# Unearthing the plant-microbe quid pro quo in root associations with beneficial fungi

Juliana Almario, Izabela Fabiańska, Georgios Saridis, Marcel Bucher

<figure><img src="image_1.png" /></figure>

## To cite this version:

Juliana Almario, Izabela Fabiańska, Georgios Saridis, Marcel Bucher. Unearthing the plant-microbe quid pro quo in root associations with beneficial fungi. New Phytologist, 2022, Early Access, 10.1111/nph.18061. hal-03639657

HAL Id: hal-03639657

https://hal.inrae.fr/hal-03639657

Submitted on 13 Apr 2022

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_2.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
<figure><img src="image_3.png" /></figure>

<figure><img src="image_4.png" /></figure>

Research review

# Unearthing the plant–microbe *quid pro quo* in root associations with beneficial fungi

Authors for correspondence:

Juliana Almario

Email: juliana.almario@univ-lyon1.fr

Marcel Bucher

Email: m.bucher@uni-koeln.de

Received: 7 September 2021

Accepted: 9 February 2022

Juliana Almario¹ ID, Izabela Fabiańska², Georgios Saridis² ID and Marcel Bucher²,³ ID

¹Ecologie Microbienne, CNRS UMR-5557, INRAe UMR-1418, VetAgroSup, Université de Lyon, Université Claude Bernard Lyon1, 43 Boulevard du 11 novembre 1918, Villeurbanne 69622, France; ²Institute for Plant Sciences, Cologne Biocenter, University of Cologne, Cologne 50674, Germany; ³Cluster of Excellence on Plant Sciences (CEPLAS), University of Cologne, Cologne 50931, Germany

## Summary

Mutualistic symbiotic associations between multicellular eukaryotes and their microbiota are driven by the exchange of nutrients in a *quid pro quo* manner. In the widespread arbuscular mycorrhizal (AM) symbiosis involving plant roots and Glomeromycotina fungi, the mycobiont is supplied with carbon through photosynthesis, which in return supplies the host plant with essential minerals such as phosphorus (P). Most terrestrial plants are largely dependent on AM fungi for nutrients, which raises the question of how plants that are unable to form a functional AM sustain their P nutrition. AM nonhost plants can form alternative, evolutionarily younger, mycorrhizal associations such as the ectomycorrhiza, ericoid and orchid mycorrhiza. However, it is unclear how plants such as the Brassicaceae species *Arabidopsis thaliana*, which do not form known mycorrhizal symbioses, have adapted to the loss of these essential mycorrhizal traits. Isotope tracing experiments with root-colonizing fungi have revealed the existence of new 'mycorrhizal-like' fungi capable of transferring nutrients such as nitrogen (N) and P to plants, including Brassicaceae. Here, we provide an overview of the biology of trophic relationships between roots and fungi and how these associations might support plant adaptation to climate change.

New Phytologist (2022)

doi: 10.1111/nph.18061

**Key words:** mycorrhiza, mycorrhizal-like fungi, nitrogen, nutrient exchange, phosphorus, symbiosis.

## Quid pro quo principle in mutualistic host–microbe interactions

Mutualistic symbioses, as defined by the German botanist and mycologist Heinrich Anton de Bary in 1878 (Oulhen et al., 2016), are interactions between organisms in which there is a reciprocal benefit for the symbionts. This type of interspecies interaction is present among many life forms and is a key factor that drives the functionality and evolution of natural ecosystems. In the case of mutualistic symbioses between microorganisms and multicellular eukaryotes, they are primarily associated with a nutritional trade between the partners in a *quid pro quo* ('giving and taking') manner.

In mutualism, both partners must constantly regulate the symbiotic association in order to maintain the highest gain relative to their own investment. From an evolutionary point of view, the ability of the symbionts to coordinate the flow of resources according to their partner's input determines the sustainability of

the mutualistic symbiosis. The oldest and probably most widespread mutualistic symbiosis world-wide is the arbuscular mycorrhizal (AM) symbiosis (Karandashov & Bucher, 2005). It is an ancient mutualistic partnership based on the principle of reciprocity between host and symbiont, which was probably crucial for symbiosis stabilization during evolution.

It is hypothesized that in the AM symbiosis, both partners can equally control their contributions to the symbiosis, depending on what the other provides, but there is obviously some danger of anthropomorphic interpretation when describing these '*quid pro quo*' mechanisms. The 'biological market theory' underlying these premises assumes that individuals prefer interactions with partners that provide more nutrients (Kiers et al., 2016). To this end, plants specifically direct the increased carbon (C) flux to the fungus that has the highest benefit, *that is* the highest phosphorus (P) supply. Accordingly, the AM fungus rewards the plant that is able to supply the most C with an increased P flux (Kiers et al., 2011). In support
of this concept, it has also been shown that when plant C flux is low, the fungus can confiscate P, which then accumulates in the fungal hyphae (Kiers et al., 2011), or is diverted to nutrient-poor patches where the host's resource requirements are higher (Whiteside et al., 2019).

The biological market theory should allow scientists to make testable predictions about resource allocation patterns and under-
lying molecular mechanisms in mutualistic symbioses and how
they vary across time, species, genotypes and environmental scales.
Despite convincing experimental support, this theory was recently
challenged in two studies on the effect of elevated CO2 and aphid
herbivory on the bidirectional exchange of C and P in the AM
symbiosis of wheat. While elevated CO2 and aphids significantly
reduced C transfer from host to mycobiont, P transfer from the
fungus to the host plant remained largely unaffected (Charters
et al., 2020). In older work using different experimental settings,
the terms of trade between different hosts with arbuscular
mycorrhizal fungi (AMF) did not conform to the biological market
theory, thus questioning the broad applicability of this theory (van
der Heijden & Walder, 2016) (and references therein). In
summary, a widely applicable theory to explain resource exchange
in mutualistic symbioses, including and beyond the AM symbiosis,
and an underlying genetic framework are still needed to understand
how mutualistic symbioses actually work.

Mycorrhizal symbioses in AM nonhost lineages

Are AM symbiosis principles applicable to other growth-promoting plant-fungal interactions? Mycorrhizal evolution gave rise to AM in early land plants; however, there is good evidence that mycorrhizal associations with Mucoromycotina fungi, a sister lineage to the Glomeromycotina fungi, also facilitated colonization of Earth's land by plants (Field et al., 2019), maybe even pre-dating the AM symbiosis (Field & Pressel, 2018). In AM nonhost liverworts from the Haplomitriopsida (Haplomitrium and Treubia; the earliest diverging land plants), the Mucoromycotinal mycorrhizal symbiosis seems to have been selected over the AM symbiosis as the sole mycorrhizal association in these plants (Field & Pressel, 2018) (Fig. 1a). Since its emergence, the AM symbiosis has been subjected to evolutionary selection in plant lineages, which are now AM hosts, and has been abandoned in AM nonhost lineages, which either became nutritional specialists (e.g. carnivorous plants), developed new root-fungus mycorrhizal symbioses including intracellular associations (orchid and ericoid mycorrhiza) and extracellular associations (e.g. ectomycorrhiza, in short ECM), or remained 'non-mycorrhizal' lineages, that is not establishing any plant-fungus symbiosis that we know of (e.g. Brassicaceae) (Brundrett & Tedersoo, 2018; Werner et al., 2018) (Fig. 1a). With the exception of orchid mycorrhiza, all these associations, such as the AM symbiosis, are based on a nutritional *quid pro quo*. Transport of nutrients from one partner to the other has been evidenced by the tracing of isotopes (e.g. ³³P, ³²P, ¹⁴C, ¹³C and ¹⁵N), in compartmentalized experimental systems, which allow the separation of a 'root compartment' from a 'fungal compartment', connected only by fungal hyphae (Pearson & Jakobsen, 1993). In the Mucoromycotinal mycorrhizal symbiosis of Haplomitriopsida liverworts,

Mucoromycotina fungi provide nitrogen (N) and P to the plant in exchange for C (Field *et al.*, 2015). In the ECM symbiosis with Basidiomycota fungi and pines, fungi provide P (Becquer *et al.*, 2018) and N (Finlay *et al.*, 1988) to the plant in exchange for plant C (Wu *et al.*, 2001). In the case of the orchid mycorrhizal symbiosis, orchids from the family Orchidaceae appear to use Basidiomycota fungi for obtaining C (Bougoure *et al.*, 2014), N (Cameron *et al.*, 2006) and P (Cameron *et al.*, 2007) for seedling development or for heterotrophic growth, in the case of nonphotosynthetic orchids. The ericoid mycorrhizal symbiosis is only observed in Ericaceae plants, and mutual exchange of C and P has been demonstrated in Basidiomycota fungi of the genus *Clavaria* and Rhododendron plants (Englander & Hull, 1980). In addition to this nutritional *quid pro quo*, these mycorrhizal associations have in common the formation of specific fungal-plant interfaces within host roots, that is intracellular arbuscules or arbuscule-like structures (AM and Mucoromycotina mycorrhiza), intracellular pelotons (orchid mycorrhiza), intracellular coils (ericoid mycorrhiza) and the intercellular Hartig net formed in ectomycorrhiza (Werner *et al.*, 2018; Genre *et al.*, 2020) (Fig. 1a).

Adaptive gene selection is the driving factor that, from an evolutionary perspective, leads to the emergence and maintenance of a plant's ability to harbour a successful AM symbiosis. Interestingly, all plant genes essential for AM symbiosis are not systematically absent or were lost in all AM nonhost lineages. In orchid and ericoid mycorrhiza, genes involved in presymbiotic communication and intracellular fungal accommodation are retained, while genes involved in nutrient exchange seem to have been lost (Fig. 1b) (Radhakrishnan et al., 2020). This suggests that in these mycorrhizal associations, intracellular fungal colonization of root cells relies on communication and infection mechanisms co-opted from the AM symbiosis pathway. In the case of ECM and in nonmycorrhizal plant lineages such as Brassicaceae, most genes that are essential in the AM symbiosis have been lost, except for genes involved in strigolactones biosynthesis (D27, CCD7 and CCD8) (Radhakrishnan et al., 2020) and in the regulation of symbiotic nutrient exchange (CBX1) (Fig. 1b). Thus, these symbiotic functions could play an important role in the ECM and in mutualistic mycorrhizal-like associations.

Mycorrhiza-like associations

The transfer of nutrients from fungal cells to plant roots was thought to be limited to the mycorrhizal associations mentioned above, but recent research suggests otherwise. Indeed, since the discovery of ‘mycorrhizal-like’ fine root endophytes from the Mucoromycotina (for a review, see Sinanaj *et al.*, 2021), other endophytic fungi from other lineages have been discovered to form mycorrhiza-like associations. Several studies have independently demonstrated N, P, S and iron (Fe) transfers from ‘mycorrhizal-like’ endophytic fungi to plants, using isotope tracking experiments in compartmentalized systems similar to those used in mycorrhizal research. Such exchanges have been evidenced in a variety of plants with diverse root-colonizing fungi not previously known to form mycorrhizal associations. In these associations, the fungi are capable of intracellular colonization of plant roots and nutrient
<figure><img src="image_5.png" /><figcaption>(b) AM symbiotic genes</figcaption></figure>

<table><thead><tr><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td rowspan="3">Pre-symbiotic communication</td><td>D27, CCD7, CCD8</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>DMI2</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>DMI3, IPD3</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td rowspan="5">Preparation for intracellular fungal accommodation</td><td>VAPYRIN</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>SbtM1, SbtM3</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>LIN, LIN-like</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>EXO70I</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>SYP13II</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td rowspan="3">Nutrient exchange</td><td>FatM, RAM2, DIS, STR, STR2</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>PT4</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>AMT2;3</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td rowspan="3">Regulation of symbiosis</td><td>RAD1, RAM1, GRAS18, GRAS38, GRAS43</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>WRI5</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>CBX1</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

**Fig. 1** (a) Root-fungus (mycorrhizal) associations in plant lineages having lost the capacity to establish the ancestral arbuscular mycorrhizal (AM) symbiosis (non-AM). Cropped images show distinctive cellular structures associated with the mucoromycotinal symbiosis, AM symbiosis (arbuscules), ectomycorrhizal symbiosis (mantle, fungal sheath), ericoid mycorrhizal symbiosis (coils) and orchid mycorrhiza (pelotons). The particular case of nonmycorrhizal Brassicaceae is shown, including hypotheses about their association with mycorrhizal-like fungi. (b) Conservation of AM-symbiosis essential plant genes in non-AM host plant lineages. Missing genomic data are shown with a hatched pattern. Reference proteins (Uniprot database) from *Lotus japonicus* and *Medicago truncatula* were BLASTed against genomes of species establishing ectomycorrhizal (*Picea glauca*, NCBI Taxonomy ID: 3330; *Pinus pinaster*, 71 647), ericoid mycorrhizal (*Rhododendron* sp., 4346) and orchid mycorrhizal associations (*Dendrobium catenatum*, 906 689; *Phalaenopsis equestris*, 78 828), as well as non-AM hosts (*Arabidopsis thaliana*, 3702; *Brassica rapa*, 3711) using BLASTP with default parameters.

transfer into the plant (major mycorrhizal features), but they do not form specific cellular structures specialized in nutrient trade, and the bidirectional nature of nutrient exchange has not been studied in most of them. Research on mycorrhizal-like fungi is relatively recent, and many important questions are still unanswered. Are the amounts of nutrients transferred to the plant relevant for plant

growth under natural conditions? Is there a systematic *quid pro quo*, that is do these fungi receive significant amounts of plant-derived C in return, or are these associations exploitative, that is without mutual nutrient exchange? How do these fungi interact with mycorrhizal fungi and more generally with the rest of the root microbiota? What is their quantitative contribution to nutrient
cycling in the rhizosphere? Is there a chemical dialogue and a
common genetic toolkit supporting root colonization and symbi-
otic functions? How old are these associations from an evolutionary
perspective? And are they in the 'waiting room' to evolve into true
mycorrhizal associations, as suggested elsewhere (Strullu-Derrien
et al., 2018)? In the following paragraphs, we will describe newly
discovered (non Mucoromycotina) mycorrhizal-like fungi and
their contribution to plant nutrition.

*Metarhizium* and closely related insect pathogenic endo-
phytes Ascomycota fungi from the *Metarhizium* and *Beauveria*
genera are entomopathogenic root endophytes found in association
with diverse plants including grasses, shrubs and trees (Wyrebek
et al., 2011). Using ¹⁵N-labelled insect larvae, it was shown that
these fungi are able to extract N from the dead larvae and transfer it
to their host plant (Behie et al., 2012), carrying it over 10–20 cm
distances (Behie & Bidochka, 2014). Reciprocally, C from ¹³C-
labelled plants was traced into fungal biomass and more specifically
in fungal chitin and trehalose compounds (Behie et al., 2017).
Interestingly, it was shown that the transfer of N from insect larvae
is a prerequisite to observe reciprocal C exchange from the plant,
verifying the *quid pro quo* principle observed in other plant–fungus
beneficial associations. Although N transfer seems to be widespread
across tested fungal isolates and hosts plants (Fabaceae and
Poaceae), higher amounts of transferred N tend to be observed in
Poaceae (Behie & Bidochka, 2014), which suggests some level of
preference in the association with monocots. The amounts of N
transferred by the fungus are likely to be relevant for plant growth
amounting up to 88% of total N in plant leaves (Behie & Bidochka,
2014). Fungal genetics has been used to identify genes involved in
N transfer, but the results are not completely clear. Indeed, contrary
to expectations, deletion of ammonium transporters (*MepC* and
*Mep2*) and a urease gene in *Metarhizium robertsii* showed increased
N transfer to barley, probably related to compensatory mechanisms
in the N metabolism of the fungus (Moonjely *et al*., 2019).

*Serendipita indica* (syn. *Piriformospora indica*) *Serendipita indica* is a basidiomycete fungus from the Sebacinales order, first isolated from a spore of the AM fungus *Glomus mosseae* in desert soil. Although *S. indica* has been rarely found in nature, sister species from the Serendipitaceae have been described world-wide as endophytes in monocotyledons and dicotyledons (including trees), and in mycorrhizal associations with green orchids. Upon inoculation, *S. indica* is able to endophytically colonize the roots and promote the growth of several monocot and dicot plant species, with virtually no plant species characterized as nonhost for *S. indica* (Weiß *et al*., 2016). In *A. thaliana* (Brassicaceae), the fungus has been shown to increase root growth, leaf biomass as well as P uptake. The observation that *S. indica*-inoculated plants could take up three times more P than control plants, over a short period of time (6 h), suggested P transfer capacities in the fungus (Shahollari *et al*., 2005), which were later confirmed using P isotope-tracing in compartmentalized systems (Bakshi *et al*., 2015). Further isotope-tracing studies showed that *S. indica* is also capable of transferring P and sulphur (S) to maize (Kumar *et al*., 2011; Narayan *et al*., 2021), and Fe to rice (Verma *et al*.,

2021). Although the molecular bases for these nutrient transfers
on the fungal side are not yet clear, the involvement of the fungal
sulphate transporter SiSuT (Narayan et al., 2021), the iron
transporter PiFTR (Verma et al., 2021) and the phosphate
transporter PiPT (Kumar et al., 2011) is strongly suspected.
Reciprocal C transfer from the plant to the fungus has not been
proven, but it is known that the fungus alters C metabolism in A.
thaliana, which could mediate the uptake of monosaccharides
from the plant by the fungus (Opitz et al., 2021).

*Heteroconium chaetospira* and other dark septate endophytes Dark septate endophytes (DSE) are a paraphyletic group of endophytic ascomycetes characterized by the formation of dark-pigmented hyphae often found inside plant roots. Plant–DSE associations have been described for more than 600 plant species and dozens of fungal taxa (Rodriguez et al., 2009). Isolation/reinoculation experiments with DSE have shown that they can promote plant growth through several mechanisms, including enhanced nutrient acquisition by the plant. The DSE *H. chaetospira* was shown to promote growth of its natural host *Brassica rapa* (Brassicaceae, Chinese cabbage) under N- and P-limited conditions. While the fungus was unable to promote plant growth in the presence of plant-available mineral N, it was able to increase plant biomass fourfold when an organic N source (amino acid) was present in the medium (Usuki & Narisawa, 2007). This is in line with findings on pleosporal and calosphaerial DSE associated with tomato (Vergara et al., 2017), which suggest that DSE can access and use organic N sources that are not available to the plant, and trade this resource with the plant in exchange for C. Indeed, N transfer between fungus and plant in the *H. chaetospira–B. rapa* association is coupled with reciprocal C transfer from the plant, as observed by tracing plant-derived ¹³C into the fungal mycelium (Usuki & Narisawa, 2007). Although the ecological significance of DSE remains enigmatic, DSE colonization of Cyperaceae and Caryophyllaceae plants under natural conditions appears to correlate with natural ¹⁵N enrichment in these plants, suggesting that DSE fungi mediate N uptake from organic sources in these nonmycorrhizal plant families (Giesemann et al., 2020).

*Colletotrichum tofieldiae* *Colletotrichum tofieldiae* was isolated from *A. thaliana* growing in a xeric grassland in central Spain on a low P soil (García *et al*., 2013). Although it has rarely been detected in other European *A. thaliana* populations (Hiruma *et al*., 2016), it has been isolated from other dicotyledonous and monocotyle-donous plants on different continents (Jayawardena, 2016). The fungus was shown to promote the growth of *A. thaliana* under low P conditions. Tracking of ³³P in compartmentalized systems showed that the fungus was capable of transferring P to the plant under low but not under high P conditions. This suggests that, as in the AM symbiosis, in this mycorrhiza-like association fungus-to-plant P transfer is regulated by the plant's phosphate starvation response (PSR). Indeed, PSR-deficient plant mutants did not express fungus-inducible PHT1 P transporters and showed reduced root colonization and P transfer by the fungus (Hiruma *et al*., 2016). On the fungal side, P transporters with high affinity for phosphate and similarity to the PHT1 family have been
<table><caption>**Table 1** Studies reporting fungus-to-plant nutrient transfers in mycorrhiza-like plant-fungus associations.</caption><thead><tr><th>Fungus (Phylum)</th><th>Plant (family)</th><th>Transfer direction</th><th>Nutrient used</th><th>Isotope used</th><th>Chemical form</th><th>Experimental system used</th><th>Detection method</th><th>Time of transfer detection (dpi)</th><th>References</th></tr></thead><tbody><tr><td>Heteroconium chaetospira (Ascomycota) DSE</td><td>Brassica rapa (Brassicaceae)</td><td>Fungus to plant</td><td>N</td><td><sup>14</sup>N</td><td>NaNO<sub>3</sub>, Gly, Leu, Phe, Valamino acids</td><td>In vitro. Agar/rock fibre</td><td>Increased plant biomass</td><td>60</td><td>Usuki & Narisawa (2007)</td></tr><tr><td>Pleosporales sp., Calosphaeriales sp. (Ascomycota) DSE</td><td>B. rapa (Brassicaceae)</td><td>Plant to fungus</td><td>C</td><td><sup>13</sup>C</td><td>CO<sub>2</sub></td><td>In vitro. Agar/rock fibre</td><td><sup>13</sup>C-NMR in roots and fungal hyphae</td><td>28</td><td>Usuki & Narisawa (2007)</td></tr><tr><td>Metarhizium robertsii (Ascomycota)</td><td>Solanum lycopersicum (Solanaceae)</td><td>Fungus to plant</td><td>N</td><td><sup>15</sup>N</td><td>(NH<sub>4</sub>)<sub>2</sub> SO<sub>4</sub>, <sup>15</sup>N-labelled plant biomass</td><td>Soil microcosms</td><td>Isotope ratio MS</td><td>50</td><td>Vergara et al. (2017)</td></tr><tr><td>Metarhizium robertsii (Ascomycota)</td><td>Phaseolus vulgaris (Fabaceae) and Panicum virgatum (Poaceae)</td><td>Fungus to plant</td><td>N</td><td><sup>15</sup>N</td><td>(NH<sub>4</sub>)<sub>2</sub> SO<sub>4</sub> injected in insect larvae (Galleria mellonella)</td><td>Soil microcosms</td><td>Increased amount of <sup>15</sup>N (NOI-5) emission spectrophotometer and <sup>15</sup>N-labelled amino acids (LC-MS) in plant shoots</td><td>7, 14 and 28</td><td>Behie et al. (2012)</td></tr><tr><td>Metarhizium spp. robertsii, acridum, flavoviride, brunneum, guizhouendse, Beauveria bassiana and Lecanicillium lecanii (Ascomycota)</td><td>P. vulgaris (Fabaceae)</td><td>Plant to fungus</td><td>C</td><td><sup>13</sup>C</td><td>CO<sub>2</sub></td><td>Soil microcosms</td><td><sup>13</sup>C-NMR on fungal hyphae</td><td>1, 7, 14 and 21</td><td>Behie et al. (2017)</td></tr><tr><td>Metarhizium spp. robertsii, acridum, flavoviride, brunneum, guizhouendse, Beauveria bassiana and Lecanicillium lecanii (Ascomycota)</td><td>P. vulgaris, Glycine max (Fabaceae), P. virgatum, Triticum aestivum (Poaceae)</td><td>Fungus to plant</td><td>N</td><td><sup>15</sup>N</td><td>(NH<sub>4</sub>)<sub>2</sub> SO<sub>4</sub> injected in insect larvae (Galleria mellonella)</td><td>Soil microcosms</td><td>Increased amount of <sup>15</sup>N (NOI-5) emission spectrophotometer in plant shoots</td><td>7, 14 and 28</td><td>Behie & Bidochka (2014)</td></tr><tr><td>M. robertsii (Ascomycota)</td><td>Phleum pratense, Bromus inermis, Dactylis spp. (Poaceae)</td><td>Fungus to plant</td><td>N</td><td><sup>15</sup>N</td><td>(NH<sub>4</sub>)<sub>2</sub> SO<sub>4</sub> injected in insect larvae (Galleria mellonella)</td><td>Field conditions</td><td>Increased amount of <sup>15</sup>N (NOI-5) emission spectrophotometer in plant shoots</td><td>28</td><td>Behie & Bidochka (2014)</td></tr><tr><td>Serendipita indica (Basidiomycota)</td><td>Zea mays (Poaceae)</td><td>Fungus to plant</td><td>P</td><td><sup>32</sup>P</td><td>Ortho-phosphate</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (autoradiography)</td><td>Data not available</td><td>Kumar et al. (2011)</td></tr><tr><td>Arabidopsis thaliana (Brassicaceae)</td><td>Fungus to plant</td><td>P</td><td><sup>32</sup>P</td><td>Ortho-phosphate</td><td>In vitro. Agar</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (scintillation counting)</td><td>6 or 14</td><td>Shahollari et al. (2005)</td></tr><tr><td>Z. mays (Poaceae)</td><td>Fungus to plant</td><td>S</td><td><sup>35</sup>S</td><td>Na<sub>2</sub> SO<sub>4</sub></td><td>In vitro. Agar</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (scintillation counting)</td><td>Data not available</td><td>Narayan et al. (2021)</td></tr></tbody></table>
<table><caption>**Table 1 (Continued)**</caption><thead><tr><th>Fungus (Phylum)</th><th>Plant (family)</th><th>Transfer direction</th><th>Nutrient</th><th>Isotope used</th><th>Chemical form</th><th>Experimental system used</th><th>Detection method</th><th>Time of transfer detection (dpi)</th><th>References</th></tr></thead><tbody><tr><td>Colletotrichum tofieldiae (Ascomycota)</td><td>A. thaliana (Brassicaceae)</td><td>Fungus to plant</td><td>Fe</td><td><sup>59</sup>Fe</td><td>Data not available</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (scintillation counting and autoradiography)</td><td>Data not available</td><td>Verma et al. (2021)</td></tr><tr><td>Heliotales sp. isolate F229 (Ascomycota)</td><td>Arabis alpina (Brassicaceae)</td><td>Fungus to plant</td><td>P</td><td><sup>33</sup>P</td><td>Ortho-phosphate</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (scintillation counting)</td><td>17</td><td>Hiruma et al. (2016)</td></tr><tr><td></td><td></td><td>Fungus to plant</td><td>P</td><td><sup>33</sup>P</td><td>Ortho-phosphate</td><td>In vitro. Agar</td><td>Radioactivity in fungus-inoculated plants (scintillation counting)</td><td>7, 10 and 15</td><td>Almario et al. (2017)</td></tr></tbody></table>

mycorrhizal roots (Paterson *et al.*, 1997). However, it is not known whether higher C exudation of ECM plant roots could inversely lead to higher N transfer from the ECM fungus to the plant. Field experiments in pine forests have shown an increase in ¹⁵N flux from soil to plants under CO₂ fertilization (fumigation), but these effects were only detected after 3 years of elevated CO₂ conditions (Hofmockel *et al.*, 2011). This may suggest that high CO₂ conditions favour ECM-mediated ¹⁵N transfer to trees, but *in vitro* experiments under controlled conditions are needed to test this hypothesis. In the case of Mucoromycotina mycorrhizal symbiosis, the exposure of liverworts to higher atmospheric CO₂ resulted in some cases in higher fungal C uptake, but this had no positive effect on P or N transfer from the fungus to the plant (Field *et al.*, 2015), suggesting that there is an uncoupling of P-for-C and N-for-C exchanges under high CO₂ conditions.

In addition to the effects of elevated CO₂, extreme temperature variations and drought may also affect nutrient exchange between plants and fungi. As with all microbes, the growth of AM fungi is temperature-dependent, with the extraradical mycelia being more temperature-sensitive than the intraradical mycelia. Using *in vitro* root organ cultures, Gavito *et al.* showed that nutrient exchange between plant and fungi (C and P) is quite robust at temperature variations between 15 and 30° (Gavito *et al.*, 2005), while temperatures of < 10° completely block mycorrhizal P uptake by the plant (Gavito *et al.*, 2003). Several research studies have shown that drought alters the profile of plant C exudation and the amount of compounds excreted by roots (Williams & Vries, 2020), but studies investigating the effects of drought on nutrient transfer between fungi and plants are still limited. As expected, symbiotic P transfer to the plant by AM fungi appears to be sensitive to drought conditions as shown in AM-inoculated *Medicago truncatula* plants, which acquired significantly more P than noninoculated plants, under drought conditions (Püschel *et al.*, 2021). As for C fluxes, under drought conditions AM colonized grasses allocate less C into rhizodeposits, which could suggest that less C was also allocated to the AM symbiont (Wang *et al.*, 2021).

## Will mycorrhiza-like associations help plants adapt to global climate change?

The importance of mycorrhizal associations for plant adaptation to climate change is widely recognized, but little attention has been paid to this in the case of the recently discovered mycorrhizal-like associations. It is likely that mycorrhizal-like fungi could play a central role by promoting nutrient uptake by nonmycorrhizal plants and by mycorrhizal plants, in ecosystems with low abundance of mycorrhizal fungi, but also by improving overall plant health (stress tolerance and disease resistance) through mechanisms other than nutrient transfer.

DSE fungi, including Heliotales taxa, are thought to promote local adaptation of plants in Arctic/alpine habitats by feeding on organic nutrient sources (Giesemann *et al.*, 2020), as AM fungal association become increasingly rare in high-altitude environments (Bueno de Mesquita *et al.*, 2018). Climate change is expected to drastically reduce snow cover and thus affect N
bioavailability in the coming years. DSE fungi could therefore
become important for the adaptation of alpine plants to reduced
snow cover and perturbed N cycling (Broadbent *et al.*, 2021).

*Serendipita indica* has been shown to promote drought resistance in rice by acting synergistically with *Bacillus* bacteria in the rhizosphere, jointly modulating plant hormone balance and subsequently rhizosheath formation (Xu *et al.*, 2021). In addition, *S. indica* enhances salt tolerance in its host *A. thaliana* via sodium (Na) and potassium (K) efflux transporters, thereby decreasing the Na content in the plant (Lanza *et al.*, 2019). Similarly, some DSE fungi are thought to improve drought resistance and salt tolerance in different plant species (Santos *et al.*, 2021). Under current global change scenarios, the abundance of plant pathogens in soil is predicted to increase (Delgado-Baquerizo *et al.*, 2020), implying that plant protection by endophytic mycorrhizal-like fungi could improve plant adaptation to increased disease pressure. *Serendipita indica* has been shown to promote plant resistance by modulating plant defences, but also by interacting with various rhizosphere bacteria acting through microbial processes involving lytic enzymes (Mahdi *et al.*, 2021). Similarly, *H. chaetospira* induces plant defence and has been described as a plant protection agent (Lahlali *et al.*, 2014).

The mutual exchange of nutrients in plant-microbe inter-
actions is a complex genetic trait. Symbioses between plants and
fungi have contributed significantly to the adaptation of plants
to new environments and trophic niches, and the bidirectional
exchange of nutrients has played an essential role (Rich et al.,
2021). We anticipate that this trait will provide genetic sources
of adaptation that will help plants resist further impacts of
climate change (such as invasion or the development of new
pathogens and drought), as well as grow crops that resist climate
change.

Acknowledgements

We apologize to all our colleagues in this field whose work could not
be cited due to a limited number of references. This work was
supported by funds from the Cluster of Excellence on Plant
Sciences of the Deutsche Forschungsgemeinschaft (DFG, German
Research Foundation) under Germany's Excellence Strategy –
EXC-2048/1 – project ID 390686111 to M.B. and by funds from
the French National Program EC2CO (Ecosphère Continentale et
Côtière) to JA. We thank three anonymous referees for providing
constructive comments on the manuscript.

Author contributions

JA and MB developed the concept of this review. All authors
contributed to the writing. JA and GS generated the figure.

ORCID

Juliana Almario ID https://orcid.org/0000-0002-1475-7819
Marcel Bucher ID https://orcid.org/0000-0003-1680-9413
Georgios Saridis ID https://orcid.org/0000-0001-8781-6886

References

Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M. 2017. Root-associated fungal microbiota of nonmycorrhizal *Arabis alpina* and its contribution to plant phosphorus nutrition. *Proceedings of the National Academy of Sciences, USA* 114: E9403-E9412.

Bakshi M, Vahabi K, Bhattacharya S, Sherameti I, Varma A, Yeh K-W, Baldwin I, Johri AK, Oelmüller R. 2015. WRKY6 restricts *Piriformospora indica*-stimulated and phosphate-induced root development in Arabidopsis. *BMC Plant Biology* 15: 305.

Barelli L, Moonjely S, Behie SW, Bidochka MJ. 2016. Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. *Plant Molecular Biology* 90: 657–664.

Becquer A, Garcia K, Amenc L, Rivard C, Doré J, Trives-Segura C, Szponarski W, Russet S, Baeza Y, Lassalle-Kaiser B *et al*. 2018. The *Hebeloma cylindrosporum* HcPT2 Pi transporter plays a key role in ectomycorrhizal symbiosis. *New Phytologist* 220: 1185–1199.

Behie SW, Bidochka MJ. 2014. Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. *Applied and Environmental Microbiology* 80: 1553–1560.

Behie SW, Moreira CC, Sementchoukova I, Barelli L, Zelisko PM, Bidochka MJ. 2017. Carbon translocation from a plant to an insect-pathogenic endophytic fungus. *Nature Communications* 8: 1–5.

Behie SW, Zelisko PM, Bidochka MJ. 2012. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. *Science* 336: 1576–1577.

Botnen SS, Thoen E, Eidesen PB, Krabberød AK, Kauserud H. 2020. Community composition of arctic root-associated fungi mirrors host plant phylogeny. *FEMS Microbiology Ecology* 96: fiaa185.

Bougoure J, Ludwig M, Brundrett M, Cliff J, Clode P, Kilburn M, Grierson P. 2014. High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid. *Plant, Cell & Environment* 37: 1223–1230.

Broadbent AAD, Snell HSK, Michas A, Pritchard WJ, Newbold L, Cordero I, Goodall T, Schallhart N, Kaufmann R, Griffiths RI *et al.* 2021. Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt. *ISME Journal* 15: 2264–2275.

Brundrett MC, Tedersoo L. 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. *New Phytologist* 220: 1108–1115.

Bueno de Mesquita CP, Sartwell SA, Ordemann EV, Porazinska DL, Farrer EC, King AJ, Spasojevic MJ, Smith JG, Suding KN, Schmidt SK. 2018. Patterns of root colonization by arbuscular mycorrhizal fungi and dark septate endophytes across a mostly-unvegetated, high-elevation landscape. *Fungal Ecology* 36: 63–74.

Calvo OC, Franzaring J, Schmid I, Müller M, Brohon N, Fangmeier A. 2017. Atmospheric CO₂ enrichment and drought stress modify root exudation of barley. *Global Change Biology* 23: 1292–1304.

Cameron DD, Johnson I, Leake JR, Read DJ. 2007. Mycorrhizal acquisition of inorganic phosphorus by the green-leaved terrestrial orchid *Goodyera repens*. *Annals of Botany* 99: 831–834.

Cameron DD, Leake JR, Read DJ. 2006. Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid *Goodyera repens*. *New Phytologist* 171: 405–416.

Charters MD, Sait SM, Field KJ. 2020. Aphid herbivory drives asymmetry in carbon for nutrient exchange between plants and an arbuscular mycorrhizal fungus. *Current Biology* 30: 1801–1808.

Cosme M, Fernández I, Van der Heijden MGA, Pieterse CMJ. 2018. Non-mycorrhizal plants: the exceptions that prove the rule. *Trends in Plant Science* 23: 577–587.

Delgado-Baquerizo M, Guerra CA, Cano-Díaz C, Egidí E, Wang J-T, Eisenhauer N, Singh BK, Maestre FT. 2020. The proportion of soil-borne pathogens increases with warming at the global scale. *Nature Climate Change* 10: 550–554.

Englander L, Hull RJ. 1980. Reciprocal transfer of nutrients between ericaceous plants and a *Clavaria* sp. *New Phytologist* 84: 661–667.

Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling D, Cameron DD, Duckett JG, Leake JR, Pressel S. 2019. Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. *New Phytologist* 223: 908–921.
Field KJ, Pressel S. 2018. Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. *New Phytologist* 220: 996–1011.

Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S. 2015. First evidence of mutualism between ancient plant lineages (Haplomitriopsidae liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO₂. *New Phytologist* 205: 743–756.

Finlay RD, Ek H, Odham G, Söderström B. 1988. Mycelial uptake, translocation and assimilation of nitrogen from ¹⁵N-labelled ammonium by *Pinus sylvestris* plants infected with four different ectomycorrhizal fungi. *New Phytologist* 110: 59–66.

García E, Alonso Á, Platas G, Sacristán S. 2013. The endophytic mycobiota of *Arabidopsis thaliana*. *Fungal Diversity* 60: 71–89.

Gavito ME, Olsson PA, Rouhier H, Medina-Peñafiel A, Jakobsen I, Bago A, Azcón-Aguilar C. 2005. Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. *New Phytologist* 168: 179–188.

Gavito ME, Schweiger P, Jakobsen I. 2003. P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO₂ enrichment. *Global Change Biology* 9: 106–116.

Genre A, Lanfranco L, Perotto S, Bonfante P. 2020. Unique and common traits in mycorrhizal symbioses. *Nature Reviews Microbiology* 18: 649–660.

Giesemann P, Eichenberg D, Stöckel M, Seifert LF, Gomes SIF, Merckx VSFT, Gebauer G. 2020. Dark septate endophytes and arbuscular mycorrhizal fungi (Paris-morphotype) affect the stable isotope composition of 'classically' non-mycorrhizal plants. *Functional Ecology* 34: 2453–2466.

Glynou K, Ali T, Buch A-K, Haghi Kia S, Ploch S, Xia X, Çelik A, Thines M, Maciá-Vicente JG. 2016. The local environment determines the assembly of root endophytic fungi at a continental scale. *Environmental Microbiology* 18: 2418–2434.

Hacquard S, Kracher B, Hiruma K, Münch PC, Garrido-Oter R, Thon MR, Weimann A, Damm U, Dallery J-F, Hainaut M *et al*. 2016. Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. *Nature Communications* 7: 11362.

van der Heijden MGA, Walder F. 2016. Reply to 'Misconceptions on the application of biological market theory to the mycorrhizal symbiosis'. *Nature Plants* 2: 1.

Hiruma K, Gerlach N, Sacristán S, Nakano R, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O'Connell R *et al*. 2016. Root endophyte *Colletotrichum tofieldiae* confers plant fitness benefits that are phosphate status dependent. *Cell* 165: 464–474.

Hofmockel KS, Gallet-Budynek A, McCarthy HR, Currie WS, Jackson RB, Finzi A. 2011. Sources of increased N uptake in forest trees growing under elevated CO₂: results of a large-scale ¹⁵N study. *Global Change Biology* 17: 3338–3350.

Jayawardena R. 2016. Notes on currently accepted species of *Colletotrichum*. *Mycosphere* 7: 1192–1260.

Karandashov V, Bucher M. 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. *Trends in Plant Science* 10: 22–29.

Kiers ET, Duhamel K, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A *et al*. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. *Science* 333: 880–882.

Kiers ET, West SA, Wyatt GAK, Gardner A, Bücking H, Werner GDA. 2016. Misconceptions on the application of biological market theory to the mycorrhizal symbiosis. *Nature Plants* 2: 1–2.

Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A *et al*. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. *Nature Genetics* 47: 410–415.

Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK. 2011. *Piriformospora indica* enhances plant growth by transferring phosphate. *Plant Signaling & Behavior* 6: 723–725.

Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G. 2014. *Heteroconium chaetospira* induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis. *PLoS ONE* 9: e94144.

Lanza M, Haro R, Conchillo LB, Benito B. 2019. The endophyte *Serendipita indica* reduces the sodium content of Arabidopsis plants exposed to salt stress: fungal ENA ATPases are expressed and regulated at high pH and during plant co-cultivation in salinity. *Environmental Microbiology* 21: 3364–3378.

Mahdi LK, Miyauchi S, Uhlmann C, Garrido-Oter R, Langen G, Wawra S, Niu Y, Guan R, Robertson-Albertyn S, Bulgarelli D *et al*. 2021. The fungal root endophyte *Serendipita vermifera* displays inter-kingdom synergistic beneficial effects with the microbiota in *Arabidopsis thaliana* and barley. *ISME Journal* 16: 876–889.

Moonjely S, Zhang X, Fang W, Bidochka MJ. 2019. *Metarhizium robertsii* ammonium permeases (MepC and Mep2) contribute to rhizoplane colonization and modulates the transfer of insect derived nitrogen to plants. *PLoS ONE* 14: e0223718.

Narayan OP, Verma N, Jogawat A, Dua M, Johri AK. 2021. Sulfur transfer from the endophytic fungus *Serendipita indica* improves maize growth and requires the sulfate transporter SiSulT. *Plant Cell* 33: 1268–1285.

Opitz MW, Daneshkhah R, Lorenz C, Ludwig R, Steinkellner S, Wieczorek K. 2021. *Serendipita indica* changes host sugar and defense status in *Arabidopsis thaliana*: cooperation or exploitation? *Planta* 253: 74.

Oulhen N, Schulz BJ, Carrier TJ. 2016. English translation of Heinrich Anton de Bary's 1878 speech, 'Die Erscheinung der Symbiose' ('De la symbiose'). *Symbiosis* 69: 131–139.

Paterson E, Hall JM, Rattray EAS, Griffiths BS, Ritz K, Killham K. 1997. Effect of elevated CO₂ on rhizosphere carbon flow and soil microbial processes. *Global Change Biology* 3: 363–377.

Pearson JN, Jakobsen I. 1993. The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with ³²P and ³³P. *New Phytologist* 124: 489–494.

Püschel D, Bitterlich M, Rydlová J, Jansa J. 2021. Drought accentuates the role of mycorrhiza in phosphorus uptake. *Soil Biology and Biochemistry* 157: 108243.

Radhakrishnan GV, Keller J, Rich MK, Vernié T, Mbadinga Mbadinga DL, Vigneron N, Cottret L, Clemente HS, Libourel C, Cheema J *et al*. 2020. An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages. *Nature Plants* 6: 280–289.

Rich MK, Vigneron N, Libourel C, Keller J, Xue LI, Hajheidari M, Radhakrishnan GV, Le Ru A, Diop SI, Potente G *et al*. 2021. Lipid exchanges drove the evolution of mutualism during plant terrestrialization. *Science* 372: 864–868.

Rodríguez RJ, White JF Jr, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. *New Phytologist* 182: 314–330.

Santos M, Cesanelli I, Diánez F, Sánchez-Montesinos B, Moreno-Gavira A. 2021. Advances in the role of dark septate endophytes in the plant resistance to abiotic and biotic stresses. *Journal of Fungi* 7: 939.

Shahollari B, Varma A, Oelmüller R. 2005. Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete *Piriformospora indica* and the protein accumulates in Triton X-100 insoluble plasma membrane microdomains. *Journal of Plant Physiology* 162: 945–958.

Sinanaj B, Hoysted GA, Pressel S, Bidartondo MI, Field KJ. 2021. Critical research challenges facing Mucoromycotina 'fine root endophytes'. *New Phytologist* 232: 1528–1534.

Strullu-Derrien C, Selosse M-A, Kenrick P, Martin FM. 2018. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. *New Phytologist* 220: 1012–1030.

Tedersoo L, Bahram M, Ryberg M, Otsing E, Köljalg U, Abarenkov K. 2014. Global biogeography of the ectomycorrhizal/sebacina lineage (Fungi, Sebacinales) as revealed from comparative phylogenetic analyses. *Molecular Ecology* 23: 4168–4183.

Thirkell TJ, Pastok D, Field KJ. 2020. Carbon for nutrient exchange between arbuscular mycorrhizal fungi and wheat varies according to cultivar and changes in atmospheric carbon dioxide concentration. *Global Change Biology* 26: 1725–1738.

Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V *et al*. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. *Proceedings of the National Academy of Sciences, USA* 110: 20117–20122.

Treseder KK. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO₂ in field studies. *New Phytologist* 164: 347–355.
Usuki F, Narisawa K. 2007. A mutualistic symbiosis between a dark septate endophytic fungus, *Heteroconium chaetospira*, and a nonmycorrhizal plant, Chinese cabbage. *Mycologia* **99**: 175–184.

Usyskin-Tonne A, Hadar Y, Yermiyahu U, Minz D. 2021. Elevated CO₂ and nitrate levels increase wheat root-associated bacterial abundance and impact rhizosphere microbial community composition and function. *ISME Journal* **15**: 1073–1084.

Vergara C, Araujo KEC, Urquiaga S, Schultz N, Balieiro FDC, Medeiros PS, Santos LA, Xavier GR, Zilli JE. 2017. Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material. *Frontiers in Microbiology* **8**: 2437.

Verma N, Narayan OP, Prasad D, Jogawat A, Panwar SL, Dua M, Johri AK. 2021. Functional characterization of a high-affinity iron transporter (*PIFTR*) from the endophytic fungus *Piriformospora indica* and its role in plant growth and development. *Environmental Microbiology* **24**: 689–706.

Wang B, Qiu Y-L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. *Mycorrhiza* **16**: 299–363.

Wang R, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA. 2021. Carbon allocation to the rhizosphere is affected by drought and nitrogen addition. *Journal of Ecology* **109**: 3699–3709.

Weiß M, Waller F, Zuccaro A, Selosse M-A. 2016. Sebacinales – one thousand and one interactions with land plants. *New Phytologist* **211**: 20–40.

Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J, West SA, Kiers ET. 2018. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. *Proceedings of the National Academy of Sciences, USA* **115**: 5229–5234.

Whiteside MD, Werner GDA, Caldas VEA, van't Padje A, Dupin SE, Elbers B, Bakker M, Wyatt GAK, Klein M, Hink MA *et al*. 2019. Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. *Current Biology* **29**: 2043–2050.

Williams A, de Vries FT. 2020. Plant root exudation under drought: implications for ecosystem functioning. *New Phytologist* **225**: 1899–1905.

Wu B, Nara K, Hogetsu T. 2001. Can ¹⁴C-labeled photosynthetic products move between *Pinus densiflora* seedlings linked by ectomycorrhizal mycelia? *New Phytologist* **149**: 137–146.

Wyrebek M, Huber C, Sasan RK, Bidochka MJ. 2011. Three sympatrically occurring species of *Metarhizium* show plant rhizosphere specificity. *Microbiology* **157**: 2904–2911.

Xu F, Liao H, Zhang Y, Yao M, Liu J, Sun L, Zhang X, Yang J, Wang KE, Wang X *et al*. 2021. Coordination of root auxin with the fungus *Piriformospora indica* and bacterium *Bacillus cereus* enhances rice rhizosheath formation under soil drying. *ISME Journal* **16**: 801–811.

<figure><img src="image_6.png" /></figure>

About New Phytologist

* *New Phytologist* is an electronic (online-only) journal owned by the New Phytologist Foundation, a **not-for-profit organization** dedicated to the promotion of plant science, facilitating projects from symposia to free access for our Tansley reviews and Tansley insights.

* Regular papers, Letters, Viewpoints, Research reviews, Rapid reports and both Modelling/Theory and Methods papers are encouraged. We are committed to rapid processing, from online submission through to publication 'as ready' via *Early View* – our average time to decision is <23 days. There are **no page or colour charges** and a PDF version will be provided for each article.

* The journal is available online at Wiley Online Library. Visit **www.newphytologist.com** to search the articles and register for table of contents email alerts.

* If you have any questions, do get in touch with Central Office (np-centraloffice@lancaster.ac.uk) or, if it is more convenient, our USA Office (np-usaoffice@lancaster.ac.uk)

* For submission instructions, subscription and all the latest information visit **www.newphytologist.com**