Printer Friendly

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

INTRODUCTION

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.

RECENT TRENDS IN TAXON USAGE

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.

SYNTHESIS

PLANT HORMONAL RESPONSE TO PLANT-THROPS

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.

PLANT ENEMY RESPONSE PARAMETERS

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.

WHAT MAY HE EXPLAINING TAXON USAGE?

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.

LITERATURE CITED

Ali, J. G. and A. A. Agrawal. 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci., 17:293-302.

Bennett, A. E., J. Alers-Garcia, and J.D. Bever. 2006. Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am. Nat., 167:141-152.

--and J.D. Bever. 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology, 88:210-218.

--, N.S. Millar, E. Gedrovics, and A.J. Karley. 2016. Plant and insect microbial symbionts alter the outcome of plant-herbivore--parasitoid interactions: implications for invaded, agricultural and natural systems. J. Ecol., 104:1734-1744.

Bever, J. D., P.A. Schultz, A. Pringle, and J.B. Morton. 2001. Arbuscular Mycorrhizal Fungi: More Diverse than Meets the Eye, and the Ecological Tale of Why. Bioscience, 51:923.

Blee, K. A. and A.J. Anderson. 1998. Regulation of arbuscule formation by carbon in the plant. Plant J., 16:523-530.

Bonfante-Fasolo, P., A. Faccio, S. Perotto, and A. Schubert. 1990. Correlation between chitin distribution and cell wall morphology in the mycorrhizal fungus Glomus versiforme. Mycol. Res., 94:157-165.

Campos-Soriano, L., J. Garcia-Martinez, and B. San Segundo. 2012. The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol. Plant Pathol., 13:579-592.

Cordier, G, M. J. Pozo, J. M. Barea, S. Gianinazzi, and V. Gianinazzi-Pearson. 1998. (Cell Defense Responses Associated with Localized and Systemic Resistance to Phytophthora parasiticalnduced in Tomato by an Arbuscular Mycorrhizal Fungus. Mol. Plant Microbe In., 11.

Der Ent, V. S., S.C.M. Wees, and C.M.J. Pieterse. 2009. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Photochemistry, 70:1581-1588.

Duchicela, A. J., T.S. Sullivan, E. Bontti, J.D. Bever, and S. Wan. 20ES. Soil aggregate stability increase is strongly related to fungal community succession along an abandoned agricultural field chronosequence in the Bolivian Altiplano. J. Appl. Ecol., 50:1266-1273.

Engelmoer, D.J. P., J.E. Behm, and E.T. Kiers. 2014. Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mole. Ecol., 23:1584-1593.

Feng, G., F. Zhang, X. Li, C. Tian, G. Tang, and Z. Rengel. 2002. Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza, 12:185-190.

Frew, A., J.R. Powell, I. Hiltpold, P.G. Allsopp, N. Sallam, and S.N. Johnson. 2017. Host plant colonisation by arbuscular mycorrhizal fungi stimulates immune function whereas high root silicon concentrations diminish growth in a soil-dwelling herbivore. Soil Biol. Biochem., 112:117-126.

Genre, A. M., M. Chabaud, A. Faccio. D.G. Barker, and P. Boneante. 2008. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncalula and Daucus carota. Plant Cell, 20:1407-1420.

Gianinazzi-Pearson, V., E. Du-Gaudot, A. Gollotte, T.A. Alaoui, and S. Gianinazzi. 1996. Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol, 133:45-57.

Harrison, M. J. 1998. Development of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol, 1:360-365.

--. 2004. Signaling in the arbuscular mycorrhizal symbiosis. Annul. Rev. Microbiol., 59:19-42.

Heidel, A.J. and I.T. Baldwin. 2004. Microarray analysis of salicylic acid- andjasinonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant, Cell, Environ., 27:1362-1373.

Helgason, T., T.J. Daniell, R. Husband, A.H. Fitter, and J.P.W. Young. 1998. Ploughing up the woodwide web? Nature, 394:431.

Hodge, A., C.D. Campbell, and A.H. Fitter. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 413:297-299.

Jakobsen, L, L. Abbott, and A. Robson. 1992. External hyphae of vesicular-aibuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol., 120:371-380.

--and L. Rosendahl. 1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol., 115:77-83.

Jie, W., L. Bai, W. Yu, and B. Cal 2015. Analysis of interspecific relationships between Funneliformismosseae and Fusarium oxysporum in the continuous cropping of soybean rhizosphere soil during the branching period. Bioconlrol Sci. lech.. 25, 1036-1051.

Jones, J.D. and J.L. Dangl, 2006. The plant immune system. Nature, 444:323-329.

Jung, S. C., A. Martinez-Medina, J.A. Lopez-Raez, and M.J. Pozo. 2012. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol., 38:651-664.

Korigheva, J., A.C. Gange, and T. Jones. 2009. Effects of mycorrhizal fungi on insect herbivores: a meta analysis. Ecology, 90:2088-2097.

Lenardon, M. D., C.A. Munro, and N.A. Gow. 2010. Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol., 13:416-423.

Malik, R. J., M.H. Dixon, and J.D. Bever. 2016. Mycorrhizal composition can predict foliar pathogen colonization in soybean. Biol. Control. 103:46-53.

Mathimaran N., R. Ruh, P. Vullioud, E. Frossard, and J. Jansa. 2005. Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza, 16:61-66.

Middleton, E. L., S. Richardson, E. Kozto, C.E. Palmer, Z. Yermakov, J.A. Henning, P.A. Schultz, and J.D. Bever. 2015. Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere, 6:1-16.

Oehl, F., E. Sieverding, J. Palenzuela, and K. Ineichen. 2011. Advances in Glomeromycota taxonomy and classification. IMA fungus, 2:191-199.

Pena, D. K. and S.R. Echeverria. 2006. Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Anmiophila arenaria. New Phytol., 169:829-810.

Pieterse, C. M., C. Zamioudis, R.L. Berendsen, D.M. Weller, S.V.. Van Wees, and P.A. Barker. 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol., 52:347-375.

Pozo, M. J., and C. Azcon-Aguilar. 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol., 10:393-398.

--, C. (Cordier, E. Dumas-Gaudot, S. Gianinazzi, J.M. Barea, and C. Azcon-Aguilar. 2002. Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot., 53:525-534.

Prieto, J. D., C. Castane, C. Calvet, A. Camprubi, D. Battaglia, V. Trotta, and P. Fanti. 2016. Tomato belowground--aboveground interactions: Rhizophagus irregularis affects foraging behavior and life history traits of the predator Macrolophus pygmaeus (Hemiptera: Miridae). Arthropod-Plant Inte., 1-8.

Qian, L., W.J. Yu, J. Q. Cut, W. G. Jie, and B.Y. Gal 2015. Funneliformis mosseae affects the root rot pathogen Fusarium oxysporum in soybeans. Arta Agrie. Stand. B., 65:321-328.

Redecker, D., A. Schubler, H. Stockinger, S.L. Sturmer, J.B. Morton, and G Walker. 2013. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Myrorrhiza, 23:515-531.

Ronsheim, M. L. 2016. Plant Genotype Influences Mycorrhiza Benefits and Susceptibility to a Soil Pathogen. Am. Midi. Nal., 175:103-112.

Rosendahl, S., P. McGee, and J. B. Morton. 2009. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mole, ecol., 18:4316-4329.

Sanders, F. F. and B. P. Tinker. 1973. Phosphate flow into mycorrhizal roots. Pesticide Sci., 4:385-395.

Schubler, A., D. Schwarzott, and C. Walker. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution** Dedicated to Manfred Kluge (Technische Universitat Darmstadt) on the occasion of his retirement. Mycol. Res., 105:1413-1421.

Spoel, S. H. and X. Dono. 2008. Making sense of hormone crosstalk during plant immune responses. Oil Host Microbe, 3:348-351.

Sundram, S., S. Meon, L.A. Seman, and R. Othman. 2015. Application of arbuscular mycorrhizal fungi with Pseudomonas aeruginosa UPMP3 reduces the development of Ganoderma basal stem rot disease in oil palm seedlings. Mycorrhiza, 25:387-397.

Sutter, R. and C. Muller. 2011. Mining for treatment-specific and general changes in target compounds and metabolic fingerprints in response to herbivory and phytohormones in Plantago lanceolata. Neto Phytol., 191:1069-1082.

Van Wees, S. G., S. Van Der Ent, and O.M. Pif.ter.se. 2008. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol., 11:443-448.

Wang, E., N. Yu, S.A. Bano, G. Lit, A.J. D. Miller, X. Got sins, X. Zhang, P. Ratet, Tadege, M. S. Mysore, J.A. Downie, J.D. Murray, G.E. Oldroyd, and M. Schultze. 2014. A H+-ATPase That Energizes Nutrient Uptake during Mycorrhizal Symbioses in Rice and Medicago truncatula. Plant Cell, 26:1818-1830.

Zipfel, C. 2014. Plant pattern-recognition receptors. Trends Immunol., 35:345-351.

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; rjm472@psu.edu

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
COPYRIGHT 2018 University of Notre Dame, Department of Biological Sciences
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Notes and Discussion Piece
Author:Malik, Rondy J.
Publication:The American Midland Naturalist
Date:Oct 1, 2018
Words:3301
Previous Article:Distribution of Sisyridae and Freshwater Sponges in the upper-Susquehanna Watershed, Otsego County, New York with a New Locality for Climacia...
Next Article:Seed Dispersal in Osage Orange (Maelura pomifera) by Squirrels (Sciurus spp.).
Topics:

Terms of use | Privacy policy | Copyright © 2020 Farlex, Inc. | Feedback | For webmasters