Plant biostimulants are referred to as natural-occurring or synthetic substances, which when applied to soil, seeds, and/or plants, can promote plant growth. There are several definitions for plant biostimulants. du Jardin (2015) defined “a plant biostimulant is any substance or microorganism applied to plants with the aim to enhance nutrition efficiency, abiotic stress tolerance and/or crop quality traits, regardless of its nutrient content”. Yakhin et al. (2017) proposed that a biostimulant is “a formulated product of biological origin that improves plant productivity as a consequence of the novel or emergent properties of the complex of constituents, and not as a sole consequence of the presence of known essential plant nutrients, plant growth regulators, or plant protective compounds.” Under the new regulation of the European Union (EU, 2019), “a plant biostimulant shall be an EU fertilizing product, the function of which is to stimulate plant nutrition processes independently of the product’s nutrient content with the sole aim of improving one or more of the following characteristics of the plant or the plant rhizosphere: (1) nutrient use efficiency, (2) tolerance to abiotic stress, (3) quality traits, or (4) availability of confined nutrients in the soil or rhizosphere”. To be more explicit, plant biostimulants are products that can improve plant growth.

Biostimulants are derived from a wide range of biological and inorganic materials (Calvo et al., 2014) and have been classified into seven categories (du Jardin, 2015): (1) humic and fulvic acids or humic substances, which are a group of heterogeneous, highly acidic compounds resulting from the decomposition of soil animal, microbial, and plant residues; (2) protein hydrolysate and other nitrogen (N)-containing compounds, referring to a mixture of amino acids and peptides obtained through enzymatic and chemical hydrolyses of animal wastes and plant residues; (3) seaweed extracts and botanicals, which are derived from seaweed or plants with biostimulant activities; (4) chitosan and other biopolymers, this includes biodegradable and biocompatible poly- and oligomers produced from natural produces; (5) inorganic compounds, mainly referring to beneficial elements, such as silicon, titanium, sodium, selenium, iodine, and aluminum (Al); (6) beneficial fungi, which include those either associated, endophytic or symbiotic with plants that possess biostimulant activities; and (7) beneficial bacteria, also referring to associated, endophytic, or symbiotic bacteria promoting plant growth. Based on the above classifications, biostimulants could be broadly divided into non-microbial and microbial plant biostimulants (Rouphael and Colla, 2020). It was estimated that biostimulant products could grow to $2 billion in sales in 2018 (Calvo et al., 2014). More than 700 scientific papers on biostimulants had been published from 2009 to 2019 (Rouphael and Colla, 2020), indicating an increasing awareness of their importance to crop production.

Beneficial fungi include Trichoderma species, mycorrhizal fungi, yeasts, endophytes, and avirulent/hypovirulent strains of some pathogens (Ghorbanpour et al., 2018). Mycorrhizal fungi are a heterogeneous group of taxa that can establish symbiotic relationships with roots of most terrestrial plants, promoting plant acquisition of nutrients in exchange for carbon sources derived from photosynthesis (Addy et al., 2005; Bonfante and Genre, 2010; Leopold, 2016). Mycorrhizas are traditionally grouped into arbuscular mycorrhiza (AM), ericoid mycorrhiza (ErM), ectomycorrhiza (EcM), and orchidaceous mycorrhiza (OrM) (Pandey et al., 2019; Miyauchi et al., 2020). AMs are considered the most widespread symbiotic association as 80-90% of terrestrial plants can be colonized by this group of fungi (Gianinazzi et al., 2010). The beneficial effects of AMs on plants are known to be most noticeable when symbiotic relationships are established at the earliest stage of plant growth (Niemi et al., 2004). AM fungi have been reported as biostimulants (Xavier and Boyetchko, 2002; Rouphael et al., 2015), natural biofertilizers (Berruti et al., 2016), and plant growth regulators (Begum et al., 2019). However, ErM fungi as biostimulants have not been reported. An ErM is referred to as a symbiotic complex of plant roots and fungal components. ErM fungi represent a unique group of fungi that can symbolize with plants in the family Ericaceae or heather family and play vital roles for plants in adapting harsh growing environments (Read, 1996); however, ErM has been the least studied, and the least understood mycorrhizal symbiosis (Vohník, 2020).

This article is intended to briefly introduce ErM fungi and review available literature related to ErM fungi in biosynthesizing bioactive compounds, promoting plant growth, and improving plant tolerance and resilience to abiotic and biotic stresses. Our review indicates that ErM fungi are valuable biostimulants that can synthesize bioactive compounds, including plant growth regulators, promote seed germination and rooting of cuttings, improve plant tolerance to heavy metals, drought, and soil salinity, and resistance to plant diseases, and enhance the growth of ericaceous plants ( Figure 1 ).

Ericoid mycorrhizal fungi largely belong to Ascomyceta and Basidiomycota (Perotto et al., 2018; Fehrer et al., 2019; Vohník, 2020). The most important ErM fungi in Ascomyceta include the Hyaloscypha hepaticicola aggregate, formerly known as the Rhizoscyphus ericae aggregate or Hymenoscyphus ericae aggregate (Fehrer et al., 2019), which include H. hepaticicola, possibly Hyaloscypha variabilis (syn. Meliniomyces variabilis) as well as Oidiodendon maius and Leohumicola spp (Vohník, 2020). H. hepaticicola was actually the first experimentally confirmed ErM species (Pearson and Read, 1973). O. maius was initially isolated by Barron (1962) from peat soils collected in Canada and subsequently from ericaceous plant roots in Japan (Tokumasu, 1973). Later, O. maius was identified from other plant roots and decayed organic materials, peat, and acidic soils (Rice and Currah, 2005; Rice and Currah, 2006). Leohumicola species are another group of ErM fungi, which have a remarkable tolerance to high temperatures (Adeoyo et al., 2018; Adeoyo et al., 2019).

The basidiomycetous ErM fungi are composed of sebacinoid fungi from Serendipitaceae (Vohník et al., 2016) and non-sebacinoid fungi (Kolařík and Vohník, 2018) as well as those from the Kurtia argillacea species complex (syn. Hyphodontia argillaceum, Hyphoderma argillaceum) (Vohník, 2020). With increasing exploitation of ErM fungi worldwide, more ericoid mycorrhizal fungi have been reported. For instance, two ascomycetous genera: Cairneyella (Midgley et al., 2016) and Gamarada (Midgley et al., 2018) were found to be ErM fungi in Australia.

Ericoid mycorrhizal fungi are able to colonize roots of ericaceous plants. The fungi initially grow on the surface of hair roots, establishing loose hyphal networks. Hyphae then penetrate cortical cell walls to form intracellular densely packed individual cells, which is known as coils (Vohník et al., 2012). Thus, ericoid mycorrhiza has structurally well-defined endomycorrhiza that are distinctly different from the other mycorrhizae due to the formation of fine compact intracellular hyphal coils in the rhizodermal cells of hair roots. The coil is the site for transferring nutrients absorbed by ErM fungi from the soil to root cells and carbohydrates fixed by plant photosynthesis to fungi. The hyphal sheaths or mantles around healthy hair roots are somewhat similar to those occurring in some EcM (Vohník, 2020). It was observed that both cell-to-cell (between neighboring rhizodermal cells) and single cell (from soil to individual rhizodermal cells) hyphal colonization happened in the rhizodermis of ErM-colonized hair roots (Massicotte et al., 2005; Vohník, 2020).

Interestingly, a recent study showed that ErM fungi, specifically those in the genus Hyaloscypha can colonize not only roots, but also stems, leaves, and flowers of Vaccinium myrtillus (Daghino et al., 2022). The colonization of the above-ground organs is explained by the evolutionary closeness between the genus Hyaloscypha and non-mycorrhizal fungal endophytes based on the genomic similarity. However, it is unknown at present what role Hyaloscypha plays in the aerial plant organs of ericaceous plants.

The family Ericaceae has about 4,500 species across 125 genera, which are either herbs, dwarf shrubs, shrubs, or trees that are distributed in tundra, heathland, and understory of boreal forests in the Northern Hemisphere (Luteyn, 2002; Grelet et al., 2009). Economically important ericaceous plants include Rhododendron L., blueberry (Vaccinium sect. Cyanococcus Rydb. spp.), bilberry (Vaccinium myrtillus L.), cranberry (Vaccinium subg. Oxycoccus (Hill) A. Gray spp.), and huckleberry (Vaccinium parvifolium sm.). Plants in the genus Rododendron are popular ornamental plants. There are more than 28,000 cultivars of Rhododendron (12,989 azaleas, 14,298 rhododendron, and 108 azaleodendrons hybrids) in the International Rhododendron Registry held by the Royal Horticultural Society (Leslie, 2002). Additionally, rhododendron plants are important ethnopharmacological and toxicological plants (Popescu and Kopp, 2013; Wei et al., 2018). On the other hand, the berries, such as blueberry and cranberry have high nutraceutical and pharmaceutical value and are considered super fruit (Whyte and Williams, 2015; Vendrame et al., 2016). Blueberry varieties include lowbush, southern highbush, northern highbush, half-high, and rabbiteye. Among them, the production of highbush varieties increased substantially from 58,400 ha in 2007 to 110,800 ha in 2014. North America accounted for more than 50% of the production area, representing about 60% of highbush blueberry production in the world in 2014 (Qiu et al., 2018).

Ericaceous plants have some unique characteristics: (1) Roots are fibrous, very fine multicellular roots ranging from 100 to 750 μm in diameter, and cortical cells never form root hairs. Instead, roots of ericaceous plants are known as hair roots (Watkinson, 2016). Roots are mainly distributed in the upper 5 cm of soil depth, representing more than 50% of new roots produced during a growing season (Atucha et al., 2020). Root growth of cranberry exhibited a unimodal curve with one significant flush at bloom and a peak at the end of fruit maturation. (2) They are able to grow in soils low in pH (4 to 5) and poor in nutrient availability. Under such a pH range, nitrification could be largely negligible due to its detrimental effect on the nitrifying bacteria (Paul and Clark, 1989). It was proposed that ericaceous plants grown in the low pH soil might lose their ability to take up nitrate (NO₃ ^-). (3) Roots are colonized by mycorrhizal fungi, mainly ErM fungi (Xiao and Berch, 1992; Usuki et al., 2003; Vohník et al., 2007; Tian et al., 2011). Root cortex and epidermis could be fully filled with mycorrhizal hyphal coils (Atucha et al., 2020). The colonization plays a critical role for ericaceous plants to absorb nutrients including NO₃ ^-. Cranberry roots inoculated with R. ericae were able to absorb NO₃ ^- under a low pH regime (Kosola et al., 2007). Accumulating evidence has indicated that the symbiosis established between roots and ErM fungi is essential for ericaceous plants to absorb nutrients and to survive and grow in the harsh environment (Read, 1996; Cairney and Meharg, 2003; Zhang et al., 2009; Perotto et al., 2012).

Ericoid mycorrhizal fungi have been shown to improve seed germination and rooting of microcuttings or stem cuttings of ericaceous plants ( Table 1 ). Seeds of ericaceous plants are small with an average length of 1.5 mm and a mean width of 0.5 mm, and they generally have a poor germination rate due to the limited supply of nutrition from the endosperm. In a mesocosm study conducted for determining if novel ErM communities could assist or hamper the shift of northward species of Rhododendron, Mueller et al. (2022) reported that germination rates of R. catawbiense and R. maximum after inoculation with novel soils containing ErM fungi were significantly greater than those of controls (without mycorrhizal fungi) or inoculated with conspecific soils, 75.2% vs. 54.5% for R. catawbiense and 65.7% vs. 54.4% for R. maximum. The increased germination rates were attributed to the occurrence in ErM fungi, but the authors did not provide the underlying mechanisms. In addition to seed germination, ErM has been documented to promote seedling growth of Rhododendron. An ErM fungus known as O. maius Om19 inoculated in a peat-based substrate substantially enhanced seedling growth of R. fortunei Lindl. because root growth including root length, root numbers, root fresh weight as well as shoot growth, including shoot overall height and shoot fresh weight of Om19 colonized seedlings were doubled compared to the uninoculated control seedlings (Wei et al., 2016a). Additionally, overall fresh and dry weights of R. fortunei seedlings inoculated with Om19 were 81% and 84% higher than those of the control, respectively. Furthermore, genes related to N uptake and metabolism were analyzed by qRT-PCR, and results showed that the expression of an ammonium transporter (AMT), two nitrate transporters (NRT1-1 and NRT1-2), glutamate synthase (GOGAT), and glutamine synthetase (GS) were highly upregulated in plants inoculated with Om19, ranging from 2 to 9 folds greater than the uninoculated plants (Wei et al., 2016a).

Ericoid mycorrhizal fungi can substantially improve rooting of stem cuttings as well as microcuttings derived from tissue culture (Eccher et al., 2010; Wei et al., 2020). Stem cuttings of blueberry plants inoculated with ErM fungi rooted more successfully and were followed by enhanced plant growth (Scagel et al., 2005a; Scagel et al., 2005b). Root initiation and root growth of dog hobble (Leucothoe fontanesiana) (Scagel, 2005b) and Vaccinium meridionale, a Colombian blueberry (Ávila Díaz-Granados et al., 2009) also increased with the inoculation of ErM fungi. Recently, micropropagation, shoot culture in particular, has been increasingly used for propagation of important ericaceous plants, such as rhododendron, cranberry, and blueberry (Fan et al., 2017; Wei et al., 2018). An interesting phenomenon observed during the rooting of microcuttings is that in vitro rooting is more difficult than ex vitro rooting (Gorecka, 1979; Fan et al., 2017; Qiu et al., 2018; Wei et al., 2018). To explore the underlying mechanisms behind this phenomenon, Wei et al. (2020) developed an in vitro culture system for R. fortunei and investigated the adventitious root (AR) formation in microcuttings inoculated with or without O. maius Om19. Key phytohormones and precursors involved in the pathway of indole-3-acetic acid (IAA) biosynthesis were analyzed in Om19 mycelium. Om19 was able to synthesize tryptophan (Trp), indole-3-pyruvate (IPA), and IAA, of which Trp concentration was greater than 4,000 mg/kg. The occurrence in Trp, IPA, and IAA indicated that Om19 biosynthesis of IAA is through the Trp-dependent pathway (Mano and Nemoto, 2012). Other hormones synthesized by Om19 include brassinolides (BRs), jasmonic acid (JA), and salicylic acid (SA). BRs were reported to positively impact the symbiosis of either tomato or tobacco roots with an AM fungus (von Sivers et al., 2019). JAs are known as a wound signal in AR formation because wounding quickly induces JA accumulation in plant tissues (Zhang et al., 2019). Increased JA concentrations have been shown to promote AR formation in cuttings by IAA accumulation in the base of stem cuttings towards AR source cells (Druege and Franken, 2019). SA is known for triggering systemic-acquired resistance (SAR) in plants (Chen et al., 1996). Low concentrations of SA was reported to promote AR formation and change the root apical meristem architecture, but high SA concentrations suppressed the root growth process (Pasternak et al., 2019). After Om19 inoculation, ARs rapidly appeared from microcuttings. Meanwhile, genes related the symbiosis including SymRK and DMI were activated in ARs, resulting in Om19 colonization of the roots. Furthermore, YUC3, a key gene controlling IAA biosynthesis in plants (Cheng et al., 2007; Won et al., 2011), genes encoding N absorption (AMT and NRT) and N metabolism (GOGAT and GS) as well as phosphate transporter (PHT) in Om19-inoculated plants were upregulated by 3 to 7 folds compared to control plants without Om19 inoculation. As a result, inoculated plants were able to take up significantly higher quantities of nutrients including N, P, K, Ca, Mg, and S, and plant growth substantially increased compared to the control plants. A working model for the Om19-mediated AR formation was proposed. The rapid AR formation on the one hand was induced by IAA produced by Om19 and on the other hand by IAA biosynthesized by plants. The high concentration of Trp synthesized by Om19 could be readily used by plant as the precursor to synthesis of IAA. The formation ARs, in turn, provided Om19 with host for colonization. This study for the first time documented the ability of Om19 to biosynthesize several hormones, of which IAA plays an important role in inducing AR formation.

This model also provides explanations as to why ex vitro rooting of microcuttings is more effective than in vitro rooting. A major component of commercial substrates is peat moss, ranging from 30% to 75% based on volume (Chen et al., 2005). As mentioned before, O. maius was initially isolated from peat soils by Barron (1962). Commercial substrates rich in peat moss might have ErM mycorrhizal fungi. Gorman and Starrett (2003) screened ErM occurrence in commercial substrates and found that the majority of the peat and peat-based substrates used in the U.S. and Canada contained ErM fungi. ErR fungi were reported to naturally colonize roots of blueberry plants during nursery production (Scagel, 2005a). Thus, the ErM fungi in the substrates could act similar to Om19 in biosynthesis of phytohormones including IAA for inducing AR formation of ericaceous plant cuttings. Those ErM may also synthesize a large amount of Trp for plants to produce endogenous IAA. In general, endogenous hormones are more effective than exogenous application. Ismail et al. (2021) reported that bacterial and fungal endophytic metabolites significantly enhanced plant growth compared to exogenous applied hormones. IAA biosynthesized inside plants by either plants or ErM could be considered endogenous and thus could be more effective for inducing AR formation than exogenous applied auxin during in vitro rooting.

Ericoid mycorrhizal fungi also produce other bioactive compounds ( Table 2 ). Some can increase bioavailability of soil mineral elements, such as siderophore for chelating soil Fe (Ahmed and Holmström, 2014). Some are enzymes, including cell-wall-degrading enzymes (PCWDEs) that can degrade soil organic matter (SOM) (Kohler et al., 2015; Martino et al., 2018). Others have antimicrobial activities (Hosoe et al., 1999; Ouyang, 2021), and still others are antioxidants, such as rutin (Lin et al., 2021).

Ericoid mycorrhizal fungi have been well documented for promoting the growth of ericaceous crops. ErM fungi are able to establish symbiotic relationships with plant roots. The established symbiosis enables plants to better adapt to acidic soils with low pH values and low nutrient status and improve root acquisition of nutrients, thus, enhancing plant growth. The growth enhancement is attributed to several factors: (1) The ability of ErM to biodegrade SOM resulting in the bioavailability of nutrients for plants; (2) the symbiosis-resultant expansion of nutrient acquisition surface area for capturing more mineral elements; and (3) the upregulation of gene expression, such as those associated with symbiosis and N and P uptake and metabolism, leading to the increased N and P absorption and metabolism and enhanced plant growth.

Plants as sessile organisms and permanently stay in their established sites. In addition to harsh environmental conditions, ericaceous plants often encounter other stressful factors, such as salt, drought, heavy metals as well as plant pathogens. Evidence has shown that in addition to growth promotion, symbiotic ErM fungi can substantially improve plant tolerance to abiotic and biotic stresses ( Table 4 ). The enhanced stress tolerance in turn can improve plant productivity compared to those without symbiotic establishment.

Ericoid mycorrhizal fungi have saprotrophic and biotrophic lifestyles and are able to biodegrade SOM and establish symbiotic relationships with plants in the family Ericaceae. The degradation of SOM results in the bioavailability of nutrients to themselves and plants. The symbiosis extends their life cycle and also enhances seed germination, rooting of cuttings, plant growth as well as tolerance to abiotic and biotic stresses. This review documents that the improved plant growth is related to hormones produced by ErM fungi and also colonization-resultant expression of genes in N and P absorption and metabolisms. Thus, ErM fungi is considered biostimulants for promoting the establishment and growth of ericaceous plants. Considering some species in the family Ericaceae are economically important crops, it is expected that some ErM fungi could be developed as biofertilizers for improve plant propagation and production.

Our understanding of the ErM-mediated biostimulating effects on ericaceous plants, however, is largely incomplete. Further research is warranted to (1) identify and isolate key genes from ErM fungi in biodegradation of SOM, particularly ON and explore the genes for improving soil fertility, (2) evaluate important ErM species or strains in biosynthesis of hormones and isolate those for increased production of hormones through bioreactor and utilize the isolates for improving plant propagation and production, (3) analyze heavy metal tolerant species or strains of ErM through omics to identify the mechanism underlying metal tolerance and use the isolates for phytoremediation of metal-contaminated soils, and (4) develop ErM biofertilizers by combining different species or strains, each with specific biostimulating effects on propagation, growth promotion, and/or stress tolerance for improving the productivity of ericaceous plants.

JC, XW, CZ, and FZ conceived the idea, WZ conducted literature search and prepared the tables and figures. JC and XW wrote the initial draft. All authors edited, refined the manuscript, and approved for its submission.

This work was supported in part by the Natural Science Foundation of Fujian Province to XW (General program, Grant No. 2020J01867).

The authors would like to thank Ms. Terri A. Mellich for critical review of this manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.