Mating-type genes of the anamorphic fungus Ulocladium botrytis affect both asexual sporulation and sexual reproduction

Wang, Qun; Shi, Wang; Xiong, Chen; James, Timothy Y.; Zhang, Xiu Guo

doi:10.1038/s41598-017-08471-3

Cited by 17 publications

(15 citation statements)

References 64 publications

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“…It has been suggested that B. cinerea mating genes participate in processes other than mating because they remain transcriptionally active at different developmental stages of the fungus (59). The role of mating genes in fungal development, including hyphal growth, asexual sporulation, and pathogenicity, was previously reported for different filamentous fungi, including plant pathogens (63)(64)(65)(66)(67). Hence, even if this organism reproduces asexually, both mating types will still be maintained in a population.…”

Section: Discussionmentioning

confidence: 82%

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures

Kozhar

Larsen

Grünwald

et al. 2020

Appl Environ Microbiol

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Many fungal pathogens have short generation times, large population sizes, and mixed reproductive systems, providing high potential to adapt to heterogeneous environments of agroecosystems. Such adaptation complicates disease management and threatens food production. A better understanding of pathogen population biology in such environments is important to reveal key aspects of adaptive divergence processes to allow improved disease management. Here, we studied how evolutionary forces shape population structure of Botrytis cinerea, the causal agent of gray mold, in the Pacific Northwest agroecosystems. Populations of B. cinerea from adjacent fields of small fruit hosts were characterized by combining neutral markers (microsatellites) with markers that directly respond to human-induced selection pressures (fungicide resistance). Populations were diverse, without evidence for recombination and association of pathogen genotype with host. Populations were highly localized with limited migration even among adjacent fields within a farm. A fungicide resistance marker revealed strong selection on population structure due to fungicide use. We found no association of resistance allele with genetic background, suggesting de novo development of fungicide resistance and frequent extinction/recolonization events by different genotypes rather than the spread of resistance alleles among fields via migration of a dominant genotype. Overall our results showed that in agroecosystems, B. cinerea populations respond strongly to selection by fungicide use with greater effect on population structure compared to adaptation to host plant species. This knowledge will be used to improve disease management by developing strategies that limit pathogen local adaptation to fungicides and other human-induced selection pressures present in Pacific Northwest agroecosystems and elsewhere. IMPORTANCE Agroecosystems represent an efficient model for studying fungal adaptation and evolution in anthropogenic environments. In this work, we studied what evolutionary forces shape populations of one of the most important fungal plant pathogens, B. cinerea, in small fruit agroecosystems of the Pacific Northwest. We hypothesized that host, geographic, and anthropogenic factors of agroecosystems structure B. cinerea populations. By combining neutral markers with markers that directly respond to human-induced selection pressures, we show that pathogen populations are highly localized and that selection pressure caused by fungicide use can have a greater effect on population structure than adaptation to host. Our results give a better understanding of population biology and evolution of this important plant pathogen in heterogeneous environments but also provide a practical framework for the development of efficient management strategies by limiting pathogen adaptation to fungicides and other human-induced selection pressures present in agroecosystems of the Pacific Northwest and elsewhere.

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Section: Discussionmentioning

confidence: 82%

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures

Kozhar

Larsen

Grünwald

et al. 2020

Appl Environ Microbiol

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“…In Penicillium chrysogenum, the MAT1-1-1 transcription factor also participates in key biological processes such as regulation of asexual development and morphogenesis, as well as amino acid, iron, and secondary metabolism (Becker et al 2015). The mating-type genes control conidial number and size in Ulocladium botrytis (Wang et al 2017). Virulence genes were also included among targets of mating-type transcription factors in Cryptococcus neoformans (Mead et al 2015).…”

Section: Discussionmentioning

confidence: 99%

Mating System in the Brown Rot Pathogens Monilinia fructicola, M. laxa, and M. fructigena

et al. 2018

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Monilinia fructicola, M. laxa, and M. fructigena are the most important pathogens responsible for brown rot disease of stone and pome fruits. Information on their mating system and sexual behavior is scant. A mating-type-specific PCR-based assay was developed and applied to 155 Monilinia isolates from 10 countries and 10 different host plants. We showed that single isolates carry only one of two opposite idiomorphs at the MAT1 locus consistent with a heterothallic mating system for all three species. MAT1-1 and MAT1-2 mating types were detected in similar proportions in samples of isolates of each species and hence there do not appear to be genetic obstacles to the occurrence of sexual reproduction in their populations. Inter simple sequence repeat markers suggested that asexual reproduction is prevalent, but that sexual recombination occurs in M. fructicola populations in Italy. The genetic architectures of the MAT1 loci of the three pathogens were analyzed. MAT1-1 and MAT1-2 idiomorphs are flanked upstream and downstream by the APN2 and SLA2 genes and resemble those of Botrytis cinerea and other heterothallic fungi in the family Sclerotiniaceae. Each idiomorph contains a specific couple of genes, MAT1-1-1 (with alpha-box domain) and MAT1-1-5 in MAT1-1, and MAT1-2-1 (with HMG-box domain) and MAT1-2-10 in MAT1-2. Small gene fragments (dMAT1-1-1 and dMAT1-2-1) from the opposite idiomorph were detected close to their flanking regions. Constitutive expression of the four MAT1 genes during vegetative growth was ascertained by transcriptomic analysis (RNA-Seq). Antisense transcription of the MAT1-1-1 and MAT1-2-1 genes and intergenic transcribed regions of the MAT1 locus were detected. These results represent new insights into the mating systems of these three economically-important pathogens which could contribute to improve the knowledge on their population biology.

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“…Though the teleomorph formation has never been successful, we found that the transcription levels of Ulocladium MAT1-1-1 and MAT1-2-1 genes were up-regulated on HAY culture media at 0-10 C with a light/dark cycle. MAT genes that are the key regulators for sexuality in filamentous ascomycetes are functional in Ulocladium (Geng et al, 2014;Wang et al, 2017), which could be activated by several environmental cues, and then control the sexual development in fungi. In addition, though specific environmental conditions can promote the expression of MAT genes of this genus, compared to Stemphylium botryosum, the significantly lower levels suggesting that environmental factors alone are insufficient to induce sexual progeny.…”

Section: Discussionmentioning

confidence: 99%

“…However, unlike the majority of homothallic fungi, MAT1-1 and MAT1-2 idiomorphs are not closely linked and flanked by identical sequences in Ulocladium species. It has been reported that U. botrytis MAT genes have the ability to induce sexual recombination in Cochliobolus heterostrophus (Wang et al, 2017), indicating that MAT locus might be functional in Ulocladium, and the expression levels of MAT genes might directly affect sexual development in fungi. Thus, the Ulocladium species has the potential for sexual reproduction.…”

Section: Introductionmentioning

confidence: 99%

Determination of the reference genes for qRT-PCR normalization and expression levels of MAT genes under various conditions in Ulocladium

Geng

2020

PeerJ

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The genus Ulocladium is thought to be strictly asexual. One of the possible reasons for the lack of sexuality in Ulocladium species is the absence of the stimulus of environmental factors. Sexual reproduction in ascomycetes is controlled by a specific region in the genome referred to as mating-type locus (MAT) that consists of two dissimilar DNA sequences in the mating partners, termed MAT1-1 and MAT1-2 idiomorphs. To identify the response of MAT loci to environmental conditions, the mRNA transcription level of MAT1-1-1 and MAT1-2-1 genes was tested using qRT-PCR under different temperatures (−20 °C, −10 °C, 0 °C, 10 °C, 20 °C, 30 °C and 40 °C), culture medias (CM, OA, HAY, PCA, PDA and V8), photoperiods (24 h light, 24 h dark, 12 h light/12 h dark, 10 h light/14 h dark and 8 h light/16 h dark), and CO2 concentrations (0.03%, 0.5%, 1%, 5%, 10%, 15% and 20%). For obtaining reliable results from qRT-PCR, the most stable internal control gene and optimal number of reference genes for normalization were determined under different treatments. The results showed that there is no universal internal control gene that is expressed at a constant level under different experimental treatments. In comparison to various incubation conditions, the relative expression levels of both MAT genes were significantly increased when fungal mycelia were grown on HAY culture media at 0–10 °C with a light/dark cycle, indicating that temperature, culture media, and light might be the key environmental factors for regulating the sexuality in Ulocladium. Moreover, MAT1-1-1 and MAT1-2-1 genes showed similar expression patterns under different treatments, suggesting that the two MAT genes might play an equally important role in the sexual evolutionary process.

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Mating-type genes of the anamorphic fungus Ulocladium botrytis affect both asexual sporulation and sexual reproduction

Cited by 17 publications

References 64 publications

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures

Mating System in the Brown Rot Pathogens Monilinia fructicola, M. laxa, and M. fructigena

Determination of the reference genes for qRT-PCR normalization and expression levels of MAT genes under various conditions in Ulocladium

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