scholarly journals Transposable element insertions shape gene regulation and melanin production in a fungal pathogen

2018 ◽  
Author(s):  
Parvathy Krishnan ◽  
Lukas Meile ◽  
Clémence Plissonneau ◽  
Xin Ma ◽  
Fanny E. Hartmann ◽  
...  

AbstractBackgroundVariation in gene expression contributes to phenotypic diversity within species and adaptation. However, very few cases of adaptive regulatory changes have been reported and the mechanisms underlying variation in gene expression remain largely unexplored. Fungal pathogen genomes are highly plastic and harbour numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work we elucidated how transposable elements contribute to variation of melanin accumulation, a quantitative adaptive trait of fungal pathogens that is involved in survival under stress conditions.ResultsWe demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogenZymoseptoria tritici. We show that differences in melanin levels between two strains ofZ. triticiare due to two levels of transcriptional regulation: 1) variation in the promoter sequence ofZmr1, and 2) an insertion of transposable elements upstream of theZmr1promoter. Remarkably, independent insertions of transposable elements upstream ofZmr1occurred in 9% ofZ. triticistrains from around the world and negatively regulatedZmr1expression, contributing to melanin accumulation variation.ConclusionsOur studies demonstrate that different layers of transcriptional control fine-tune the synthesis of melanin. These regulatory mechanisms potentially evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments.

2019 ◽  
Vol 20 (22) ◽  
pp. 5755 ◽  
Author(s):  
Denise Drongitis ◽  
Francesco Aniello ◽  
Laura Fucci ◽  
Aldo Donizetti

The biology of transposable elements (TEs) is a fascinating and complex field of investigation. TEs represent a substantial fraction of many eukaryotic genomes and can influence many aspects of DNA function that range from the evolution of genetic information to duplication, stability, and gene expression. Their ability to move inside the genome has been largely recognized as a double-edged sword, as both useful and deleterious effects can result. A fundamental role has been played by the evolution of the molecular processes needed to properly control the expression of TEs. Today, we are far removed from the original reductive vision of TEs as “junk DNA”, and are more convinced that TEs represent an essential element in the regulation of gene expression. In this review, we summarize some of the more recent findings, mainly in the animal kingdom, concerning the active roles that TEs play at every level of gene expression regulation, including chromatin modification, splicing, and protein translation.


2006 ◽  
Vol 16 (7) ◽  
pp. 1188-1194
Author(s):  
Dae-Soo Kim ◽  
Jae-Won Huh ◽  
Hong-Seok Ha ◽  
Tae-Hong Kim ◽  
Un-Jong Jo ◽  
...  

2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Cécile Lorrain ◽  
Alice Feurtey ◽  
Mareike Möller ◽  
Janine Haueisen ◽  
Eva Stukenbrock

Abstract Transposable elements (TEs) impact genome plasticity, architecture, and evolution in fungal plant pathogens. The wide range of TE content observed in fungal genomes reflects diverse efficacy of host-genome defense mechanisms that can counter-balance TE expansion and spread. Closely related species can harbor drastically different TE repertoires. The evolution of fungal effectors, which are crucial determinants of pathogenicity, has been linked to the activity of TEs in pathogen genomes. Here, we describe how TEs have shaped genome evolution of the fungal wheat pathogen Zymoseptoria tritici and four closely related species. We compared de novo TE annotations and repeat-induced point mutation signatures in 26 genomes from the Zymoseptoria species-complex. Then, we assessed the relative insertion ages of TEs using a comparative genomics approach. Finally, we explored the impact of TE insertions on genome architecture and plasticity. The 26 genomes of Zymoseptoria species reflect different TE dynamics with a majority of recent insertions. TEs associate with accessory genome compartments, with chromosomal rearrangements, with gene presence/absence variation, and with effectors in all Zymoseptoria species. We find that the extent of RIP-like signatures varies among Z. tritici genomes compared to genomes of the sister species. The detection of a reduction of RIP-like signatures and TE recent insertions in Z. tritici reflects ongoing but still moderate TE mobility.


2021 ◽  
Author(s):  
UDAYKUMAR KAGE ◽  
Donald Gardiner ◽  
Jiri S Stiller ◽  
Kemal Kazan

To date, translational regulation of key genes controlling infection-related processes in fungal pathogens during their interactions with plants has not been studied. Here, we employed ribosome profiling (ribo-seq) to study translational responses and how such responses are coordinated with transcriptional changes in the fungal pathogen Fusarium graminearum (Fg), which causes Fusarium head blight (FHB), a destructive disease of cereal crops worldwide. Transcription and translation were not always coordinated with approximately 22% of Fg genes showing a discordant relationship during wheat infection. Nitrite reductase, which we show here as an important component of fungal virulence, is only regulated at the translational level in Fg. In addition, more than 1000 new open reading frames (ORFs), many of which are short and highly conserved, were identified in the Fg genome. Like in higher eukaryotes, translation is controlled by upstream ORFs (uORFs) in Fg during infection. Similarly, miRNAs control both transcription and translation in Fg during wheat infection. However, Fgdicer2-dependent miRNAs do not have a significant effect on transcriptional gene expression at the global outset. The ribo-seq study undertaken here for the first time in any fungal pathogen discovered novel insights about the biology of an important plant pathogen.


2017 ◽  
Author(s):  
Janine Haueisen ◽  
Mareike Möller ◽  
Christoph J. Eschenbrenner ◽  
Jonathan Grandaubert ◽  
Heike Seybold ◽  
...  

AbstractFilamentous plant pathogens exhibit extraordinary levels of genomic variability that is proposed to facilitate rapid adaptation to changing host environments. However, the impact of genomic variation on phenotypic differentiation in pathogen populations is largely unknown. Here, we address the extent of variability in infection phenotypes of the hemibiotrophic wheat pathogen Zymoseptoria tritici by studying three field isolates collected in Denmark, Iran, and the Netherlands. These three isolates differ extensively in genome structure and gene content, but produce similar disease symptoms in the same susceptible wheat cultivar. Using advanced confocal microscopy, staining of reactive oxygen species, and comparative analyses of infection stage-specific RNA-seq data, we demonstrate considerable variation in the temporal and spatial course of infection of the three isolates. Based on microscopic observation, we determined four core infection stages: establishment, biotrophic growth, lifestyle transition, and necrotrophic growth and asexual reproduction. Comparative analyses of the fungal transcriptomes, sequenced for every infection stage, revealed that the gene expression profiles of the isolates differed significantly, and 20% of the genes are differentially expressed between the three isolates during infection. The genes exhibiting isolate-specific expression patterns are enriched in genes encoding effector candidates that are small, secreted, cysteine-rich proteins and putative virulence determinants. Moreover, the differentially expressed genes were located significantly closer to transposable elements, which are enriched for the heterochromatin-associated histone marks H3K9me3 and H3K27me3 on the accessory chromosomes. This observation indicates that transposable elements and epigenetic regulation contribute to the infection-associated transcriptional variation between the isolates. Our findings illustrate how high genetic diversity in a pathogen population can result in highly differentiated infection and expression phenotypes that can support rapid adaptation in changing environments. Furthermore, our study reveals an exceptionally high extent of plasticity in the infection program of an important wheat pathogen and shows a substantial redundancy in infection-related gene expression.Author summaryZymoseptoria tritici is a pathogen that infects wheat and induces necrosis in leaf tissue. Z. tritici field populations exhibit high levels of genetic diversity, and here we addressed the consequences of this diversity on infection phenotypes. We conducted a detailed comparison of the infection processes of three Z. tritici isolates collected in Denmark, the Netherlands, and Iran. We inoculated leaves of a susceptible wheat cultivar and monitored development of disease symptoms and infection structures in leaf tissue by confocal microscopy. The three isolates exhibited highly differentiated spatial and temporal patterns of infection, although quantitative disease was similar. Furthermore, more than 20% of the genes were differentially expressed in the three isolates during wheat infection. Variation in gene expression is particularly associated with transposable elements, suggesting a role of epigenetic regulation in transcriptional variation among the three isolates. Finally, we find that genes encoding putative virulence determinants were enriched among the differentially expressed genes, suggesting that each of the three Z. tritici isolates utilizes different strategies to manipulate host defenses. Our results emphasize that phenotypic diversity plays an important role in pathogen populations and should be considered when developing crop protection strategies.


2010 ◽  
Vol 34 (8) ◽  
pp. S27-S27
Author(s):  
Jianqi Cui ◽  
Xiuying Pei ◽  
Qian Zhang ◽  
Bassel E. Sawaya ◽  
Xiaohong Lu ◽  
...  

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