Heterokaryon formation and vegetative compatibility in Sclerotinia sclerotiorum

Ford, Eugene; Miller, Russell; GRaY, H.; Sherwood, John E.

doi:10.1016/s0953-7562(09)80893-9

Cited by 54 publications

(48 citation statements)

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“…However, the majority of the isolates were mycelially incompatible, likely minimizing the possibility of heterokaryon formation and mitotic recombination in nature that is rare (Clutterbuck, 1996). Heterokaryon formation has been reported only in laboratory conditions for S. sclerotiorum (Ford et al, 1995). All isolates in this study showed single alleles for each and every locus, suggesting the isolates are homokaryotic at least for the loci concerned.…”

Section: Discussionmentioning

confidence: 66%

“…Sexton et al (2006) suggested the possibility of formation of heterokaryotic sclerotia when the disease pressure is high and simultaneous coinfections might occur, producing sclerotia with multiple genotypes facilitating outcrossing. Indeed, outcrossing was observed in forced heterokaryonic sclerotia of S. sclerotiorum (Ford et al, 1995). Ekins et al (2006) observed ascospore dimorphism in S. sclerotiorum, reminiscent to the morphological feature found in the heterothallic species S. trifoliorum.…”

Section: Discussionmentioning

confidence: 86%

“…However, studies using independent microsatellite markers found high genotypic diversity, discordance between multilocus haplotypes and MCGs and random association of alleles, and inferred occurrence of recombination, implicitly outcrossing, in S. sclerotiorum populations in potato fields in Washington State, USA (Atallah et al, 2004), bean fields in Brazil (Gomes et al, 2011) and canola fields in Australia (Sexton et al, 2006), Turkey (Mert-Turk et al, 2007), Iran (Hemmati et al, 2009), China and United States (Attanayake et al, 2013). As parasexuality in S. sclerotiorum has been shown only once under laboratory conditions (Ford et al, 1995), outcrossing is supposed to play a key role in generating recombinant genotypes.…”

Section: Introductionmentioning

confidence: 99%

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Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay

et al. 2014

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The occurrence and frequency of outcrossing in homothallic fungal species in nature is an unresolved question. Here we report detection of frequent outcrossing in the homothallic fungus Sclerotinia sclerotiorum. In using multilocus linkage disequilibrium (LD) to infer recombination among microsatellite alleles, high mutation rates confound the estimates of recombination. To distinguish high mutation rates from recombination to infer outcrossing, 8 population samples comprising 268 S. sclerotiorum isolates from widely distributed agricultural fields were genotyped for 12 microsatellite markers, resulting in multiple polymorphic markers on three chromosomes. Each isolate was homokaryotic for the 12 loci. Pairwise LD was estimated using three methods: Fisher's exact test, index of association (I A ) and Hedrick's D 0 . For most of the populations, pairwise LD decayed with increasing physical distance between loci in two of the three chromosomes. Therefore, the observed recombination of alleles cannot be simply attributed to mutation alone. Different recombination rates in various DNA regions (recombination hot/ cold spots) and different evolutionary histories of the populations could explain the observed differences in rates of LD decay among the chromosomes and among populations. The majority of the isolates exhibited mycelial incompatibility, minimizing the possibility of heterokaryon formation and mitotic recombination. Thus, the observed high intrachromosomal recombination is due to meiotic recombination, suggesting frequent outcrossing in these populations, supporting the view that homothallism favors universal compatibility of gametes instead of traditionally believed haploid selfing in S. sclerotiorum. Frequent outcrossing facilitates emergence and spread of new traits such as fungicide resistance, increasing difficulties in managing Sclerotinia diseases.

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Section: Discussionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 86%

Section: Introductionmentioning

confidence: 99%

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Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay

et al. 2014

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“…For example mutants such as Neurospora crassa Pk-1 and Pk-4 produce abnormal asci in crosses with wild type strains, even when the mutant is used as the male parent and does not contribute any maternal tissue (17,18). Different asci will contain genetically different sets of nuclei if the female parent mates with multiple male partners (19) or if either parent contains genetically different nuclei (20,21), because each ascus is produced by karygamy of a different pair of parental nuclei (22).…”

Section: Resultsmentioning

confidence: 99%

Dispersal of fungal spores on a cooperatively generated wind

Roper

Seminara²,

Bandi³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Because of their microscopic size, the forcibly ejected spores of ascomycete fungi are quickly brought to rest by drag. Nonetheless some apothecial species, including the pathogen Sclerotinia sclerotiorum, disperse with astonishing rapidity between ephemeral habitats. Here we show that by synchronizing the ejection of thousands of spores, these fungi create a flow of air that carries spores through the nearly still air surrounding the apothecium, around intervening obstacles, and to atmospheric currents and new infection sites. High-speed imaging shows that synchronization is self-organized and likely triggered by mechanical stresses. Although many spores are sacrificed to produce the favorable airflow, creating the potential for conflict among spores, the geometry of the spore jet physically targets benefits of the airflow to spores that cooperate maximally in its production. The ability to manipulate a local fluid environment to enhance spore dispersal is a previously overlooked feature of the biology of fungal pathogens, and almost certainly shapes the virulence of species including S. sclerotiorum. Synchronous spore ejection may also provide a model for the evolution of stable, self-organized behaviors.hydrodynamics | cooperation | fungal spores T he forcible launch of sexual spores into dispersive air flows enables ascomycete fungi to propagate between physically distant patches of habitat; for example, the pathogen Sclerotinia sclerotiorum disperses from apothecia in the ground to infect the flowers of crop plants (1), and dung fungi in the genus Ascobolus must escape from their dung piles to be ingested by animals (2, 3). Although their microscopic size enables spores to be transported by even slow flows of air, it also severely limits the distance that they may travel ballistically. Launched at a speed of 8.4 m·s −1 , the 12 μm long spores of S. sclerotiorum would be decelerated to rest after traveling less than 3 mm (4, 5). In response to this constraint, fungi have evolved multiple adaptations to maximize spore range. For example, spores that cohere during launch benefit from increased inertia (6), while individually ejected spores may be shaped in order to minimize drag (5).Here we demonstrate the remarkable ability of apothecial fungi to manipulate their own fluid environment and negate the range constraints imposed by fluid drag. It has long been known (7,8) that in many species spore discharge is almost synchronous between the asci of an individual apothecium, so that hundreds, thousands, or tens of thousands of spores can be discharged in a single puff, lasting a fraction of a second (Fig. 1 A, B). Discharge may be initiated spontaneously, or by changes in air pressure, or when an apothecium is touched. Buller (9) first connected spore coejection with the creation of a flow of air. In this work we adapt algorithms originally developed to simulate hundreds of thousands of droplets in clouds to prove that the hydrodynamic cooperation of spores creates a flow of air. Our simulations, analytic models,...

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“…An example of such behavior is found in the ascomycete fungus Rossellinia necatrix , and it appears to be triggered by a single Mendelian factor . Although there is increasing evidence of similar behavior across fungi (Ford et al 1995;Giovannetti et al 2003;Micali and Smith 2003;Iotti et al 2012;Smith and Lafontaine 2013), there is only one example where a gene has been isolated. This example is the vic4 gene of the chestnut blight fungus Cryphonectria parasitica (Ascomycota).…”

Section: Stage Of Rejectionmentioning

confidence: 99%

Histocompatibility as Adaptive Response to Discriminatory Within-Organism Conflict: A Historical Model

Gilbert

2015

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Online enhancement: appendix.abstract: Multicellular tissue compatibility, or histocompatibility, restricts fusion to close kin. Histocompatibility depends on hypervariable cue genes, which often have more than 100 alleles in a population. To explain the evolution of histocompatibility, I here take a historical approach. I focus on the specific example of marine invertebrate histocompatibility. I use simple game-theoretical models to show that histocompatibility can evolve through five steps. These steps include the evolution of indiscriminate fusion, the evolution of discriminatory within-organism conflict, the evolution of minor histocompatibility, the evolution of major histocompatibility, and the evolution of major histocompatibility cue polymorphism. Allowing for gradual evolution reveals discriminatory within-organism conflict as a selective pressure for histocompatibility and associated cue polymorphism. Existing data from marine invertebrates and other organisms are consistent with this hypothesis.

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Heterokaryon formation and vegetative compatibility in Sclerotinia sclerotiorum

Cited by 54 publications

References 27 publications

Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay

Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay

Dispersal of fungal spores on a cooperatively generated wind

Histocompatibility as Adaptive Response to Discriminatory Within-Organism Conflict: A Historical Model

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