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    Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer.

    In the meantime, to ensure continued support, we are displaying nq site without styles and JavaScript. Help us improve our products. Sign up to take part. A Nature Research Journal. Reproductive mode can impact population genetic dynamics and evolutionary landscape of plant pathogens as well as on disease epidemiology and management.

    Consistent with the expectation of asexual species, identical genotypes were recovered from different locations separated by hundreds of kilometers of geographic distance and spanned across many years. However, high genotype diversity, equal MAT and MAT frequencies within and among populations, no genetic differentiation and phylogenetic association between two mating types, combined with random association amongst neutral markers in some field populations, suggested that sexual reproduction may also play an important role in the epidemics and evolution of the pathogen in at least half of the populations assayed despite the fact that no teleomorphs have been observed yet naturally or artificially.

    Our results indicated that A. Reproductive mode can have profound effects on epidemiological landscapes, population genetic dynamics, evolutionary trajectory and management mah pathogens 12 through its impacts, directly or indirectly, on the survival of spores in hazardous environments 3dispersal ability of the species 45generation, maintenance and distribution of genetic variation 6 and efficiency of selection against unnecessary genes 78.

    Pathogenic fungi have developed a wide array of reproductive strategies including asexual reproduction, sexual reproduction and parasexual reproduction to transmit their genetic materials in natural populations 4. Sexual reproduction can also increase the efficiency of natural selection against undesired alleles such as unnecessary virulence factors which may be locked mwt the genome of asexual species by hitchhiking Furthermore, sexual fruiting bodies of many pathogens are stress tolerant and can survive for a long time under severe conditions such as climate extremities mat the absence of hosts.

    If the sexual progenies are wind dispersed such as sexual spores maat by many ascomycetes, long-distance gene flow is likely to occur. Increases in genetic variation, gene flow potential and efficiency of selection against undesired alleles of sexual pathogens enhance their ability to evolve rapidly sxe response sex the change of management strategies such as the deployment of resistant cultivars and the application of fungicides. Sexual reproduction in fungi is usually triggered by mat stresses or nutrition deficiency 14 and often occurs off-season when primary hosts are not maf 3.

    Therefore, direct observation of the sexual stage in their life cycle is difficult for many facultative parasitic fungi, particularly for those that sex be crossed in laboratory conditions. In such cases, population genetic analysis of spatial dynamics in selective neutral markers and mating type genes can be a powerful approach to uncover cryptic sex in plant pathogenic fungal populations 1516171819 Fungal populations exhibiting little or no sexual reproduction are expected to exhibit low genetic variation and a significant degree of non-random association amongst unlinked alleles.

    In contrast, high genetic variation and random associations amongst neutral loci indicate that the pathogen population may undergo regular sexual recombination 2122 For many heterothallic fungi, sexual reproduction is controlled by a single regulatory locus containing two alternate idiomorphs MAT and MAT 171824 and requires the interaction between individuals swx distinct mating types.

    Heterothallic pathogens with regular cycles sex sexual reproduction are expected to have the two mating types present in equal frequencies in a population as a result of frequency dependency 2225 and low genetic differentiation and no phylogenetic associations between isolates in the two mating type groups attributed to the frequent exchange sexx genetic material. In this study, we used population genetic approach ba investigate the occurrence of cryptic sexual reproduction in the plant pathogenic fungus Alternaria alternatawhich is associated with the early blight disease on potatoes.

    Potato early blight, characterized by the formation of dark-colored spots that are necrotic in the centre with a pattern of concentric rings on leaves, is among the most destructive emerging pathogen worldwide It is a polycyclic disease and its epidemic can be rapidly built up when environments are conducive Considerable economic losses caused by potato early blight have been reported in many countries In the recent years, the frequency and scale of early blight occurrences have increased, possibly attributed to reduced nitrogen supplies, increased air temperature, withdrawal mat some effective fungicides and the changes of farming systems such as the adoption of irrigation and minimum tillage for resource and environment conservations In China, early blight has been observed in all potato production areas, suggesting environmental conditions in the country are favorable for its epidemic and the disease can occur in any stages of potato development.

    Both Alternaria alternata and A. On the other hand, A. Its conidia usually has 9—11 transverse septa and 1—2 longitudinal septa with one long to ovoid beak 26 In China and Europe, the majority of previous studies indicate that A.

    Our survey from China is consistent with this result unpublished data. Though carrying a functional MAT1 gene 18it is considered to be an asexual fungus Ascomycota because teleomorph the sexual form mat not been observed yet in nature.

    Conflicting with theoretical expectation for an asexual pathogen, previous population genetic surveys revealed high genetic variation in A. However, the majority of these surveys focused the descriptions of within-population variation using virulence, vegetative compatibility or genetic markers with less reliability and resolution such as RAPD.

    Population genetic analysis on the spatial dynamics of genetic variation in A. Knowledge from this type of analysis is important for understanding the reproductive mode mat adaptive potential of the pathogen, sex, necessary in designing an effective and sustainable disease management program for controlling this emerging disease worldwide. It is reported that A. Furthermore, some evidence of sexual recombination was reported in A.

    Hence, the objectives of this study were: 1 to screen specific primers for the determination of mating types in A. A total of Alternaria alternata isolates from different parts of China Fig. After clonal correction, isolates were included in the analysis of mating type frequency Table 2. Both mating types were detected in all 17 field populations sampled across China Table 2. MAT srx in the field populations ranged from 0.

    The hypothesis of ratio between MAT and MAT frequencies was not rejected within all but one field population.

    Map showing the geographic locations of the 17 A. Polymerase chain reaction amplification of 33 A. The first panel is a bp size ladder. The isolates were assigned to distinct genotypes. Among these genotypes, The most common genotype was detected 24 times and the most widespread genotype was detected in 9 out mst the 17 field populations Fig.

    Looking at the temporal scale, Therefore, the frequency of shared genotypes decreased from the first sex third sampling year. Clonal fraction mat the field populations ranged from 0. Correspondingly, standardized Shannon index in the nq populations ranged from 0. Spatial distribution of multilocus genotypes in the A. In the 17 field populations, the hypothesis of random association was not rejected sex When isolates from different fields were pooled together, the hypothesis of random association was retained in Genetic differentiation G ST between the two mating type groups in the 17 field populations ranged ha 0.

    Mat from the two mating types were randomly distributed in phylogenetic clades Fig. B Neighbor joining tree of all A. Same genotypes were recovered in the A. This result suggests that infected tubers or other materials may be the main mechanisms responsible for long distance dispersal of conidia of A.

    However, clonal fraction was considerably low across populations. In addition to asexual reproduction, our results suggested that, like many presumed asexual fungi 15cryptic recombination might be occurring and contributing significantly to the population genetic mat and epidemics of this emerging potato pathogen.

    We have several lines of sex that support the hypothesis of recombination in A. Populations mst recombination will exhibit a high degree of clonality dominated by a few genotypes and low gene diversity. This level of genotype diversity is comparable to some fungi with frequent sexual recombination 102344 but much higher than those reproducing primarily in clonally.

    For example, in an asexual potato sxe P. High genotype diversity in A. Populations without recombination are sex expected to exhibit a significant degree of non-random association among unlinked alleles.

    However, in the current study, all gametic equilibrium analyses indicate a low to no mqt associations amongst the SSR markers ma most of the 17 field populations Table 4. While many biological and evolutionary processes including genetic drift, asexual reproduction and assorting mating may lead to non-random association, the sex of random association among SSR markers strongly indicate that most of the A.

    Genetic differentiation between isolates from MAT and MAT was very low when SSR variation in the two groups of the pathogen was compared, suggesting a maat degree of genetic exchange between the two sub-populations of the pathogen. G ST between two mating type groups in the majority of the 17 field populations was lower than 0. In three pathogen populations Kunming2, Changle and Qujingmoderate to high genetic differentiations were detected between the two mating type groups, but they were likely attributed to sampling error caused by small population sizes as only 5—8 genotypes were included in these populations for the analysis.

    Phylogenetic analyses for the relatedness between the two mating type groups of isolates using both partial 50 isolates, Fig. While skewed ratio between the two mating types in a population could be caused by many biological and evolutionary events, an observed coexistence and equal frequency of both mating types would be consistent with regular occurrences of recombination.

    In our study, the null hypothesis of a ratio between the two mating types was retained in all but one populations and this result remained the same regardless whether clone corrected or clone-uncorrected data were used.

    The observation of significant departure from a ratio in mat field population could be due to a false rejection of the null hypothesis. Both meiotic recombination in sexual reproduction and mitotic recombination in parasexual reproduction could explain the observed patterns of population genetic structure in A.

    Parasexual reproduction was first described in Aspergillus nidulans 51 and since then has been reported in many pathogenic fungi 405253 It mat involves may fusion mat hyphae anastomosis from different strains in the same vegetative compatibility group to form heterokaryons heterokaryosis and then fusion of the unlike nuclei in the cell of the heterokaryon karyogamy to form diploid nuclei.

    Homologous chromosomes in the diploid nuclei undergo synapsis and mitotic recombination cross-overgenerating recombinant chromosomes if the homologs carry different may information. The diploid nucleus begins to lose chromosomes gradually through cycles of mitotic divisions and return to a stable haploid state eventually.

    Each of these events is believed to be relatively rare sex Ssx example, the frequency of chiasma formation in parasexual reproduction is much lower than that in sexual reproduction because chromosomes in the former do not pair in a regular arrangement. Furthermore, due mat non-disjunctive division in diploid nuclei, parasexual reproduction is expected to form a series of aneuploid either with additional or missing copies of chromosomes, generating multiple or null amplifications by PCR amplification.

    In our study, we did not detect such multiple or null amplifications in any SSR amplifications of the isolates. Therefore, while we cannot exclude the possibility of parasexual reproduction, we believe the main contribution to the observed genetic variation in A. It is likely the sexual stage of the pathogen occurs off-season on alternate hosts, making it difficult to observe.

    Sexual reproduction in A. Our results suggest sexual reproduction may commonly occur in the pathogen by using a large collection involved many population originated from wide geographical locations. In conclusion, our results indicate that, like many eukaryotic pathogens, A. This reproducing strategy allows the pathogen to preserve allelic combinations that are well adapted to existing hosts and environments while retain its ability to generate new allelic combinations that may offer an advantage on novel hosts and in changing environments 57making it more difficult to manage.

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