Field‐based experimental evolution of three cereal pathogens using a mark–release–recapture strategy

Zhan, Jiasui; McDonald, Bruce A.

doi:10.1111/ppa.12130

Cited by 28 publications

(27 citation statements)

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“…"Mark-release-recapture" experiments based on artificial inoculations were performed with fungal pathogens of wheat, including Z. tritici (15,35,40,41; see also the reviews by Zhan and McDonald [16,17]). Under natural conditions, given the high diversity of Z. tritici populations (20), the earliest cohort of lesions is caused by different genotypes, and the probability of recapturing one of them on the upper leaves at the end of the epidemic is almost zero.…”

Section: Discussionmentioning

confidence: 99%

“…Fungal development is temperature dependent (13,14), so that seasonal fluctuations, which are suspected to constitute shortterm selection pressure for fitness traits, might modify the dynamic of annual epidemics even within a year. Moreover, several infection cycles can amplify short-term selection pressure due to competition between pathogen strains (15)(16)(17).…”

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confidence: 99%

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Seasonal Changes Drive Short-Term Selection for Fitness Traits in the Wheat Pathogen Zymoseptoria tritici

Suffert

Ravigné

Sache

2015

Appl Environ Microbiol

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cIn a cross-infection experiment, we investigated how seasonal changes can affect adaptation patterns in a Zymoseptoria tritici population. The fitness of isolates sampled on wheat leaves at the beginning and at the end of a field epidemic was assessed under environmental conditions (temperature and host stage) to which the local pathogen population was successively exposed. Isolates of the final population were more aggressive, and showed greater sporulation intensity under winter conditions and a shorter latency period (earlier sporulation) under spring conditions, than isolates of the initial population. These differences, complemented by lower between-genotype variability in the final population, exhibited an adaptation pattern with three striking features: (i) the pathogen responded synchronously to temperature and host stage conditions; (ii) the adaptation concerned two key fitness traits; (iii) adaptation to one trait (greater sporulation intensity) was expressed under winter conditions while, subsequently, adaptation to the other trait (shorter latency period) was expressed under spring conditions. This can be interpreted as the result of short-term selection, driven by abiotic and biotic factors. This case study cannot yet be generalized but suggests that seasonality may play an important role in shaping the variability of fitness traits. These results further raise the question of possible counterselection during the interepidemic period. While we did not find any trade-off between clonal multiplication on leaves during the epidemic period and clonal spore production on debris, we suggest that final populations could be counterselected by an Allee effect, mitigating the potential impact of seasonal selection on long-term dynamics.T hermal variation, including seasonal fluctuations and also climate change, appears to be one of the main drivers of the predicted change in plant disease distributions (1-3). The adaptive response of plant pathogens to thermal variations may involve the movement of pathogen populations, as well as phenotypic plasticity and selection, so that full characterization requires extensive measurements of fitness traits under various environmental conditions. How the seasonality of disease development (e.g., the duration of the epidemic and interepidemic periods, through modifications of the biotic and abiotic environment) will be modified by climate change is a question increasingly addressed in the literature (4-6). In contrast, how seasonal climate variation within a year currently affects the dynamics of pathogen populations has received less attention. However, this knowledge would be very useful for characterizing the potential effects of warming on future population dynamics. Indeed, the effects of seasonal variation are measurable at this time and offer very interesting prospects for experimentation. Investigation of such current effects of seasonality is particularly interesting because they might induce shortterm selection in the fitness traits of pathogen populations that...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Seasonal Changes Drive Short-Term Selection for Fitness Traits in the Wheat Pathogen Zymoseptoria tritici

Suffert

Ravigné

Sache

2015

Appl Environ Microbiol

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“…Adding more host cultivars or species and more fungicides would quickly increase the degree of diversity that confronts the pathogen population at the field scale where most pathogen evolution occurs (figure 1). Other approaches to increasing genetic diversity through plant breeding strategies [69] or through physical mixing of different cultivars or isogenic lines carrying different R-genes have already been thoroughly described and shown to lower disease [80] as well as to slow pathogen evolution [81].…”

Section: Example 4: Rapid Global Dissemination Of New Clones Carryingmentioning

confidence: 99%

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

McDonald

Stukenbrock

2016

Phil. Trans. R. Soc. B

274

199

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Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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“…Mark-release-recapture experiments have been reported for the wheat pathogen Phaeosphaeria nodorum (Bennet et al 2007;Shah et al 1995) and other pathogens (Zhan and McDonald 2013). The development and validation of selectively neutral, codominant and highly polymorphic molecular markers for R. solani AG 3-PT (Ceresini et al 2002) offers practical feasibility of tagging and tracking R. solani AG 3-PT genotypes across generations in a mark-release-recapture experiment.…”

Section: Introductionmentioning

confidence: 99%

“…The increase in the array of molecular techniques and computing technologies, offers endless possibilities of conducting mark-release-recapture experiments that allow tracking of inoculum sources during disease development and thus determines the inoculum origin (Bardin et al 2014;Sommerhalder et al 2010;Zhan et al 1998;Zhan and McDonald 2013). Mark-release-recapture experiments have been reported for the wheat pathogen Phaeosphaeria nodorum (Bennet et al 2007;Shah et al 1995) and other pathogens (Zhan and McDonald 2013).…”

Section: Introductionmentioning

confidence: 99%

Relative Contribution of Seed Tuber- and Soilborne Inoculum to Potato Disease Development and Changes in the Population Genetic Structure of Rhizoctonia solani AG 3-PT under Field Conditions in South Africa

et al. 2018

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Understanding the contribution of seed tuber-and soil-borne inocula of Rhizoctonia solani AG 3-PT in causing potato disease epidemics is an important step in implementing effective management strategies for the pathogen. A two-year study was conducted to evaluate the contribution of each source of inoculum using an integrative experimental approach combining field trials and molecular techniques. Two distinct sets of genetically-marked isolates were used as seed tuber-borne and soil-borne inocula in a mark-release-recapture experiment. Disease assessments were done during tuber initiation and at tuber harvest Both inoculuma sources were found to be equally important in causing black scurf disease, whereas soil-borne inocula appeared to be more important for root and stolon infection, and seed-borne inocula contributed more to stem canker. However, seed tuber transmitted genotypes accounted for 60% of the total recovered isolates when genotyped using three PCR-RFLP markers. The changes in population structure of the experimental 1 R. solani population over the course of the growing season and across two growing seasons were investigated using eight microsatellite markers. The populations at different sampling times were somewhat genetically differentiated as indicated by Nei's gene diversity (0.24 -0.27) and the fixation index (F ST ) . The proportion of isolates with genotypes that differed from the inoculants ranged from 13% to 16% in 2013 and 2014, respectively, suggesting the possibility of emergence of new genotypes in the field. Because both soilborne and tuber-borne inocula are critical, it is important to ensure the use of pathogen-free seed tubers to eliminate seed tuber-borne inoculum and the introduction of new genotypes of R. solani for sustainable potato production in South Africa.

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Field‐based experimental evolution of three cereal pathogens using a mark–release–recapture strategy

Cited by 28 publications

References 92 publications

Seasonal Changes Drive Short-Term Selection for Fitness Traits in the Wheat Pathogen Zymoseptoria tritici

Seasonal Changes Drive Short-Term Selection for Fitness Traits in the Wheat Pathogen Zymoseptoria tritici

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

Relative Contribution of Seed Tuber- and Soilborne Inoculum to Potato Disease Development and Changes in the Population Genetic Structure of Rhizoctonia solani AG 3-PT under Field Conditions in South Africa

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