A Genre

A Idnurm

C Zamioudis

CO Micali

CP Humphreys

D Chandran

D Redecker

E Tisserant

ET Kiers

F Maillet

G Kuhn

H Kaku

JD Jones

JM Plett

JM Smith

Joseph Heitman

KA Sedzielewska

M Chabaud

M Hijri

Nicolas Corradi

P Bonfante

Paola Bonfante

S Halary

S Kloppholz

SB Malik

SE Smith

TE Pawlowska

WJ Deakin

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PLoS Pathogens

The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection.

Bonfante, Paola

Institutional Research Information System University of Turin

PearlsThe Arbuscular Mycorrhizal Symbiosis: Origin andEvolution of a Beneficial Plant InfectionNicolas Corradi1*, Paola Bonfante21Canadian Institute for Advanced Research, Department of Biology, University of Ottawa, Ottawa, Ontario, Canada, 2Department of Life Science and Systems Biology,University of Torino, Torino, Piemonte, ItalyAn Ancient and Ecologically Critical FungalLineageArbuscular mycorrhizal fungi (AMF) represent a monophyleticfungal lineage (Glomeromycota) that benefits terrestrial ecosystemsworldwide by establishing an intimate association with the roots ofmost land plants: the mycorrhizal symbiosis. This relationshipresults in an improved acquisition of nutrients (e.g., phosphate andnitrates) from the soil by the plant partners and, in exchange,allows the AMF to obtain the photosynthetically fixed carbonsources (e.g., sugars) necessary for their survival and propagation[1,2] (Figure 1). This fungal lineage is known to impact thefunction and biodiversity of entire ecosystems by producingextensive underground networks, composed of hyphae and spores,that interconnect a number of unrelated individual plant species[1,2]. These networks also function as a significant sink foratmospheric carbon dioxide, and represent significant under-ground ‘‘nutrient highways’’ that benefit entire plant andmicrobial communities. Indeed, AMF spores and hyphae are alsoa valuable source of food for many soil microorganisms (i.e.,bacteria, other fungi, and nematodes), and because of their manybeneficial effects on terrestrial ecosystems, AMF are widely used inorganic agriculture and plant nurseries to improve the growth ofeconomically important species.Besides their enormous benefits for terrestrial ecosystemsaround the globe, AMF are also known for their atypicalevolutionary history and cellular features. For instance, it iscurrently thought that this intimate fungal–plant association hasevolved over at least 500 million years—an extremely long-termco-evolutionary history, which has led many to suggest that AMFcould have played a major role in the colonization of land byplants [3]. This hypothesis is also consistent with recent reportsdescribing the capacity of some AMF species to infect the mostancient plant lineages (e.g., liverworts) and improve their overallfitness [4].From a cellular point of view, AMF cells are at odds with thoseof many other eukaryotes, harbouring hundreds of haploid nucleiwithin one cytoplasm throughout their entire life cycle (i.e., septaare absent). The genetic structure of these co-existing nuclei hassparked a long-standing and intense scientific debate, and it iscurrently unclear whether such nuclei are genetically similar (e.g.,homokaryons) [5] or divergent (e.g., heterokaryons) [6,7].Nevertheless, it is now generally accepted by the mycorrhizalresearch community that genes isolated from one spore are oftencharacterized by an atypically high degree of intra-individualsequence polymorphism.The Elusive Genome of AMF Contains a Typical‘‘Biotrophic’’ Gene RepertoireGiven the outstanding importance of AMF for the overall healthand biodiversity of many ecosystems worldwide, one could easilyassume that the genomes of many AMF would have been alreadysequenced and would be readily available in gene depositories forcomparison and inspection. Unfortunately, however, this is farfrom being the case, and until earlier this year, sequenceinformation on AMF consisted of only two published completemitochondrial genomes and a handful of unrelated nuclear genesequences. So, why is that? Obviously, there are many causes, themost notorious being difficulties in culturing these fungi underaxenic conditions, the presence of a relatively elevated intra-individual sequence polymorphism hampering genome assemblies,and, finally, a nuclear genome size that could well be an order ofmagnitude larger than what was previously thought (e.g., mostrecent analyses suggest a genome size of around 150 megabases)[8,9].This past year, however, the field of AMF genome researchexperienced a major breakthrough with the publication of thetranscriptome of the model AMF Rhizophagus (Glomus) intraradices[10]. The gene repertoire of this AMF was found to mirror that ofother biotrophic fungi, with many genes involved in stealth hostcolonization and nutrient assimilation (e.g., metabolism ofphosphate, nitrate, and lipids). Many AMF genes were also foundto be shared exclusively with other, more diverged mycorrhizalfungi (e.g., Tuber melanosporum, an ascomycete, and Laccaria bicolor, abasidiomycete), providing long awaited insights into the origin andevolution of mycorrhiza-specific genes. The R. intraradices genomealso encodes a large number of proteins that have not beenreported in other genomes, suggesting that these have originatedand been maintained to play an essential function exclusive tothese ecologically relevant fungi [10].An Ancient Asexual Lineage with Many GenesNecessary for Sexual ReproductionAMF have long been considered to represent an ancient asexuallineage, having evolved for over 500 million years in the absence ofsexual reproduction. However, recent studies on the gene contentCitation: Corradi N, Bonfante P (2012) The Arbuscular Mycorrhizal Symbiosis:Origin and Evolution of a Beneficial Plant Infection. PLoS Pathog 8(4): e1002600.doi:10.1371/journal.ppat.1002600Editor: Joseph Heitman, Duke University Medical Center, United States ofAmericaPublished April 19, 2012Copyright:  2012 Corradi, Bonfante. This is an open-access article distributedunder the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided theoriginal author and source are credited.Funding: N.C. is a scholar of the Integrated Microbial Biodiversity program of theCanadian Institute for Advanced Research (CIFAR-IMB). This work was supportedby NSERC-Discovery grants to N.C., and P.B. was funded by a grant from theRegione Piemonte. The funders had no role in study design, data collection andanalysis, decision to publish, or preparation of the manuscript.Competing Interests: The authors have declared that no competing interestsexist.* E-mail: ncorradi@uottawa.caPLoS Pathogens | www.plospathogens.org 1 April 2012 | Volume 8 | Issue 4 | e1002600of several species have revealed that these organisms harbour abattery of genes that generally function only during sexualprocesses [10,11]. These include proteins that are known onlythrough their involvement in the process of meiosis (e.g., Spo11,Dmc1, and Rec8) [12], as well as homologues of genes that composethe mating type locus of basal fungal lineages (e.g., SexP and SexMof Mucorales) [13]. The exact function of these gene sets iscurrently unknown, and, obviously, their identification is notconclusive evidence that AMF are indeed capable of undergoingsome sort of cryptic sexuality. Nevertheless, the identification ofsex-related genes in this supposedly ancient asexual fungal lineageopens up the exciting possibility that AMF may not represent oneof the ‘‘highly exclusive’’ lineages commonly referred to as‘‘ancient asexuals’’, an artificial grouping that currently includesthe AMF, the ostracod Darwinula stevensoni, and the bdelloı¨d rotifers[14].Mycorrhizal Colonization versus PathogenicInfection: Similarities and DifferencesAs sessile organisms, plants have developed many strategies forinteracting with microbes from different kingdoms, both beneficialand pathogenic, and a relevant goal in biology is to understandwhether plant mutualists and pathogens share common molecularand cellular mechanisms for colonizing their hosts. Interestingly, anumber of recent findings appear to support this possibility. Acompelling example is represented by type III secretion systems, amolecular syringe that is used by both pathogenic and symbioticbacteria to translocate effectors (i.e., secreted molecules that alterplant processes and facilitate colonization) into host cells [15]. Theprocess for colonizing plant tissues reveals additional commonaspects that are shared between fungal plant pathogens andsymbionts. For instance, both rust fungi (pathogens) and AMF(symbionts) develop feeding structures surrounded by a membraneof host origin, and in both cases the physical separation of thefungus is complete but allows nutrient movements. In thisparticular example, sugars always flow from the plant towardsthe associated fungus, but only in the case of the AMF is the plantrewarded by a reverse flow of phosphate or nitrogen compounds[16].The cellular and molecular mechanisms underlying theconstruction of these feeding structures also share many commonaspects between fungal plant pathogens and symbionts. Thebiogenesis of the perihaustorial membrane typical of rusts requirescomplex polarized events of secretion [17] that mirror those foundin the perifungal membrane biogenesis of AMF [18]. Accordingly,the transcriptomic profiles of haustorial and arbusculated cellsshow an impressive similarity, as their changes indicate an activemetabolism in those cells directly involved in the response to theinvading fungus, irrespective of its nutritional strategy. This hasbeen shown using laser microdissection, which allows site-specificprofiling specific to host processes following both types ofinteractions. For instance, in Arabidopsis infected by Golovinomyces,genes involved in photosynthesis, cold/dehydration responses,defence, auxin signalling, and cell cycle were detected [19], whilesimilar analyses in arbusculated cells from legume plants revealedan activation of nutrient transporters, cell-wall-related genes, andtranscription factors [18]. In both cases, the data pointed towardsan enhanced plant metabolism imposed by both pathogenic andsymbiotic fungi, and to an accommodation process related to theircolonization events.Both Mycorrhizal and Pathogenic Fungi Have toCope with the Plant Immune SystemIn order to deal with pathogens, plants have developed aninnate immune system that triggers resistance mechanisms [20]. Adramatic increase in our current knowledge has originated fromthe characterization of both elicitors (or microbial-associatedmolecular patterns [MAMPs]) and effectors, the microbialmolecules that initiate effector-triggered immunity [20]. Chitin isone of the best known fungal elicitors, and many chitin receptorshave been identified as key regulators of plant responses [21]. Inthe case of AMF, it is quite interesting to observe that AMF releasediffusible molecules that activate a range of responses in the hostplant [22], and lipochitooligosaccharides have been recognized asone of these crucial elicitors [23]. The development of genomicFigure 1. Establishment of the mycorrhizal symbiosis. An AMF contacts the surface of a legume root, by producing swollen structures calledhyphopodia (in yellow) (A). Evident defence reactions are not detectable, and the epidermal cells appear alive, with the nuclei visible as blue spots.Once inside the root, the AMF colonizes the inner cortical cells, producing highly branched structures called arbuscules. Notwithstanding the massivecolonization, the plant cells remain alive (B). Pictures kindly provided by Andrea Genre and Mara Novero, University of Torino.doi:10.1371/journal.ppat.1002600.g001PLoS Pathogens | www.plospathogens.org 2 April 2012 | Volume 8 | Issue 4 | e1002600sequencing projects for mycorrhizal fungi has opened unexpectedpossibilities: not only pathogenic fungi, but also mycorrhizal fungiproduce effectors; as virulence factors they reach the host nucleusand activate different responses [24,25]. These recent discoveriesunderpin how ecologically different organisms (e.g., pathogensversus symbionts) can use a very similar vocabulary during theirdialogue with the host, suggesting that some of the determinantsidentified as modulators of host immunity are probably commonto both types of associations [26].AcknowledgmentsWe would like thank Risa Sargent for useful comments on a previousversion of the manuscript.References1. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungusinteractions in mycorrhizal symbiosis. Nat Commun 1: 48.2. Smith SE, Read DJ, Harley JL (1997) Mycorrhizal symbiosis. San Diego(California): Academic Press. 605 p.3. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from theOrdovician. Science 289: 1920–1921.4. Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, et al. (2010)Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants.Nat Commun 1: 103.5. Pawlowska TE, Taylor JW (2004) Organization of genetic variation inindividuals of arbuscular mycorrhizal fungi. Nature 427: 733–737.6. Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscularmycorrhizal fungi inherit genetically different nuclei. Nature 433: 160–163.7. Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiplegenomes in arbuscular mycorrhizal fungi. Nature 414: 745–748.8. Sedzielewska KA, Fuchs J, Temsch EM, Baronian K, Watzke R, et al. (2011)Estimation of the Glomus intraradices nuclear DNA content. New Phytol 192:794–797.9. Hijri M, Sanders IR (2004) The arbuscular mycorrhizal fungus Glomus intraradicesis haploid and has a small genome size in the lower limit of eukaryotes. FungalGenet Biol 41: 253–261.10. Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, et al.(2011) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices(DAOM 197198) reveals functional tradeoffs in an obligate symbiont. NewPhytol 193: 755–769.11. Halary S, Malik SB, Lildhar L, Slamovits CH, Hijri M, et al. (2011) Conservedmeiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage.Genome Biol Evol 3: 950–958.12. Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM (2008) Anexpanded inventory of conserved meiotic genes provides evidence for sex inTrichomonas vaginalis. PLoS ONE 3: e2879. doi:10.1371/journal.pone.0002879.13. Idnurm A, Walton FJ, Floyd A, Heitman J (2008) Identification of the sex genesin an early diverged fungus. Nature 451: 193–196.14. Smith JM (1986) Evolution—contemplating life without sex. Nature 324:300–301.15. Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies:rhizobial protein secretion systems. Nat Rev Microbiol 7: 312–320.16. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, et al. (2011)Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science333: 880–882.17. Micali CO, Neumann U, Grunewald D, Panstruga R, O’Connell R (2011)Biogenesis of a specialized plant-fungal interface during host cell internalizationof Golovinomyces orontii haustoria. Cell Microbiol 13: 210–226.18. Genre A, Ivanov S, Fendrych M, Faccio A, Zarsky V, et al. (2012) Multipleexocytotic markers accumulate at the sites of perifungal membrane biogenesis inarbuscular mycorrhizas. Plant Cell Physiol 53: 244–255.19. Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC (2009) Lasermicrodissection of Arabidopsis cells at the powdery mildew infection site revealssite-specific processes and regulators. Proc Natl Acad Sci U S A 107: 460–465.20. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323–329.21. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N,et al. (2006) Plant cells recognize chitin fragments for defense signaling through aplasma membrane receptor. Proc Natl Acad Sci U S A 103: 11086–11091.22. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, et al. (2011)Arbuscular mycorrhizal hyphopodia and germinated spore exudates triggerCa2+ spiking in the legume and nonlegume root epidermis. New Phytol 189:347–355.23. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, et al. (2011) Fungallipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63.24. Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, et al. (2011) A secretedeffector protein of Laccaria bicolor is required for symbiosis development. CurrBiol 21: 1197–1203.25. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomusintraradices promotes symbiotic biotrophy. Curr Biol 21: 1204–1209.26. Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficialmicrobes. Mol Plant Microbe Interact 25: 139–150.PLoS Pathogens | www.plospathogens.org 3 April 2012 | Volume 8 | Issue 4 | e1002600

The arbuscular mycorrhizal symbiosis: Origin and evolution of a beneficial plant infection

Crossref

The Arbuscular Mycorrhizal Symbiosis: Origin and Evolution of a Beneficial Plant Infection

A secreted effector protein of Laccaria bicolor is required for symbiosis development.

A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy.

An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis.

Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis.

Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria.

Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage.

Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi.

Evolution—contemplating life without sex.

Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.

Genre A

Identification of the sex genes in an early diverged fungus.

Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators.

Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei.

Modulation of host immunity by beneficial microbes.

Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas.

Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants.

Mycorrhizal symbiosis.

Organization of genetic variation in individuals of arbuscular mycorrhizal fungi.

Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor.

Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis.

Symbiotic use of pathogenic strategies: rhizobial protein secretion systems.

The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has a small genome size in the lower limit of eukaryotes.

The plant immune system.

The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont.

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The Arbuscular Mycorrhizal Symbiosis: Origin and Evolution of a Beneficial Plant Infection

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