecular clock estimates

Paleogene
50 Ectomycorrhizas

66
Ericaceae (Leucothoe)

Origins of soil and litter decomposers: Medicago

Cretaceous
loss of lignin oxidoreductases; CAZYmes expanded
Multiple origins of ericoid and orchid mycorrhizal 100
associations: maintenance of a high repertoire of
PCWDEs Quercus

Angiosperms

145
Multiple origins of ectomycorrhizas: losses of lignin
oxidoreductases and PCWDEs; diversification of
MiSSPs
Jurassic

Multiple origins of brown rots 201

Triassic

Pinus

Origin of white rots 254

Permian

Conifers
Diversification of saprophytic cellulolytic apparatus: Early relatives of conifers Telemachus
expansion of CAZymes (e.g. GH6, GH7) Cordaites

Early saprophytic or parasitic Agaricomycotina; 299 Mycorrhizal associations involving

Carboniferous

limited ligninolytic peroxidases and CAZymes Pennsylvanian roots (= true mycorrhizas)

Loss of PCWDEs in Glomeromycotina Occurrence of Basidiomycota

Mississippian
(based on occurrence of clamp connection)
359
Devonian

Late Trees and forests

Middle
Fungal–plant associations (paramycorrhizas)
Early
Occurrence of Mucoromycotina
419 Stratified lichens
Possible origin of the common symbiotic
Ordovician Silurian

signaling pathway (CSSP)

Terrestrial plant remains – Charophytes
443
Late
Spores attributed to terrestrial plants
Middle
Occurrence of Glomeromycotina
Early
485
Late
Cambrian

Middle

Early Horneophyton
Liverwort-like plants
541

Fig. 2 Emergence of key symbiotic genomic traits related to mycorrhizal symbiosis evolution (left) based on molecular clock estimates along the geological
time scale/geological epochs from the Cambrian to the Paleogene (middle) with oldest known fossils (right). The orange asterisk represents the formation of
the Rhynie chert at 407 Ma. Illustrations of early land plants (liverwort-like plants, Horneophyton), early relatives of conifers (Cordaites), conifers (Telemachus,
Pinus), and Angiosperms (Quercus, Medicago) are shown. CAZymes, carbohydrate-active enzymes; GH, glycosyl hydrolase; MiSSPs, mycorrhiza-induced
small secreted proteins; PCWDEs, plant cell wall-degrading enzymes. Adapted from Strullu-Derrien et al. (2018).

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occultum (Paraglomerales) possesses a much smaller genome size nucleus and spatial RNA sequencing techniques to explore the
(39.6 Mb) and fewer genes and repeats than most AMF relatives transcriptomes of AM symbiosis at the cellular and spatial
(Malar et al., 2022). Intriguingly, these early-branching AMF resolution level. They identified cell type-specific responses to
appear to be less beneficial in terms of stimulating plant growth symbiosis, in agreement with previous studies using laser capture
than the more recently evolved AMF (S€ale et al., 2021). The microdissection-based transcriptomic analyses (Gaude et al., 2012;
genome of Geosiphon pyriformis (Archaeosporales), which estab- Hogekamp & K€ uster, 2013). These RNA profiling studies have
lishes symbiosis with the N-fixing cyanobacterium Nostoc identified a set of robust symbiosis-responsive genes, including
punctiforme, shares all hallmarks of obligate AMF biotrophy, many characterized marker genes that are critical to symbiosis, such
suggesting that this fungus has an evolutionary history similar that as those involved in P metabolism (e.g. MtPT4) and those encoding
to of AMF (Malar et al., 2021). Genome and molecular biology effector-like proteins (Fig. 2). Although the identity and function of
analyses have revealed that AMF obligate biotrophy results from a most transcripts differentially expressed by plants and fungi during
loss of fatty acid biosynthesis but also entails the loss of genes symbiotic interactions have not yet been characterized, these studies
encoding plant cell wall-degrading enzymes (PCWDEs), as well as provide valuable insights into the molecular mechanisms under-
genes involved in thiamine synthesis (Tisserant et al., 2013; lying AM symbiosis (see Lanfranco & Bonfante, 2023 for a review).
Reinhardt et al., 2021). A breakthrough was the demonstration that As effector-like small secreted proteins and small RNAs play a
host plants supply R. irregularis with large amounts of fatty acids key role in plant–pathogen interactions, they have also been
(Kameoka & Gutjahr, 2022). The combination of Hi-C and HiFi investigated in AM associations (Ledford et al., 2023). Aparicio
PacBio sequencing identified two sets of homologous chromo- Chac
on et al. (2023) identified a set of mycorrhiza-induced secreted
somes among thousands of coexisting nuclei in AMF hetero- effector-like proteins, some of which regulate the expression of host
karyons. These two sets of related genomes differ in content, gene genes. Teulet et al. (2023) found proteins with structural similarity
expression, and epigenetic regulation, and the abundance of each to known Fusarium oxysporum dual domain effectors. Of the
set varies depending on the host plant and environmental hundreds of predicted effector proteins from the AM fungus R.
conditions (Sperschneider et al., 2023). irregularis, only five have been characterized to date: nucleus-
The notion that AMF are ancient asexual organisms has been localized secreted protein 7 (Kloppholz et al., 2011), putative
challenged by genomic analysis (Ropars et al., 2016). Genomic strigolactone-induced secreted protein 1 (Tsuzuki et al., 2016),
regions and nuclear organizations associated with sexual reproduc- nucleus-localized crinkler effector 1 (Voß et al., 2018), secreted
tion have been identified, including meiosis-specific genes, putative LysM-containing effector RiSLM (Zeng et al., 2020), and nuclear-
mating-type loci, and homokaryotic-dikaryotic life stages (Kok- localized effector 1 (Wang et al., 2021).
koris et al., 2021; Reinhardt et al., 2021; Yildirir et al., 2022). There is limited information on how plant or fungal genetic
Various Mucoromycotina fungi can establish AMF-like sym- variations affect plant transcriptional responses to fungi (Mateus
biotic associations with liverworts, hornworts, and other land et al., 2019). The impact of AMF endobacteria and virome and
plants. However, the genomes of these symbionts have not yet been hyphal-associated microbial communities on the regulation of gene
sequenced. These so-called fine-root endophytes can enhance plant expression and physiological capabilities of the association remain
growth and nutrition (Hoysted et al., 2023) and are often more unclear and require further investigation (Lanfranco & Bon-
abundant in agricultural fields than in native biomes (Albornoz fante, 2023).
et al., 2022). Niche differentiation between the Mucoromycotinian
and Glomeromycotinian AMF has been suggested (Mansfield
2. Ectomycorrhizal fungi
et al., 2023), pointing to their agronomic and ecological relevance,
as they may have complementary functions in ecosystems. Genome The transition from saprotrophism to ECM symbiosis is a key
sequencing of fine-root endophytes will highlight their evolution, evolutionary event that has occurred multiple times during the
biology, and ecology. evolution of Fungi (Tedersoo et al., 2010; Strullu-Derrien et al.,
The development of symbiotic structures and metabolic activity 2018; Fig. 2). Although the exact mechanisms driving these
in symbiotic tissues requires integrated coordination and commu- transitions remain unclear, comparative genomic and phyloge-
nication between symbionts, leading to changes in gene expression nomic studies have provided hypotheses and patterns for further
and activation of signaling pathways. Conservation of the ‘common investigations (Kohler et al., 2015; Miyauchi et al., 2020; Lebreton
symbiotic signaling pathway’ (CSSP) among various angiosperm et al., 2021). The transition to an ECM lifestyle likely occurred
species is highly noteworthy (Fig. 2; Delaux et al., 2015). This through a series of steps, starting with soil/litter saprotrophic fungi
underscores the shared evolutionary origin of this ancient symbiotic colonizing plant roots and gradually forming a mutualistic
signaling pathway. Phylogenomic studies have suggested that relationship with the host. Ecological factors such as easy access
certain features of this pathway may have predated the evolution of to soluble carbohydrates may have driven this transition. In
the first terrestrial plants in the Middle to Late Ordovician and nutrient-poor environments, the formation of mutualistic associa-
contributed to the establishment of the earliest AM associations tions with plants allows ECM fungi to access soluble carbohydrates
with ancestral land plants (Delaux et al., 2015). To date, only a few and vitamins, thereby expanding their ecological niche. The ability
studies have measured fungal transcriptional responses to different of ECM fungi to form symbiotic associations with a diverse range
environmental conditions (Grunwald et al., 2009; Hohnjec et al., of tree species suggests adaptive radiation, specific symbiotic
2005; Zeng et al., 2018). Serrano et al. (2023) utilized both single- mechanisms, and niche specialization during their evolutionary

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history (Martin et al., 2016, 2017; Sato, 2023; Fig. 2). ECM Lebreton et al., 2021). This makes mycorrhizal fungi dependent on
fungal lineages diverging in the Late Cretaceous might have had their host plants for C. Nevertheless, many of the sequenced fungi
opportunities to co-evolve with ECM angiosperms (e.g. through have maintained a unique array of PCWDEs, including endoglu-
the development of host recognition systems; Tang et al., 2021; canases and oxidoreductases/laccases, suggesting that several ECM
Lebreton et al., 2022; Looney et al., 2022) and repression of plant fungi possess diverse abilities to scavenge plant and microbial detritus
defenses (Plett et al., 2011, 2014; Kang et al., 2020), resulting in (necromass) from soil and litter (B€odeker et al., 2014; Veneault-
their expansion into novel niche spaces and subsequent rapid Fourrey et al., 2014; Op De Beeck et al., 2018; Pellitier & Zak, 2018;
diversification (Martin et al., 2016; Sato, 2023). The repeated Nicol
as et al., 2019; Floudas et al., 2020; Maillard et al., 2023). Fine-
evolution of the ECM lifestyle (and the absence of reversion to the tuned regulation of these PCWDE genes is necessary to avoid
ancestral state) and convergent evolution in hundreds of fungal triggering plant defense responses (Miyauchi et al., 2020).
lineages highlight its adaptive significance and underscore the In Mucoromycota, Endogonales is an enigmatic group of fungi
selective pressures driving this evolutionary development (Wolfe that establish ectomycorrhizal symbiosis and biotrophic associa-
et al., 2012; Lebreton et al., 2021). tions with ferns, lycophytes, hornworts, and liverworts, as well as
Gene copy numbers of PCWDEs tend to show distinct patterns comprising of putative saprotrophs associated with decayed wood
associated with specific ecological niches in fungi (Floudas et al., and leaf litter (Desiro et al., 2017). To better understand the
2012, 2020; Kohler et al., 2015) because of their role in the evolution of mycorrhizal symbioses and trophic ecology in
degradation of plant cell wall material (Fig. 2). A drastic contraction Endogonales, the genomes of four collections of Endogonaceae,
in the gene families encoding PCWDEs is a hallmark of ECM and including three ECM collections and one putative saprotroph, were
AM fungi (Fig. 3). Most lack ligninolytic class II peroxidases sequenced (Chang et al., 2019). The genomes of ECM isolates
(PODs), invertases, endocellulases, cellobiohydrolases, and exhibit typical characteristics of ECM fungi, including a restricted
cellulose-binding motifs, which restrict their ability to degrade set of PCWDE genes. Furthermore, dating analysis suggested that
SOM and the plant cell walls of their hosts. As ancestral ECM Endogonaceae originated in the Permian–Triassic boundary,
lineages shifted toward symbiotic relationships, the need for these indicating that the mycorrhizal association between Endogonales
degradative enzymes diminished, resulting in their gradual loss over and plants may have played a critical role in the colonization of land
evolutionary time (Martin & Selosse, 2008; Wolfe et al., 2012; by plants.

200
CAZyme gene
copy number
Lower Higher
150 9 Glomerales
25 Pezizales
80 Boletales
Orchid
30 Russulales
mycorrhizal
100 2 Thelephorales
fungi
Arbuscular 33 Agaricales
PC2 (9.91%)

mycorrhizal 1 Eurotiales
fungi 13 Cantharellales
50 2 Onygenales
2 Corticiales
3 Atheliales
1 Hysterangiales
0 1 Diversisporales
6 Sebacinales
Ericoid
1 Gomphales
mycorrhizal
7 Helotiales
fungi
–50 Ectomycorrhizal 1 Pleosporales
fungi

–100
–200 –100 0 100 200 300 400
PC1 (74.52%)

Fig. 3 Differential distribution of the gene copy numbers for CAZyme genes acting on microbial, fungal, and plant polysaccharides, and lignin derivatives in
the genomes of 217 species of arbuscular mycorrhizal fungi, ectomycorrhizal fungi, orchid mycorrhizal fungi or ericoid mycorrhizal fungi with contrasting
ecologies. Principal coordinate analysis of the total CAZyme gene copy numbers identified in arbuscular mycorrhizal fungi, ectomycorrhizal fungi, ericoid
mycorrhizal fungi, and orchid mycorrhizal fungi. Each symbol corresponds to a genome of the mycorrhizal species available in the JGI MycoCosm database
(mycocosm.jgi.doe.gov). The taxonomic order of the sequenced species is indicated by different colored symbols as shown in the legend (right panel). Note the
divergent distributions in CAZyme gene sets in various mycorrhizal lifestyles with an increasing repertoire of CAZyme from arbuscular mycorrhizal fungi (lower) to
ericoid mycorrhizal fungi (higher; from left to right). Principal component analysis (PCA) was performed using the MycoCosm PCA tool (mycocosm.jgi.doe.gov).
CAZyme gene repertoires were obtained after semi-manual curation of protein sequences by the CAZy team (www.cazy.org) (Drula et al., 2022).

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The field of mycorrhizal genetics has strayed beyond mere on colonization by mycorrhizal fungi for their establishment and
genome comparison and gene discovery to the realm of systems growth (Perotto & Balestrini, 2023). Thus, orchids cannot survive
biology, exploring the cellular and molecular bases of symbiosis. without mycorrhizal fungi (Rasmussen & Rasmussen, 2014). In
This evolution was driven by the availability of large-scale recent years, there has been a growing interest in the genomics of
transcriptomic datasets (Plett et al., 2014, 2019; Liao et al., orchids and ORM fungi to unravel the genetic mechanisms
2018; Bouffaud et al., 2020; Ruytinx et al., 2021). They have underlying orchid-fungal interactions and the specificity of these
facilitated the identification of gene networks and hubs involved in symbiotic relationships (Chen et al., 2022; Song et al., 2022). The
key biological processes such as nutrient uptake, metabolism, and genomes of several orchid species (Cai et al., 2015; Zhang
signaling in ECM symbiosis. Various ECM symbioses are et al., 2016, 2017; Yang et al., 2021; Jiang et al., 2022; Li
characterized by the upregulation of genes from overlapping et al., 2022) have been sequenced. Comparison of chromosome-
functional categories, such as information storage and processing, scale genome assemblies of two closely related orchid species, the
transport, and metabolism. However, each association expressed a partially mycoheterotrophic P. zijinensis and the fully mycoheter-
distinct set of symbiosis-associated genes involved in redox otrophic P. guangdongensis, with genomes of autotrophic orchids,
reactions, nutrient transport, and metabolism. A significant suggests that mycoheterotrophy is associated with increased
number of these genes have orthologs in saprotrophic species, substitution rates and gene loss in P. guangdongensis. Conversely,
indicating that they are not unique to ECM fungi but are associated trehalase genes, which are responsible for converting trehalose to
with essential core metabolic pathways (Lebreton et al., 2022; glucose, have expanded in most sequenced orchids, reflecting the
Looney et al., 2022; Wu et al., 2022). Because of these alterations in reliance of orchid seeds, which lack endosperms, on trehalose
gene expression, ectomycorrhizal interactions lead to changes in the obtained from ORM fungi during the protocorm stage. Further-
levels of fungal and host plant metabolites, including marked shifts more, this study showed that mature plants of P. guangdongensis,
in the metabolism and transport of carbohydrates, amino acids, unlike photosynthetic orchids, continue to express trehalase genes
aromatic acids, organic acids, fatty acids, and water (Hortal to exploit the trehalose released by its mycosymbionts.
et al., 2017; Plett et al., 2021, 2023; Tang et al., 2021; Bogar, 2023; Genome sequencing efforts have targeted specific ORM fungi to
Stuart et al., 2023). gain a deeper understanding of their genetic repertoires and
Novel genes specific to the ECM lifestyle, such as those coding symbiotic capabilities. The genomes of Tulasnella calospora,
for mycorrhiza-induced small secreted proteins (Plett et al., 2011, Sebacina vermifera, and Ceratobasidium spp. (Miyauchi et al.,
2014; Plett & Martin, 2011; Pellegrin et al., 2015) and small RNAs 2020) have been published, and a dozen additional ORM fungi in
(Wong-Bajracharya et al., 2022), have also emerged, enhancing the Tulasnellaceae, Serendipitaceae, and Ceratobasidiaceae have been
symbiotic capabilities of ECM fungi and controlling host plant sequenced at the JGI. In contrast to ECM and AMF, ORM fungi
immunity as well as the ingress of other microbes colonizing the possess a large set of PCWDEs that are expressed during their
host plant. Several genes that possibly mediate compatibility interactions (Balestrini et al., 2014; Chen et al., 2017, 2022;
between plants and fungi have been identified (Lofgren et al., 2021; Ghirardo et al., 2020; Fig. 3). Similar to ERM fungi, ORM species
Tang et al., 2021; Lebreton et al., 2022). often have a higher set of PCWDEs than wood decayers and
Identifying plant genes that contribute to and are required for soil/litter decomposers (Miyauchi et al., 2020), which supports
ECM symbiosis is a daunting task, and a limited number of genes their dual saprotrophic/symbiotic lifestyles. We hypothesized that
have been identified and characterized (Tagu et al., 2005; Labb
e the size of the PCWDE repertoire is reflective of the age of the
et al., 2019). Notably, Cope et al. (2019) have demonstrated that mycorrhizal symbiosis along the saprotrophy to symbiosis
the ECM fungus L. bicolor releases lipochitooligosaccharides and continuum, with AMF symbiosis emerging in the Early Devonian
uses the CSSP to colonize Populus roots. On the other hand, the (393–419 Ma), ECM symbiosis during the Jurassic (c. 200 Ma),
conserved core CSSP genes appear to be missing in the ECM- and mycorrhizal associations with Ericaceae and orchid species up
forming Pinaceae lineage (Garcia et al., 2015). to the Cretaceous (c. 117 Ma; Strullu-Derrien et al., 2018; Fig. 2).
Continued efforts in genomics will further enhance our under-
standing of the complex interactions between orchids and their
3. Orchid mycorrhizal fungi
mycorrhizal partners, contributing to conservation efforts and
With nearly 30 000 species, the orchid family offers valuable orchid cultivation in horticulture and restoration practices.
resources for studying plant evolution and environmental adapta-
tion, and serves as an economically and culturally important
4. Ericoid fungi
ornamental plant in human society. Orchids appeared to have
emerged c. 112 million years ago (Ma; Fig. 2). The subfamilies Ericoid mycorrhiza fungi form mutualistic symbioses with a wide
Orchidoideae and Epidendroideae diverged from each other at the range of Ericaceae plants, including heathers, blueberries, and
end of the Cretaceous, and the tribes of the upper epidendroids rhododendrons, and play crucial roles in nutrient acquisition
diverged rapidly between 37.9 and 30.8 Ma (Givnish et al., 2015; and stress tolerance in nutrient-poor and acidic soils. Genome
Zhang et al., 2017). Orchids are renowned for their reliance on sequencing has focused on several key ERM species, including the
mycorrhizal fungi during germination, seedling establishment, and archetypal ERM fungi Rhizoscyphus ericae and Oidiodendron maius
nutrient acquisition, particularly during the early stages of their life (Kohler et al., 2015; Grelet et al., 2016; Martino et al., 2018). The
cycle. The protocorms of germinating orchids are fully dependent availability of these genomes has provided insights into the genetic

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repertoire and functional attributes of ERM fungi. According to

III. Mycorrhizal networks
phylogenomic analysis, the most recent common ancestor of the
sequenced ERM fungi, including O. maius, M. bicolor, M. Underground mycorrhizal networks are crucial for nutrient
variabilis, and R. ericae, was estimated to be c. 118 Ma (Martino acquisition and transport by plants. They consist of interconnected
et al., 2018). Remarkably, this age coincides with the emergence of hyphae that extend from the mycorrhizal roots to the surrounding
the Ericaceae family, which was estimated to have originated c. soil, forming extraradical mycelial threads (Fig. 4). In natural soils,
117 Ma (Fig. 2; Schwery et al., 2015). This suggests that ancestral numerous intermingled mycorrhizal networks of varying sizes
ERM fungi and their plant partners have undergone simultaneous develop as each host plant is colonized by multiple fungal
diversification, and the early establishment of this symbiosis may symbionts, up to several dozen per adult tree (Rog et al., 2020).
have initiated evolution of the Ericaceae family. This resembles They play a vital role in efficiently prospecting soil, scavenging
theories that symbiotic associations between plants and early AM, nutrients, transporting them to the host roots, and contributing to
such as fungi, enabled plants to colonize land at 450 Ma (Selosse & essential ecosystem services, including soil structure enhancement
le Tacon, 1998). Unlike other types of mycorrhizal associations, and water uptake (Table 1). Furthermore, mycorrhizal networks
ERM fungi demonstrate a relatively low dependence on plants play a crucial role in C cycling and storage (Hawkins et al., 2023;
because of their enhanced saprotrophic capabilities. Their extensive Table 1). The establishment and activity of these hyphal networks
repertoire of degradative enzymes indicates that they may be relies on a continuous supply of plant C compounds.
facultative symbionts representing recently recruited lineages of Within hyphal networks established by mycorrhizal fungi, a
soil-decomposer fungi, many of which are endophytes (Grelet specific subset called common mycorrhizal networks (CMNs) is
et al., 2016; Martino et al., 2018). The sustained expression of formed when the mycobiont establishes physical connections
PCWDEs in colonized roots likely aids in penetrating the thick between the roots of two or more plant species. The transfer of
outer cell walls of plants, allowing the establishment of intracellular sugars and other nutrients among interconnected plants, often
structures within the epidermal root cells of ericaceous hosts involving saplings, through CMNs has been suggested in several
(Martino et al., 2018). studies (Finlay & Read, 1986; Arnebrant et al. 1993; Simard

MN 5
7 6 1
3
4 2
CMN

Amino acids
Carbohydrates
MN Fatty acids MN
Hormones
MicroRNAs
Peptides MN
?

Fig. 4 View of the soil mycorrhizal community in a hypothetical forest dominated by oak species associated with different types of mycorrhizal fungi that form
separate underground networks (MN) that may possibly be used to transport amino acids, carbohydrates, fatty acids, signaling microRNAs or peptides and
hormones. An evergreen oak (Quercus ilex) (1) forms ectomycorrhizal roots and hyphal networks with Xerocomellus chrysentheron (red cracking bolete) (2)
and Laccaria amethystina (amethyst deceiver) (3), whereas a sessile oak (Quercus petrea) (4) establishes ectomycorrhiza (ECM) and hyphal networks with
Xerocomellus chrysentheron (2) and fly agaric (Amanita muscaria) (5). ECM rootlets are shown as colored dots on root systems. X. chrysentheron hyphal
networks link Q. ilex and Q. petrea through a common mycorrhizal network (CMN). The nonphotosynthetic bird’s nest orchid Neottia nidus-avis and its orchid
mycorrhiza (ORM) fungal network (6) parasitize the evergreen oak mycorrhizal network. The lesser periwinkle (Vinca minor) is colonized by AMF, forming an
independent mycorrhizal network (7). Different colors represent different mycorrhizal fungal networks, with ECM rootlets as dots of the same color. Note that
other combinations are possible (e.g. boreal forests with ECM trees often harbor an understory of shrubs (e.g. Vaccinium) that form ericoid mycorrhiza (ERM)
associations; Illustration courtesy of Florian Gadenne).

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Table 1 Ecosystem services provide by mycorrhizal mycelia and networks.

Ecosystem service Ecological importance Selected references

Nutrient uptake and plant Mycorrhizal fungi can promote plant growth and nutrient uptake. Up to 90% van der Heijden et al. (2008)
growth stimulation of plant P and N can be acquired by mycorrhizal fungi. Some plants are fully
dependent on nutrients acquired by mycorrhizal fungi.
Belowground C storage Plants allocate 5–30% of their photoassimilates to mycorrhizal symbionts. Up van der Heijden et al. (2008); Hawkins
and C cycling to 13 Gt of CO2 fixed by terrestrial plants is, at least temporarily, allocated to et al. (2023)
the underground mycelium of mycorrhizal fungi.
Soil structure formation Fungal hyphae and hyphal exudates enmesh soil particles together into larger Jastrow et al. (1998)
and aggregation aggregates and contribute substantially to the promotion of soil structure.
Water uptake and Reduction in nutrient leaching by mycorrhizas. Water uptake by fungal Ahonen-Jonnarth et al. (2003); Cavagnaro
reduction in nutrient hyphae. Evidence from natural systems is largely missing. et al. (2015); Kakouridis et al. (2022)
leaching losses
Promotion of seedling CMN can quickly colonize the roots of emerging seedlings and can have van der Heijden & Horton (2009)
establishment strong effects on the success of seedling establishment. No effects or even
negative effects are also regularly reported.
Interplant C and nutrient High amounts of transfer have been observed in mycoheterotrophic plants Simard et al. (1997); Klein et al. (2016);
transfer and orchid protocorms. The ecological significance of transfer among green Henriksson et al. (2023); Karst et al. (2023);
plants is debated and needs further study. Merckx (2023)

et al., 1997; Wu et al., 2001; Klein et al., 2016; Selosse et al., 2016; Consequently, the ecological significance of CMNs in nutrient
Cahanovitc et al., 2022). However, the mechanisms underlying cycling has been the subject of scrutiny and debate (Robinson &
these transfers are complex, and it is challenging to discern the Fitter, 1999; Henriksson et al., 2023; Karst et al., 2023; Robinson
specific role of CMNs vs other pathways such as nutrient and signal et al., 2024). Therefore, there is an urgent need to identify the
movement through the soil solution (Babikova et al., 2013). physiological and ecological roles of mycorrhizal networks
Many mycorrhizal fungi are generalists and have a broad host range, (including CMNs) in natural ecosystems, and their relative
and several plants can be interconnected by hyphal networks. For importance in supporting plant growth and seedling establishment.
instance, glasshouse experiments have provided evidence that R. Imaging tools for tracking and probing individual hyphae in
irregularis is not host-specific, and that all mycorrhizal hosts within intermingled mycelial networks in soils should be developed to test
plant communities can possibly be interconnected by CMN formed whether nuclei, transcripts, proteins, and metabolites can migrate
by this symbiont (van der Heijden, 2004; Kivlin, 2020). In AMF, the from one plant individual to another via CMNs. Integrated
fusion of hyphae through anastomosis and hyphal healing mechan- approaches combining multi-locus genomic sequencing to assess
isms has been observed in vitro (Giovannetti et al., 2001; de la the spatial distribution and size of genotypes, their activity by
Providencia et al., 2005). Hyphal fusion plays a crucial role in AMF metatranscriptomics/metaproteomics, and the measurement of
networks, ensuring their interconnectedness and physical stability; metabolic fluxes between different mycorrhizal plants in natural
however, the spatial distribution of these networks in situ is unknown. settings are currently being developed and will provide valuable
In ECM fungi, genetic individuals (genets) can simultaneously information on the functioning of mycorrhizal networks.
colonize multiple trees (Beiler et al., 2010). DNA fingerprinting
studies have identified large genets in several Boletales species (Fiore-
IV. Mapping mycorrhizal diversity
Donno & Martin, 2001; Hirose et al., 2004; Beiler et al., 2010).
Although these studies have provided evidence of very large genetic In recent years, there has been strong focus on documenting
individuals (> 10 m), the extent of physiological integration or underground biodiversity and creating global maps of various soil
communication between different parts of these extensive mycelial organisms. Efforts have been made to provide global maps of
networks remains largely speculative and requires further investiga- microbial biomass (Xu et al., 2013), earthworms (Phillips
tion. Most importantly, the size of ECM genets, including their et al., 2019), protists (Oliverio et al., 2020), bacteria (Bahram
subterranean mycelial networks (and CMNs), is expected to be et al., 2018; Delgado-Baquerizo et al., 2018), fungi (Tedersoo
considerably smaller. Most species investigated thus far have produced et al., 2014; Vetrovsk
y et al., 2020), and overall soil biota (Delgado-
much smaller genets (< 1 m; Gryta et al., 2000; Grelet et al., 2010; Baquerizo et al., 2020). In addition, global distribution maps of
Hortal et al., 2012; Murat et al., 2013). If genetic individuals are of mycorrhizal plants, AM, and ECM fungi have been published (Opik €
small size, it is unlikely that hyphae produced by different fungal et al., 2010; Tedersoo et al., 2014; Davison et al., 2015; Soudzi-
species originating from single mycorrhizal rootlets can connect lovskaia et al., 2019; Fig. 5). However, global maps of ORC and ERM
distant neighboring plants. In addition, most ECM genets exist as fungi, as well as ‘mycorrhizal’ Mucoromycota fine-root endophytes,
autonomous entities because of the presence of vegetative incompat- are still lacking. Furthermore, maps documenting the world-wide
ibility loci that prevent the fusion of individuals that differ genetically distribution of mycorrhiza-associated microbes, such as mycorrhiza-
at the heterokaryon incompatibility (het) loci, that is, anastomosis helper bacteria, fungi, and protists, are required to fully understand
between incompatible genotypes triggers cell death (Paoletti, 2016). the breadth of mycorrhizal systems (Frey-Klett et al., 2007; Emmett

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Fig. 5 Global map of the percentage of total aboveground plant biomass linked to the different mycorrhizal categories. (a) arbuscular mycorrhizal plants; (b)
ectomycorrhizal plants; (c) nonmycorrhizal plants. Map resolution was 10 arcmin. Published by Soudzilovskaia et al. (2019).

et al., 2021; Yang et al., 2023; Zhang et al., 2023). Identifying the
EM AM NM

Relative importance of mycorrhizas

genetic diversity of these mycorrhiza-associated microorganisms and
analyzing their spatiotemporal dynamics is crucial, as emerging
studies have suggested their involvement in nutrient uptake

for plant productivity

Forests
facilitation and other services provided by mycorrhizal hyphae
(Zhang et al., 2022; Li et al., 2023; Wang et al., 2023a,b). The ability
of mycorrhizal fungi to acquire nutrients appears to be influenced by Grasslands
the composition of the bacteria associated with mycorrhizal hyphae.
For instance, Zhang et al. (2023) demonstrated that common AM
hyphal-associated bacteria promote plant growth and mycorrhizal Arable
formation. The concept of ‘mycorrhiza suppressive soil’ has been lands
proposed for soils where microbial communities impede the nutrient
uptake facilitated by mycorrhizal hyphae (Svenningsen et al., 2018). Disturbance
Variations in hyphae-associated microbial communities may con-
tribute to the challenges encountered when replicating mycorrhizal Fig. 6 Relative importance of mycorrhizal associations for plant productivity
experiments. Recent studies have demonstrated that protists feeding and ecosystem performance in different ecosystem types. forests,
on hyphae-associated bacteria can affect mycorrhizal nutrient uptake, grasslands, and arable ecosystems. Different ecosystem types are dominated
thereby highlighting the intricate nature of these multitrophic by different mycorrhizal associations. AM, arbuscular mycorrhizas; EM,
ectomycorrhizas; NM, nonmycorrhizal.
interactions (Rozmos et al., 2022). Additionally, it has been suggested
that AMF harbor an ancient lineage of mycoviruses (Ezawa
et al., 2023), and a recent study suggested a recent and single importance compared with other essential microbial groups,
infection of a large dsDNA viral genome in the genome of an AM including bacteria, endophytic and saprotrophic fungi, protists,
fungal strain (Zhao et al., 2023). However, the role of viruses in archaea, viruses, and soil micro- and mesofauna, as well as their
regulating mycorrhizal function, including their effect on the genetic interactions. The relative importance of mycorrhizas for plant
structure of the mycorrhizal mycobiome, remains poorly understood productivity and ecosystem performance depends on the ecosystem
and requires further investigation. Overall, these studies emphasize type (Fig. 6). We propose that mycorrhizal associations, including
the need to consider the ‘holobiont’ concept when trying to mycorrhizal helper bacteria, play a paramount role in forests,
understand mycorrhizal functioning (Vandenkoornhuyse followed by grasslands and arable land (Fig. 6). This contention is
et al., 2015; Wang et al., 2023b). supported by observations that ECM fungi are responsible for a
substantial part of N acquisition in many forests, especially in
nutrient-poor soils (Hobbie & Hobbie, 2006). Recent studies have
V. Mycorrhizal symbiosis in ecosystems
revealed a strong correlation among tree productivity, ECM
composition, and beta diversity (Anthony et al., 2022; S. Luo
1. Determining the relative importance of mycorrhizas
et al., 2023), further reinforcing this observation. However, it is
Numerous studies have emphasized the significance of mycorrhizal crucial to acknowledge that the significance of mycorrhizal
fungi in promoting plant growth and ecosystem functioning. associations depends on nutrient availability, and their importance
However, there is a lack of research that clearly defines their relative diminishes in nutrient-rich soils. The effects also depend on plant

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species identity, as some plants, such as a wide range of members of experimental forest site with the sequencing of soil eukaryotic RNA
Brassicaceae or Proteaceae, do not engage in associations with extracts, the precise gene expression of each mycelial network
mycorrhizal fungi. extending beneath a tree species can be evaluated (Auer et al., 2023;
In grasslands, mycorrhizal associations exhibit greater varia- Zeng et al., 2023). The use of metatranscriptomics will also help
bility. AMF, the dominant mycorrhizal fungi in grasslands, have an decipher the relative importance of each fungal species within the
important impact on grassland functioning by altering competitive different soil biota in measuring genes involved in plant nutrition,
interactions among plant species, leading to either increased or C cycling, disease resistance, and stress adaptation.
decreased plant diversity (van der Heijden et al., 1998; Hartnett
et al., 1999). However, the relative importance of mycorrhizas for
VI. Mycorrhizal symbiosis and plant community
biomass production in grasslands is lower, as biomass production
dynamics
often remains similar with or without mycorrhizas, signifying
changes in plant species composition (van der Heijden et al., 1998; It is increasingly recognized that soil microbes, including
Hartnett et al., 1999). In arable and highly disturbed systems, mycorrhizal fungi, can mediate plant interactions and thus may
mycorrhizal symbiosis is expected to have the lowest relative contribute to biodiversity-productivity relationships, shaping plant
importance. These systems usually have a lower abundance or an communities (Klironomos, 2002; Van der Heijden et al., 2008;
absence of mycorrhizal associations, whereas fungal and bacterial Schnitzer et al., 2011). Manipulative experiments targeting the
pathogens are more abundant (Labouyrie et al., 2023). Non- abundance and presence of AMF and ECM have consistently
mycorrhizal and ruderal plant species often dominate these systems demonstrated their profound effects on plant diversity and
(Read, 1991). Nonetheless, it is crucial to acknowledge that co- community structure (Liang et al., 2019). Notably, the paucity of
occurring plant species within the same ecosystem may exhibit studies that manipulate other types of mycorrhizal symbioses, such
different mycorrhizal responsiveness, and that some plant species as ERM and ORM, to investigate their effects on plant growth and
and crops in arable fields benefit from mycorrhizal symbiosis. establishment warrants further investigation and research atten-
Moreover, exceptions have been observed, such as plant species in tion. It is worth noting that the majority of studies in this field are
extremely weathered and nutrient-poor soils in Australia, which relatively short-term, typically spanning < 1 yr. Therefore, there is a
have cluster roots and do not form associations with mycorrhizal pressing need for long-term investigations to provide deeper
fungi (Lambers et al., 2008). Notably, nonmycorrhizal plants are insights into the role of mycorrhizal associations in plant
not always restricted to low-nutrient soils; for example, Proteaceae communities. This necessity is particularly critical for perennial
are present throughout most of the Southern Hemisphere. In brief, plant communities, which represent the predominant vegetation
the relative importance of mycorrhizal symbiosis in ecosystems type on Earth, including grasslands, savannahs, and forests.
fluctuates depending on the specific ecosystem type, nutrient An increasing body of evidence from global surveys has
availability, and plant species composition. It is important to highlighted the significance of mycorrhizal associations in shaping
acknowledge the current geographical bias in mycorrhizal research, plant community structure, diversity, and productivity. Large-scale
which predominantly focuses on temperate and boreal regions and forest inventories have provided valuable insights into the role of
potentially overlooks the greater diversity of viable mycorrhizal mycorrhizal types in structuring forest ecosystems and tree
and nonmycorrhizal strategies in subtropical and tropical ecosystems. diversity. Carteron et al. (2022), for instance, conducted an
Addressing this gap is essential for obtaining a more comprehensive analysis of 82 000 forest plots across the United States and found
understanding of mycorrhizal associations world-wide. Additionally, that forests dominated by ECM fungi or AMF tend to exhibit lower
there is a trend toward overinterpreting data, which can hinder tree diversity. By contrast, forests with a mixture of mycorrhizal
progress in certain research fields (Kuyper & Jansa, 2023). strategies supported a higher number of tree species. More recently,
Y. H. Luo et al. (2023), using the same database, demonstrated that
mixed mycorrhizal plots displayed greater productivity than plots
2. Linking genes to ecological traits
in which either AMF- or ECM-associated tree species were
The growing availability of mycorrhizal fungal genomes (Lebreton dominant. These findings suggest that the coexistence of both
et al., 2021) presents unprecedented opportunities to investigate mycorrhizal types can complement each other and enhance
the functional diversity of soil fungal communities. This can be ecosystem function. Additionally, the positive effects of mixed
achieved through expert and accurate annotation of environmental mycorrhizal strategies on forest productivity were more pro-
metabarcoding (Anthony et al., 2022), metagenomics (Hagh- nounced in plots with lower tree species richness (Y. H. Luo
Doust et al., 2023), and metatranscriptomic (Auer et al., 2023; et al., 2023). However, the mycorrhizal type of the dominant plant
Zeng et al., 2023) datasets. The latter approach has been used to species also plays a crucial role in facilitating or suppressing
examine gene expression in ECM root tips in natural environ- subordinate or understory species. For example, a study conducted
ments, including the effects of anthropogenic N deposition on in the Great Smoky Mountains of the United States found a
ECM tree metabolism (Liao et al., 2018; Law et al., 2022; Rivera positive relationship between herb species richness and the number
P
erez et al., 2022). Anthony et al. (2022) showed that tree growth of AM tree species (Newman & Reddell, 1988). Deng et al. (2023)
was linked to the gene copy number of genes involved N uptake and conducted a large-scale tree biodiversity experiment in China and
assimilation in associated ECM symbionts. By combining high- observed that the relationship between tree species richness
throughput metabarcoding of fungal species residing in a specific and productivity is dependent on the mycorrhizal type. Specifically,

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a positive relationship was observed between the richness of AM nonnative inoculum, which may pose a threat to soil and plant
trees and productivity, whereas no such relationship was observed biodiversity and ecosystem functioning (Hart et al., 2018). Before
for ECM trees. By contrast, S. Luo et al. (2023) showed a positive introducing an inoculant to the market, it is crucial to adhere to a
relationship between mycorrhizal diversity and aboveground range of basic quality criteria in order to assess inoculum viability
productivity in a subtropical evergreen broad-leaved forest and efficacy under controlled conditions (Salomon et al., 2022).
ecosystem. Metatranscriptomics and metaproteomics approaches Additionally, tools need to be developed to enable farmers or
can help identify the mechanisms and key gene networks involved foresters to predict under which conditions (crop type, crop
in mediating the observed biodiversity-ecosystem functioning genotype, soil type, nutrient availability, and weather conditions)
relationships. Moreover, the presence or absence of mycorrhizal inoculation is beneficial and economically viable. For example, a
symbionts can facilitate or impair the establishment of invasive recent field inoculation study in 54 well-fertilized arable soils in
species (e.g. Pringle et al., 2009; Dickie et al., 2010). Switzerland found that the success rate of AMF inoculation was
best predicted by the presence of fungal pathogen genes in the soil,
suggesting that inoculation can also help reduce biotic stress (Lutz
VII. Mycorrhiza applications
et al., 2023). Overall, mycorrhizal fungi have a great potential as
There is considerable interest in enhancing agricultural sustain- biological agents for sustainable production. However, it is
ability and utilizing biological approaches to promote crop plant essential to elucidate the specific conditions under which
yield, as well as facilitate ecosystem restoration and sustainability. inoculation is most effective. A combination of high-throughput
Mycorrhizal fungi have important potential as they are known to rDNA metabarcoding, RNA sequencing, and metaproteomics
promote plant growth and provide protection against biotic and would be a powerful approach to assess mycorrhizal inoculation
abiotic stresses in agriculture and forestry. A recent meta-analysis by success and to reveal whether field inoculation enhances specific
Averill et al. (2022) indicated that restoring the native soil ecosystem functions. For instance, the level of transcripts (or
microbiome could lead to an average acceleration of 64% in plant proteins) coding for nutrient transporters (or other functional traits
biomass production across various ecosystems. However, the that can be traced back to mycorrhizal fungi) can be linked to
responsiveness of plants to mycorrhizal inoculation can be highly particular ecosystem functions, such as plant yield, nutrient
dependent on the experimental conditions, nutrient availability, content, SOM decomposition, or disease/stress resistance. Multi-
and the specific plant species being studied (Lekberg & omics approaches can also help to reveal the relative importance of
Koide, 2005; Hoeksema et al., 2010; Chaudhary et al., 2016). mycorrhizal traits in comparison with other traits (e.g. nutrient
Too often, the literature presents an overly optimistic view of the uptake by plant roots or organic matter decomposition by
importance of AMF in crop yield (for a discussion, see Ryan & nonmycorrhizal soil biota). Such studies will rely on a combination
Graham, 2018; Rillig et al., 2019a,b). Additionally, results can vary of traditional ecology/agronomy approaches (e.g. assessing plant
based on plant genotypes (An et al., 2010) and crop domestication yield, decomposition with litter or tea bags, disease suppression
status (Mart
ın-Robles et al., 2018). For example, a recent study assays, hyphal compartments only accessible to fungal hyphae, or
comparing 99 wheat lines demonstrated a wide range of growth the inclusion of organic nutrient patches) and environmental
responses to inoculation, varying from 30% decrease to 80% genomics approaches. For instance, Liu et al. (2023) revealed that
increase in shoot biomass (Thirkell et al., 2022). This highlights the the application of pesticides is linked to genes responsible for N
importance of carefully considering the plant genotype, AMF fixation, iron transport, and P metabolism, enabling the elucida-
species, genotypes, and likely nuclear organization (heterokaryons tion of how environmental stressors can influence soil functioning.
vs homokaryons) when attempting to promote agricultural yield However, the analytical methodology required to integrate
through mycorrhizal inoculation. ecology/agronomy approaches with genomics, transcriptomics,
Many studies evaluating plant growth responses to mycorrhizal proteomics, metabolomics, and phenomics data remains nascent.
inoculation have been conducted under highly controlled condi- Owing to their nature, -omics data are intrinsically highly variable
tions in glasshouses, often using sterilized and nutrient-poor soils. and noisy, leading to several issues when trying to compare or
Comparing the results of such studies to field conditions can be reproduce them in natural settings. Integrating multi-omic data
challenging. To make field inoculation practical and widely will likely rely on co-expression or co-abundance network
adopted, it is essential to conduct field inoculation trials and approaches, such as those developed in random forest-based
employ appropriate inoculation techniques that can easily be methods (Huynh-Thu et al., 2010). In this approach, multiple
implemented by farmers or foresters. Mycorrhizal fungi can types of -omics and ecological data can be integrated by identifying
be coated onto seeds, applied as dressing or as ‘fertilizer’ grains, or proteins and transcripts that shift their abundance in a coordinated
sown together with (or below) seeds (Vos
atka et al., 2012; Oliveira manner across a range of experimental conditions (e.g. crop yield)
et al., 2019; Rocha et al., 2019). The addition of natural soils or samples.
containing indigenous populations of mycorrhizal fungi (and other
microbes) to neighboring sites or tree nurseries has also been
VIII. Future directions
advocated, as these inoculants may be better adapted to local
conditions. Furthermore, field inoculation can change native AMF By applying genomics and other -omics approaches to the study of
communities (Basiru & Hijri, 2022), and there are concerns mycorrhizal symbioses, we gained deeper insight into the
regarding the potential unintended consequences of using a molecular, physiological, and ecological processes underlying these

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mutualistic associations. This knowledge should be translated into

practical applications that promote ecosystem functioning and Box 1. Topical questions in the genomics of mycorrhizal associations.
conservation, contribute to the overall mitigation of climate What are the genomic mechanisms underlying the specificity and
change, and ensure sustainable arable land. Numerous long-term recognition of plant hosts and mycorrhizal fungi and how do these
challenges remain in leveraging genomics and other -omics tools to mechanisms contribute to the establishment and maintenance of
deepen our understanding of mycorrhizal symbioses, including symbiosis?
their evolution, development, function, and ecology (Table 1). How do idiosyncrasies in the gene repertoire of mycorrhizal fungi
influence their ability to interact with different plant species, and what
are the implications for plant diversity and ecosystem functioning?
1. Expanding the repertoire of mycorrhizal genomes How does genomics inform our understanding of the complex
regulatory networks involved in mycorrhizal symbiosis, including the
The current collection of sequenced mycorrhizal genomes genes and pathways responsible for signaling, nutrient transport, and
represents only a fraction (c. 0.4%) of the estimated 50 000 establishment of mutualism?
mycorrhizal fungal species identified. To capture the true genetic What is the genomic basis of the response of mycorrhizal fungi to
and functional diversity of this fungal guild, it is crucial to sequence environmental stressors, such as changes in soil pH, drought,
additional genomes using novel sequencing initiatives, such as the pesticides, plastics, nutrient availability, and climate fluctuations, and
how does this affect their symbiotic interactions with plants?
JGI 10 000 Fungal Genomes project, Darwin Tree of Life, or Earth
How can genomics contribute to the understanding of the evolution of
Microbiome. Exploring the genomes of mycorrhizal species from mycorrhizal symbiosis and the genetic changes that have occurred over
understudied ecosystems, such as the Arctic, montane, desert, and time, leading to a diverse range of mycorrhizal associations observed in
tropical biomes, could reveal specific gene sets associated with nature?
adaptation to these environments. Additionally, investigating the What are genomics-based strategies for engineering or enhancing
genomic blueprints of poorly explored early diverging mycorrhizal mycorrhizal symbiosis in crops to improve nutrient uptake efficiency,
lineages, fine-root Mucoromycotina endophytes, bryophytes- stress tolerance, and overall plant performance?
associated mutualists, and mycorrhiza-like endophytic fungi can What is the role of epigenetic modifications in mediating plant-
mycorrhizal fungus interactions, and how do epigenetic changes
shed light on the functional capabilities and transition from influence the outcomes of the symbiotic relationship?
saprotrophism to mutualism in these fungal groups. Can comparative genomics shed light on the genetic basis of functional
differences among various mycorrhizal fungal species and how can this
knowledge be applied to optimize fungal partners for specific
2. Advancing our understanding of basic biological processes agricultural or ecological goals?
Utilizing approaches such as multiplexed single-cell and 3D spatial How can genomics, metatranscriptomics, and metaproteomics con-
gene expression analysis of mycorrhizal roots, transcriptomic-based tribute to our understanding of the role of mycorrhizal fungi in carbon
cycling, soil health, and overall ecosystem services and how might this
co-expression analysis, proteomics, and protein–protein interac- knowledge inform environmental management strategies?
tion studies can aid in linking genes to established biological
processes and potentially predict evolutionary relationships as well
as ecological adaptation (see Box 1). Approaches involving high-
throughput protein-folding computations (e.g. AlphaFold; Jumper our planet that remain largely underexplored. A consensus has
et al., 2021) can help identify protein structures encoded by emerged that most of this diversity, both known and unknown,
symbiosis-regulated genes with unknown functions, such as resides in the tropics. The mycobiome diversity in deserts and polar
effector-like secreted proteins (Teulet et al., 2023). Understanding regions remains uncharacterized, but their populations are
the origin of these effector proteins is crucial, whether they evolved changing rapidly, driven by anthropogenic climate change
from saprotrophic ancestors or emerged anew to facilitate (Baldrian et al., 2023). We urge researchers to examine the
colonization within plant tissues. Addressing the signaling path- biogeography of various mycorrhizal associations within these
ways and specific molecules involved in symbiotic development and biomes. Other threats to soil habitats, such as microplastics, can
the intricate molecular crosstalk between mycorrhizal partners are also alter or even create new habitats for mycorrhizal fungi (Leifheit
needed. Currently, the master genes that trigger the development of et al., 2021). Owing to initiatives such as the Society for the
ectomycorrhizal symbiosis in both fungal and plant partners (if Protection of Underground Networks, a better understanding of
any) are unknown. Furthermore, it is important to investigate the these mycorrhizal mycobiomes would allow us to improve
factors underlying the varying host ranges of different mycorrhizal predictions of anthropogenic impacts on microbiome composi-
species (Lebreton et al., 2021; Tang et al., 2021). Why certain tion, resilience, evolution, and productivity (Averill et al., 2022;
mycorrhizal fungal species can colonize a wide range of hosts, Baldrian et al., 2023) (Box 1). The global inventory of mycorrhizal
whereas others exhibit more restricted preferences, remains an fungi, such as GlobalFungi (Vetrovsk
y et al., 2020), must be
intriguing aspect that requires further exploration. accompanied by an atlas designed to explore microbial functions in
space and time (to be described later). Given the increasing number
of threats to the soil environment, there is an urgent need to
3. Unearthing mycorrhizal diversity
characterize healthy soil microbiomes in ecosystems that are
Although progress has been made, especially in temperate and currently unaffected by environmental threats (if any). This
boreal ecosystems (Peay et al., 2016), there are still vast regions of provides a baseline for understanding how these microbial

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Phytologist Tansley review Review 1499

communities might respond to global changes. It would also help to various components of forest or grassland plots. These integrated
identify tipping points that could permanently change the approaches will offer valuable insights into the functioning of
composition and function of the soil microbiome. For instance, fungal/plant communities. The adoption of this genome-to-
large-scale inventories of European forests have shown that N ecosystem strategy will be crucial in unraveling the contributions
deposition causes tipping points in mycorrhizal composition and of fungal guilds that thrive in the soil and roots within intricate
functioning (van der Linde et al., 2018). Although hundreds of terrestrial ecosystems (Box 1).
studies have described the composition of the mycorrhizal
mycobiome in various ecosystems, little is known about the
5. Promoting sustainable agriculture and forestry
connectivity between different components and mycorrhizal
community shifts during succession and along the gradient of Gaining insights into the genetic basis of beneficial traits in
grassland-, shrub-, and tree-dominated zones. mycorrhizal fungal populations and communities is crucial for the
development of strategies aimed at optimizing their use as
biofertilizers or biocontrol agents, thereby reducing reliance on
4. Environmental genomics
chemical inputs and promoting sustainable land management
Understanding the processes driving variations in natural microbial practices. To achieve sustainable agriculture and forestry, it is
communities across space and time is a critical challenge for imperative to harness the potential of mycorrhizal symbioses and
ecologists. With an increasing number of available fungal genomes exploit the functional traits of the mycorrhizal inoculants. To
from ecologically relevant species (see Section II), it is now possible successfully manage mycorrhizal fungal communities and promote
to map anonymous DNA and RNA reads from soil and ecologically sustainable agriculture or restoration initiatives, it is
mycorrhizal roots to identify mycorrhizal species and their specific crucial to identify the range of fungal taxa present and the factors
gene expression patterns, including targeting the mycorrhizal genes that influence their diversity and distribution at both regional and
responsible for nutrient uptake, symbiosis development and continental levels. DNA metabarcoding surveys can foster applica-
signaling, and SOM decomposition. However, metagenomic tions and predict under which conditions inoculation is beneficial
approaches are still challenging for assembling entire fungal for farmers and land managers (e.g. low abundance or diversity of
genomes from soil samples because they usually represent a very mycorrhizal fungi) (Box 1). These genotyping approaches can also
low proportion of soil DNA. Higher-throughput sequencing can identify whether specific crop microbiomes are characteristic of
help address the depth-of-coverage issue, but this can lead to other well-performing (high-yield and high nutrient use efficiency)
problems related to the high computational demands for large systems to distinguish them (functionally) from poorly performing
datasets. By contrast, using RNA profiling of soil hyphae and (low-yield and large nutrient losses) systems. Moreover, such tools
mycorrhizal root tips, we can now assess whether multiple can be used to identify how mycorrhizal inoculation can alleviate
symbiotic species can coexist on (or beneath) the same host tree biotic stress (e.g. high pathogen abundance). Furthermore,
by utilizing the same resources and performing identical ecological metatranscriptomics, metagenomics, and stable isotope probing
functions (i.e. exhibiting high functional similarity) or by utilizing may provide functional insights into and identify the role of
different resources and providing distinct functions (i.e. exhibiting mycorrhizal helper bacteria and other microbial consortia that
limited functional similarity; see Section V.2). Metatranscrip- contribute to plant growth. Mycorrhizal fungi can also facilitate the
tomics of soil fungal communities (Auer et al., 2023; Zeng establishment and growth of plants in degraded habitats. However,
et al., 2023) can be used to better understand the role of mycorrhizal it is necessary to investigate the specific conditions under which the
networks, including CMN, because they can help identify whether application of mycorrhizal fungi is beneficial, the compatible host
different tree individuals within a plot are truly colonized by the plants (or even genotypes), and whether specific taxa of mycorrhizal
same fungus, and whether the same sets of genes are expressed in fungi can be applied alone or in microbial consortia, along with
different tree individuals. However, several challenges limit the other microorganisms such as mycorrhiza-helper bacteria and
widespread application of metatranscriptomics, including the protists, or using a complex field inoculum (Allsup et al., 2023).
lower stability of RNA compared with that of DNA, greater Similar to the human microbiome, there is an important potential
difficulty in extracting RNA, and difficulty in obtaining informa- for microbiome engineering (Silverstein et al., 2023). Many
tive messenger RNA transcripts that provide insights into its commercially available mycorrhizal products are either nonviable
functional role (Auer et al., 2023). It is difficult to ascertain whether or ineffective (Salomon et al., 2022), and it is often overlooked
nuclei, transcripts, proteins, and metabolites can translocate from whether the fungi present in these commercial inoculants have been
one plant to another through CMNs in natural settings. The successfully established in the field. Therefore, it is essential to DNA
absence of imaging tools that can trace and investigate individual barcode the inoculum, trace the establishment and survival of
hyphae within intermingled mycelial networks in soil presents a mycorrhizal fungal isolate(s) in the field, and determine the
significant obstacle in understanding this phenomenon. Never- economic and ecological feasibility of their application.
theless, ongoing research is developing integrated methods that
combine rDNA metabarcoding to evaluate the distribution of
6. Promoting C sequestration and climate resilience
operational taxonomic units, estimate fungal genotype size through
multi-locus eDNA population genomics, metatranscriptomics, Mycorrhizal symbioses have the potential to contribute to climate
metaproteomics, and measurement of metabolic fluxes between change mitigation by promoting C sequestration and cycling in soil

Ó 2024 The Authors New Phytologist (2024) 242: 1486–1506

New Phytologist Ó 2024 New Phytologist Foundation www.newphytologist.com
 New
1500 Review Tansley review Phytologist

(Hawkins et al., 2023). Mycorrhizal networks contribute to c. 20– networks (Fig. 4). FMM was funded by the Laboratory of Excellence
30% of the microbial biomass present in soils (Leake et al., 2004), ARBRE (ANR-12-LABX-ARBRE-01), the U.S. Department of
representing substantial soil C storage. C fluxes through mycor- Energy JGI (Office of Science of the US Department of Energy under
rhizal mycelia are high, and C can be immobilized in both mycelia Contract No. DE-AC02-05CH11231), the Beijing Advanced
and secretions on both organic and mineral substrates for long Innovation Center for Tree Breeding by Molecular Design (Beijing
periods (Finlay & Clemmensen, 2017). Metabarcoding surveys Forestry University), and Huazhong Agricultural University. MvdH
coupled with genomic/transcriptomic studies can help to identify acknowledges funding from the Swiss National Science Foundation
fungal species and genetic traits associated with high C sequestra- (grants 310030_188799 and 40IN40_215832) and the Gebert R€ uf
tion potential (Plett et al., 2021) (Box 1). A recent study Foundation.
demonstrated that mycorrhizal interactions might be a driver of
alternative stable states and tipping points in tundra ecosystems.
These regions are typically dominated by ERM associations that are Competing interests
associated with SOM accumulation and slow decomposition. None declared.
However, tree encroachment can lead to an abrupt decrease in
belowground SOM linked to the abundance of ECM trees that
contribute to SOM decomposition while scavenging N (Clem- ORCID
mensen et al., 2021). In dry ecosystems, additional drought and
reduced rainfall can reduce the abundance of ECM fungi, leading Marcel G. A. van der Heijden https://orcid.org/0000-0001-
to increase abundance of saprotrophic fungi and enhanced SOM 7040-1924
decomposition (Querejeta et al., 2021). Furthermore, mineral Francis M. Martin https://orcid.org/0000-0002-4737-3715
weathering in deeper soil horizons and mycelial biomass depends
on SOM abundance and nutrient availability (Mahmood References
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