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Recent Trend: Is the Role of Arbuscular Mycorrhizal Fungi in Plant-Enemies Performance Biased by Taxon Usage?


Arbuscular mycorrhizal (AM) fungi are monophyletic in origin and constitute five orders, 29 genera, and 230 species (Oehl el al., 2011; Schussler el al., 2001; Redecker el al. 2013). Multifunctional, these organisms are the subject of research conducted al both community and molecular levels (Bever el al., 2001; Harrison, 2004). AM-fungi can colonize plant roots and are mutually beneficial to plant hosts participating in carbon-resource exchange (Jakobsen and Rosendahl, 1990; jakobsen el al., 1992; Wang et al., 2014). While these fungi often enrich plant quality and nutritional value, mycorrhizal interactions can also induce gene expression patterns that resemble pathogen-associated responses (jones and Dangl, 2006; Gianinazzi, 1996; Pearson et al., 1996). Consequently, appressoriuin formation or initial contact between mycorrhizae and plant host may upregiilale a myriad of planl defenses (Harrison, 1998; Genre et al., 2008). As chilin is evolutionary conserved among fungi (Lenardon el al., 2010; Bonfante-Fasolo et al., 1990) and exposure to AM-fungi has the potential to prime defenses and confer resistance toward natural enemies (Jung et al., 2012; Campos-Soriano et at., 2012; Zipfel, 2014). While this may seem promising, especially as it relates to bioproteclion, discrepancies in mycorrhizal laxa usage maybe biasing this area of research

Plant enemies, including pests and pathogens, may be attracted to plants colonized by mycorrhizae given that mycorrhizal plants are often nutritionally enriched (Jakobsen el al., 1992; Bennett et al., 2005). As networks of mycorrhizal mycelia scavenge nitrogen and phosphorus (Hodge el al., 2001; Sanders and Tinker, 1973), these nutritional resources are then exchanged within the confines of plant root cortical cells (Blee and Anderson, 1998; Wang el al., 2014). Improving plant growth and nutritional uptake may improve a plant's tolerance of natural enemies (Bennett and Bever, 2007; Feng el al, 2002; Middleton et al., 2015), but it may also lead to greater pathogen and herbivore exploitation. Prieto et al. (2016) observed when given a choice, myrid bug (Hernipteran) had a preference for plants colonized by AM-fungi. Meanwhile, Ronsheim (2016) revealed among Allium spp, the genotype that is most susceptible toward Sclerotium cepivorum, the causal agent of onion rot, received greater growth benefit from AMfungi, in comparison to the genotype that showed resistance.

Although plant-enemies may exploit healthier hosts, mycorrhizal protection may still prevail (Bennett et al., 2006). Arbuscule formation has been shown to provide localized immunity against intracellular pathogens and root feeding herbivores (Pozo el al., 2002; Pena and Echeverria, 2006; Frew el al., 2017). Meanwhile, recent advances in sequence data analysis has shown that AM-fungi reduces pathogen abundance within roots and the corresponding rhizosphere (Jie et al., 2015; Qian et al., 2015). However, aboveground effects are not as straightforward, as systemic acquired resistance includes bioprotection toward enemies antagonizing distal plant tissues (der Ent et al., 2009; Pieterse et al., 2014; Pozo and Azcon-Aguilar, 2007). Considering the effects of a broad range of mycorrhizal taxa on plant-enemy outcomes may provide additional insight onto the robustness of mycorrhizae in systemic acquired resistance. It may be the case that our understanding of tnycorrhizal influence on plant-enemy outcomes are limited by redundancy in mycorrhizal taxon usage. For this reason, it is important to investigate taxon usage in this area of research.


A survey was conducted to determine the latest trends in mycorrhizal plant-enemy performance. The terms "Myrorrhiz* AND biocontrol OH insect OH pathogen OH nematode" were used for query in Google Scholar. Articles considered in this survey were published between 2014 and 2017 to uncover recent bioprotection trends. The survey included all articles reporting plant-enemy performance with respect to mycorrhizae versus mycorrhizal control. Studies that reported plant tolerance to biotic stress, or trophic links that did not directly interact with the plant host, were not included in this survey. A total of 42 studies were identified in which herbivore, pathogen, or nematode performance was assessed in lhe presence or absence of AM-fungi. The results revealed that mycorrhizae did not reduce plant-enemy performance in 25% of case studies. In addition, the majority of studies that quantified plant-enemy performance featured fungal pathogens or herbivores, while few studies featured viruses and bacterial pathogens. Interestingly, 75% of plant-enemy performance studies featured a single species of AM-fungi, and perhaps even more compelling is the observation that the majority of studies featured either Hliizophtigus irregularis or Funneliformis mosseae (Fig. D. I bis suggests the latest trends in mycorrhizal bioprotection may not be as robust as one might expect, due to redundancy in taxon usage.



While the role of AM-fungi in plant-herbivore interactions may depend on ecological context, realized bioprotection may also depend on feeding guild. Herbivores of a phloem feeding guild are likely lo evade plant defenses, while chewers may be more vulnerable toward plant immune responses (Ali and Agrawal, 2012). For example, in Plantago lanceolala, chewing herbivores were observed to induce secondary metabolites. Meanwhile, phloem feeders were observed to down regulate these compounds (Suiter and Muller, 2011). This may relate to the fact that chewers induce the transcription of jasmomic acid-dependent genes, while phloem feeders are more likely to induce the transcription of salicylic aciddependent genes (Heidel and Baldwin, 2004).

Among pathogens there is also a similar dichotomy with respect to trophic guild. Biotrophic pathogens that effectively feed on living cells induce defense genes of the salicylic acid pathway, whereas necrotrophs that effectively feed on dead cells, induce defense genes of the jasinonic acid defense pathway (Spoel and Dong, 2008). 'I'hese plant defense pathways may allow mycorrhizae to modulate resistance toward pathogens. Rhizobacteria's microbial-associated molecular patterns, including flagella and lipopolysaccharides, may elicit plant defenses and confer induced systemic resistance (Van Wees et til., 2008). Similarly, AM-fungi may enable systemic acquired resistance by localizing PATHOGENESIS RELATED-1 protein to the site of pathogen attac k (Cordier et al., 1998). By reducing the negative effect of pathogens at distal plant tissues, mycorrhizae may effectively facilitate bioprotection. However, the role of mycorrhizae in these interactions are a bit complex. As mycorrhizae may induce a plant's salicylic acid-dependent genes during the initial stages of root colonization, but then relax its effect on this plant hormonal pathway, to then induce jasinonic acid-dependent genes during mature stages of colonization, including arbuscule formation (Pozo and Azcon-Aguilar, 2007). This may suggest bioprotection provisioned by mycorrhizae may also depend on development and life-stage position.


Among pathogens, change in density or transcript level may be an effective measure of plant enemy performance (Jie el al. 2015; Qian et al, 2015; Malik et al, 2016). However, herbivores may be a bit more intricate. As herbivore growth rate, development time, consumption, mass, fecundity, survival, opposition preference, plant damage, or density may all yield different outcomes with respect to bioprotection (Koricheva et al., 2009). For example Bennett et al. (2016) found AM-fungi did not reduce density of a phloem feeder (aphid). Despite this, AM-fungi improved parasitoid attack on aphids via oviposition preference. Ibis suggests if the parameter used to report plant-enemy performance is parasitism, then the role of AM-fungi in bioprotection is validated, but if the parameter is aphid density, ilien bioprotection is not validated. Regardless of the specific measure utilized, the majority of recent studies support reduction in plant-enemy performance by AM-fungi, perhaps suggesting a promising role for AM-fungi in mediating tolerance or resistance toward plant enemies. However, there is still a need to expand these studies beyond single species of AM-fungi. As a way to determine potential synergistic and antagonistic relationships that may exist among AM-fungal combinations, especially as these relationships pertain to fungal communities. Al the community level, species that provide bioprotection may be outconipeted by cheater laxa that do not provide protection. Competition effects may explain the observation by Malik et al. (2016(i), that Entrophaspora infrequent provides bioprotection against foliar pathogen, but is ultimately outcompeted by F. mosseae, a nonprotective mycorrhizal taxon.


Anthropogenic disturbances, including land cultivation and agricultural practices, may be limiting mycorrhizal biodiversity (Duchicela et al., 2013). As a result altered soil physical properties due to agricultural practices may favor F. mosseae. This is supported by Helgason el al. (1998), which found F. mosseae is most abundant at agricultural sites, such that F. mosseae makes up 92% of OTU's. Rosendahl et al. (2009) provides additional evidence that suggests F. mosseae's range expansion and global distribution is attributed to agriculture, Rhizophagus irregularis, another taxon that is often used in studies is also observed to be over-represented in agricultural soils with high clay content (Mathimaran et al, 2005). It may be the case that mycorrhizal taxa that experience the greatest taxon usage, also happen to be the taxa that benefit the most from land cultivation. F. mosseae and It irregularis environmental abundances may also be attributed to their ability to outcompete other mycorrhizal taxa. Malik et ai (2016) showed that when Glycine max was inoculated with a mycorrhizal consortia that included F. mosseae, as well as three other mycorrhizal taxa (Entrophospora infrequens, C.laroideogbmus daroideum, and Racocctra fulgida), sporulation was only detected for F. mosseae, suggesting that F. mosseae can compete effectively for plant resources that are necessary to promote its own abundance. Similarly, coinoculation with R. irregularis and Glomus aggregatum lead to greater R. irregularis ultraradical and extraradical colonization (Engelmoer el al., 2014).

By de facto, R. irregularis, and F. mosseae may be mycorrhizal model organisms. Despite the fact this classification is rarely used when referring to mycorrhizae. In addition mycorrhizal taxon usage is rarely justified in article methodologies, this lack of justification may be due to a snowball effect', such that contemporary taxon usage is modelled off past taxon usage. Thereby, favoring the high usage rates of R. irregularis and F. mosseae. Alternatively, this trend in taxon usage may be a technical issue, in that R. irregularis and F. mosseae may be the most cullurable of the ~230 species of AM-fungi.

The survey presented here suggests bioprotection studies are biased toward R. irregularis and F. mosseae (Fig. D. Although it may be the case that these two species are most efficient at providing bioprotection, this generalization cannot be made without an increase in laxon usage, pairwise comparisons, and fungal community treatments. Moving forward, studies in this area of research should draw conclusions based on multiple AM-Fungal taxa and follow the approach of Sundram et al. (2015), which showed R. irregularis, a taxon of high usage rate (Fig. 1), reduces stem rot in tropical trees. Whereas Rhizophagus clams (formerly Glomus darum), a taxon of low usage rate, does not. The advantage of this approach is that generalizations about AM-fungi are not based on a single overrepresented taxon (Fig. D. Therefore, studies addressing the role of AM-fungi in bioprotection should take into account multiple AM-fungal taxa to better understand mycorrhizal mediated effects on plant-enemy performance.

Acknowledgment.--Alfred P. Sloan Foundation, Penn State Button Waller Fellowship, and reviewers al The American Midland Naturalist. Also, James D. Bever and Sidney 1.. Sturmer for taxonomic support. In addition, the generous support of David M. FCissenstat. Also, thanks to Logan W. Cole for encouragement and helpful discussions.


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RONDY J. MALIK (1), The Huck Institute of Life Sciences, Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, Pennsylvania 16802. Submitted 1 December 2017; Accepted 1 May 2018

(1) Corresponding author: e-mail;

Caption: FIG. 1.--Recent trend in taxon usage among bioprotection studies. Studies assessing plant-enemy performance were evaluated. All taxa nomenclature presented in this chart were updated according to INVAM and Mycoliank
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Title Annotation:Notes and Discussion Piece
Author:Malik, Rondy J.
Publication:The American Midland Naturalist
Date:Oct 1, 2018
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