Mating-type loci of Ustilago esculenta are essential for mating and development

Zhang, Yafen; Yin, Yumei; Hu, Peng; Yu, Jiajia; Xia, Wei; Ge, Qianwen; Cao, Qian; Cui, Henggang; Yu, Xiaoping; Ye, Zihong

doi:10.1016/j.fgb.2019.01.008

Cited by 6 publications

(18 citation statements)

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“…The strains of U. maydis used in this study are also listed in Supplementary Table S1. The growth conditions and media for E. coli (Russell and Sambrook, 2001), U. maydis (Holliday, 1974), and U. esculenta (Zhang et al, 2019) have previously been described. The growth conditions of Zea mays (the early golden bantam) and the wild Z. latifolia used for pathogenic development assays of tested strains before and after stem injection have previously been described (Flor-Parra et al, 2007;Zhang et al, 2019).…”

Section: Strains and Plant Growth Conditionsmentioning

confidence: 99%

“…Induced expression of either the active bE/bW heterodimer or Rbf1 triggers a dimorphic switch from budding yeast-like growth to filamentous tip growth in the typical smut fungi U. maydis (Heimel et al, 2010a,b). In U. esculenta, the UeRbf1 and b genes also participate in filamentous growth (Hu et al, 2015;Zhang et al, 2019). First, we detected the expression levels of the UeRbf1 and b genes in the UeKpp2 double mutant cross relative to the WT strain cross during mating, using qRT-PCR.…”

Section: Defective Filamentous Growth In Uekpp2 Mutants Is Related Tomentioning

confidence: 99%

“…The T type strain shows the pathogenic life cycle of typical smut fungi, with three distinct stages (Zhang et al, 2017): the budding growth stage of haploid cells from diploid teliospore germination; the mating stage, which is a prerequisite for infection; and pathogenicity development, with proliferation and teliospore formation happening in planta. The mating stage includes two steps: fusion of two compatible haploid cells, mainly regulated by a pheromone receptor system that consists of pheromones and pheromone receptors (encoded at the triallelic a mating-type locus), and post-fusion filamentation that is capable of infection, controlled by the active heterodimeric bE/bW complex (Liang et al, 2019;Zhang et al, 2019). The T type strain causes gray jiaobai, which is discarded by farmers due to its unacceptable taste and potential to trigger hypersensitivity pneumonitis (Fujii et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Its mating system consists of both a and b matingtype loci (Bakkeren et al, 2008;Raudaskoski and Kothe, 2010;Zuo et al, 2019). The recognition of pheromones by opposite pheromone receptors, encoded at the a locus, elicits the fusion of two compatible haploid cells (Szabo et al, 2002;Zhang et al, 2019). The heterodimeric transcription factor bE/bW, which is encoded by the b locus, triggers filamentation and pathogenicity (Yan et al, 2016;Zhang et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…The recognition of pheromones by opposite pheromone receptors, encoded at the a locus, elicits the fusion of two compatible haploid cells (Szabo et al, 2002;Zhang et al, 2019). The heterodimeric transcription factor bE/bW, which is encoded by the b locus, triggers filamentation and pathogenicity (Yan et al, 2016;Zhang et al, 2019). The cross-talk between the highly conserved cAMP pathway and the mitogenactivated protein kinase (MAPK) pathway is crucial for mating by integrating pheromone signaling and environmental cues (Feldbrügge et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Functional Properties of the MAP Kinase UeKpp2 in Ustilago esculenta

Zhang

Cao

et al. 2020

Front. Microbiol.

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Ustilago esculenta undergoes an endophytic life cycle in Zizania latifolia. It induces the stem of its host to swell, forming the edible galls called jiaobai in China, which are the second most commonly cultivated aquatic vegetable in China. Z. latifolia raised for jiaobai can only reproduce asexually because the U. esculenta infection completely inhibits flowering. The infection and proliferation in the host plants during the formation of edible gall differ from those of conventional pathogens. Previous studies have shown a close relationship between mitogen-activated protein kinase (MAPK) and fungal pathogenesis. In this study, we explored the functional properties of the MAPK UeKpp2. Cross-species complementation assays were carried out, which indicated a functional complementation between the UeKpp2 of U. esculenta and the Kpp2 of Ustilago maydis. Next, UeKpp2 mutants of the UeT14 and the UeT55 sporidia background were generated; these showed an aberrant morphology of budding cells, and attenuated mating and filamentous growth in vitro, in the context of normal pathogenicity. Interestingly, we identified another protein kinase, UeUkc1, which acted downstream of UeKpp2 and may participate in the regulation of cell shape. We also found a defect of filamentous growth in UeKpp2 mutants that was not related to a defect of the induction of mating-type genes but was directly related to a defect in UeRbf1 induction. Overall, our results indicate an important role for UeKpp2 in U. esculenta that is slightly different from those reported for other smut fungi.

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Section: Strains and Plant Growth Conditionsmentioning

confidence: 99%

Section: Defective Filamentous Growth In Uekpp2 Mutants Is Related Tomentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Functional Properties of the MAP Kinase UeKpp2 in Ustilago esculenta

Zhang

Cao

et al. 2020

Front. Microbiol.

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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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Cloning and disruption of the UeArginase in Ustilago esculenta: evidence for a role of arginine in its dimorphic transition

Zhang

et al. 2019

BMC Microbiol

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Background Ustilago esculenta , a typical dimorphic fungus could infect Zizania latifolia and induce host stem swollen to form an edible vegetable called Jiaobai in China. The strains differentiation especially in the mating ability and pathogenicity is closely related to different phenotypes of Jiaobai formed in the fields. Dimorphic switching, a tightly regulated processes, is essential for the pathogenetic development of dimorphic fungi. In responses to environment cues, dimorphic switching can be activated through two conserved cell signaling pathways-PKA and MAPK pathways. Previous study indicated that exogenous arginine could induce hyphal formation in several dimorphic fungi through hydrolysis by arginase, but inhibit the dimorphic transition of U. esculenta . We conducted this study to reveal the function of arginine on dimorphic transition of U. esculenta . Results In this study, we found that arginine, but not its anabolites, could slow down the dimorphic transition of U. esculenta proportionally to the concentration of arginine. Besides, UeArginase , predicated coding arginase in U. esculenta was cloned and characterized. UeArginase mutants could actually increase the content of endogenous arginine, and slow down the dimorphic transition on either nutritious rich or poor medium. Either adding exogenous arginine or UeArginase deletion lead to down regulated expressions of UePkaC , UePrf1 , mfa1.2 , mfa2.1 , pra1 and pra2 , along with an increased content of arginine during mating process. Conclusion Results of this study indicated a direct role of arginine itself on the inhibition of dimorphic transition of U. esculenta , independent of its hydrolysis by UeArginase. Electronic supplementary material The online version of this article (10.1186/s12866-019-1588-2) contains supplementary material, which is available to authorized users.

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Mating-type loci of Ustilago esculenta are essential for mating and development

Cited by 6 publications

References 48 publications

Functional Properties of the MAP Kinase UeKpp2 in Ustilago esculenta

Functional Properties of the MAP Kinase UeKpp2 in Ustilago esculenta

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

Cloning and disruption of the UeArginase in Ustilago esculenta: evidence for a role of arginine in its dimorphic transition

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