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      Host specialisation and disparate evolution of Pyrenophora teres f. teres on barley and barley grass

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          Abstract

          Background

          Pathogens evolve in an arms race, frequently evolving virulence that defeats resistance genes in their hosts. Infection of multiple hosts may accelerate this virulence evolution. Theory predicts that host diversity affects pathogen diversity, with more diverse hosts expected to harbour more diverse pathogens that reproduce sexually. We tested this hypothesis by comparing the microsatellite (SSR) genetic diversity of the barley leaf pathogen Pyrenophora teres f. teres (Ptt) from barley (monoculture) and barley grass (outbreeding). We also aim to investigate host specificity and attempt to track virulence on two barley cultivars, Maritime and Keel.

          Results

          Genetic diversity in barley Ptt populations was higher than in populations from barley grass. Barley Ptt populations also had higher linkage disequilibrium levels, indicating less frequent sexual reproduction, consistent with the Red Queen hypothesis theory that genetically diverse hosts should select for higher levels of sexual reproduction of the pathogen. SSR analyses indicate that host-associated Ptt populations do not share genotypes and have independent evolutionary histories. Pathogenicity studies showed host specificity as host-associated Ptt isolates could not cross-infect hosts. Minimum spanning network analyses indicated two major clusters of barley Ptt. One cluster represents Maritime virulent and isolates from Western Australia (WA). Low PhiPt population differentiation between WA populations and those from Maritime and Keel, indicated a WA origin of the Maritime and Keel virulences. The main minimum spanning network cluster is represented by a panmictic population structure, represented by isolates from all over Australia.

          Conclusions

          Although barley Ptt populations are more diverse than barley grass Ptt populations, this may be a result of the size and number of founder Ptt populations to Australia, with larger and more barley Ptt populations introduced. More frequent sexual reproduction of Ptt on barley grass support the Red Queen Hypothesis and suggest evolutionary potential of pathogens on diverse hosts are high. Extensive gene flow of Ptt between regions in Australia is suggested to maintain a panmictic population structure, with human-mediated dispersal aiding in virulence evolution of Ptt on barley.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-019-1446-8) contains supplementary material, which is available to authorized users.

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          Most cited references55

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          Estimation of average heterozygosity and genetic distance from a small number of individuals.

          M Nei (1978)
          The magnitudes of the systematic biases involved in sample heterozygosity and sample genetic distances are evaluated, and formulae for obtaining unbiased estimates of average heterozygosity and genetic distance are developed. It is also shown that the number of individuals to be used for estimating average heterozygosity can be very small if a large number of loci are studied and the average heterozygosity is low. The number of individuals to be used for estimating genetic distance can also be very small if the genetic distance is large and the average heterozygosity of the two species compared is low.
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            Pathogen population genetics, evolutionary potential, and durable resistance.

            We hypothesize that the evolutionary potential of a pathogen population is reflected in its population genetic structure. Pathogen populations with a high evolutionary potential are more likely to overcome genetic resistance than pathogen populations with a low evolutionary potential. We propose a flexible framework to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. According to this framework, pathogens that pose the greatest risk of breaking down resistance genes have a mixed reproduction system, a high potential for genotype flow, large effective population sizes, and high mutation rates. The lowest risk pathogens are those with strict asexual reproduction, low potential for gene flow, small effective population sizes, and low mutation rates. We present examples of high-risk and low-risk pathogens. We propose general guidelines for a rational approach to breed durable resistance according to the evolutionary potential of the pathogen.
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              Population biology of multihost pathogens.

              The majority of pathogens, including many of medical and veterinary importance, can infect more than one species of host. Population biology has yet to explain why perceived evolutionary advantages of pathogen specialization are, in practice, outweighed by those of generalization. Factors that predispose pathogens to generalism include high levels of genetic diversity and abundant opportunities for cross-species transmission, and the taxonomic distributions of generalists and specialists appear to reflect these factors. Generalism also has consequences for the evolution of virulence and for pathogen epidemiology, making both much less predictable. The evolutionary advantages and disadvantages of generalism are so finely balanced that even closely related pathogens can have very different host range sizes.
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                Author and article information

                Contributors
                celeste.linde@anu.edu.au
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                8 July 2019
                8 July 2019
                2019
                : 19
                : 139
                Affiliations
                ISNI 0000 0001 2180 7477, GRID grid.1001.0, Division of Ecology and Evolution, Research School of Biology, ANU College of Science, , The Australian National University, ; RN Robertson Building, 46 Sullivans Creek Road, Canberra, ACT 2600 Australia
                Author information
                http://orcid.org/0000-0002-8207-1202
                Article
                1446
                10.1186/s12862-019-1446-8
                6615293
                31286867
                2c22aaf9-68f9-4b2e-ba65-0599607a0157
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 17 August 2018
                : 27 May 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100008584, Grain Research and Development Corporation;
                Award ID: DAQ00178
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000980, Grains Research and Development Corporation;
                Award ID: DAQ00187
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Evolutionary Biology
                host specificity,virulence evolution,pathogen,genetic diversity,sexual reproduction

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