Folding Features and Dynamics of 3D Genome Architecture in Plant Fungal Pathogens

Xia, Chongjing; Huang, Liang; Huang, Jie; Zhang, Hao; Huang, Ying; Benhamed, Moussa; Wang, Meinan; Chen, Xianming; Zhang, Min; Liu, Taiguo; Chen, Wanquan

doi:10.1128/spectrum.02608-22

Cited by 8 publications

(7 citation statements)

References 59 publications

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“…For instance, the arbuscular mycorrhizal fungus, Rhizophagus irregularis , manifests clearly defined A/B compartments that align with transcriptional activity and repeat content ( 73 ). Conversely, other fungi show minimal chromatin compartmentalization ( 74 ). In our study, we find that genome compartmentalization of F .…”

Section: Discussionmentioning

confidence: 99%

The jet-like chromatin structure defines active secondary metabolism in fungi

Shao,

Wang,

Zhang

et al. 2024

Nucleic Acids Research

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Eukaryotic genomes are spatially organized within the nucleus in a nonrandom manner. However, fungal genome arrangement and its function in development and adaptation remain largely unexplored. Here, we show that the high-order chromosome structure of Fusarium graminearum is sculpted by both H3K27me3 modification and ancient genome rearrangements. Active secondary metabolic gene clusters form a structure resembling chromatin jets. We demonstrate that these jet-like domains, which can propagate symmetrically for 54 kb, are prevalent in the genome and correlate with active gene transcription and histone acetylation. Deletion of GCN5, which encodes a core and functionally conserved histone acetyltransferase, blocks the formation of the domains. Insertion of an exogenous gene within the jet-like domain significantly augments its transcription. These findings uncover an interesting link between alterations in chromatin structure and the activation of fungal secondary metabolism, which could be a general mechanism for fungi to rapidly respond to environmental cues, and highlight the utility of leveraging three-dimensional genome organization in improving gene transcription in eukaryotes.

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Section: Discussionmentioning

confidence: 99%

The jet-like chromatin structure defines active secondary metabolism in fungi

Shao,

Wang,

Zhang

et al. 2024

Nucleic Acids Research

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“…The Illumina clean reads of each isolate were further trimmed, by removing adapter and primer sequences at read ends using Trimmomatic-0.39 (Bolger et al, 2014) with the following settings: LEADING:20 TRAILING:20 SLIDINGWINDOW:4:20 MINLEN:100. The high-quality trimmed reads were mapped to the Pst CYR34 reference genome (Xia et al, 2022) using the BWA-MEM (Li & Durbin, 2010) with default parameters except for: -r 1.0. The CYR34 genome was selected as the reference because a) it is the most prevalent race in China, and b) it is well-annotated with high quality (BUSCO completeness of 97.0%).…”

Section: Methodsmentioning

confidence: 99%

Population genomic analyses reveal extensive genomic regions within selective sweeps associated with adaptation and demographic history of a wheat fungal pathogen

Xing,

Xia,

Huang

et al. 2023

Preprint

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Plant pathogens can quickly evolve in response to the changing host and environment, resulting in destructive epidemics. The fungusPuccinia striiformisf. sp.tritici(Pst), causing wheat stripe rust disease worldwide, is one such pathogen. In the arms race between pathogens and hosts, changes in host populations exerted continuous selective forces on the dynamics of pathogens. However, the footprints of these selection forces and the demography ofPstremain poorly explored, limited our understanding the evolutionary processes that shape the spread and evolution of pathogens. In this study, we revealed several features of worldwidePstpopulations through population genomic analyses. There might be limited gene flow betweenPstpopulations from China and other countries. A slower rate of linkage disequilibrium decay was detected comparing to rust fungi with known sexual reproduction. Furthermore, we detected extensive hard and soft sweeps associated withPstadaptation. Genes within the selective sweeps were enriched in secreted proteins and effectors and showed functions related to pathogenicity or virulence, temperature tolerance, and fungicide resistance implying that ChinesePstpopulations suffered positive selection pressures from host and abiotic factors. Moreover, demographic history indicatedPstpopulations experienced strong bottlenecks at the beginning of the wheat domestication around 10,000 years ago and during modern agriculture around 100 years ago, suggesting that the crop domestication and breeding programs could continuously contribute to the decline of pathogen effective population sizes. Our results provided insights into the evolution of thePstgenome and highlighted the role of modern agriculture on pathogen demography.Author SummaryWheat stripe rust, as a pathogen of wheat, is capable of inducing significant yield reduction on a global scale. Traditional epidemiological investigations have elucidated the causative agent behind this disease, the wheat stripe rust pathogen, as an organism exhibiting swift adaptive evolution in response to its environment.However, the precise mechanisms underpinning its adaptive strategies and the ensuing alterations in population dynamics remain relatively unexplored.In our research, we have undertaken an analysis encompassing wheat stripe rust samples throughout the world. Employing population genomics methods, we have sought to discern the genomic footprints corresponding to the adaptive process within the pathogen. These genomic footprints have illuminated the operation of positive selection pressures caused by both the host plant and the ecological context.Concurrently, it have provided insights into the population size that the wheat stripe rust pathogen has undergone over millennia. Notably, its change in population size revealed the demographic history associated with wheat domestication.

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“…Similar patterns of TAD-like structures have been observed in S. cerevisiae , where globule structures are delimited by transcriptionally active genes that are often in a convergent orientation (Tsochatzidou et al 2017 , Schalbetter et al 2019 ). Additionally, TAD-like structures can be seen in E. festucae , where RIP’d AT-rich heterochromatic regions strongly interact to form large structures to compact chromatin (Winter et al 2018 ), and in the fungal pathogen Puccinia striiformis , which may form uninsulated RGCs across each chromosome arm (Xia et al 2022 ). Another example of TAD-like structures is found in V. dahliae and related Verticillium species where Hi-C datasets display TAD-like structures with increased internal chromatin contact probabilities and few intrachromosomal contacts beyond the TAD-like structure boundaries (Fig.…”

Section: The Spatial Organization Of Fungal Chromatinmentioning

confidence: 99%

“…To date, only the arbuscular mycorrhizal fungus Rhizophagus irregularis , a member of the Glomeromycetes clade, displays clear A/B compartments (Fig. 3D ) (Xia et al 2022 , Yildirir et al 2022 ). In contrast, other fungi display minimal chromatin compartmentalization, possibly reflecting the presence of smaller heterochromatic regions integrated among larger euchromatin domains (Xia et al 2022 ).…”

Section: The Spatial Organization Of Fungal Chromatinmentioning

confidence: 99%

“…3D ) (Xia et al 2022 , Yildirir et al 2022 ). In contrast, other fungi display minimal chromatin compartmentalization, possibly reflecting the presence of smaller heterochromatic regions integrated among larger euchromatin domains (Xia et al 2022 ). However, segregation of fungal chromatin in a manner analogous to A/B compartments, where heterochromatic regions aggregate yet are separated from euchromatic TAD-like structures, has been observed in the Hi-C datasets of multiple fungal species, including S. cerevisiae (Duan et al 2010 ), S. pombe (Mizuguchi et al 2014 ), N. crassa (Galazka et al 2016 , Rodriguez et al 2022 ), E. festucae (Winter et al 2018 ), A. bisporus (Hoencamp et al 2021 ), and V. dahliae (Seidl et al 2020 ).…”

Section: The Spatial Organization Of Fungal Chromatinmentioning

confidence: 99%

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Nuclear genome organization in fungi: from gene folding to Rabl chromosomes

Torres

Reckard

Klocko

et al. 2023

FEMS Microbiology Reviews

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Comparative genomics has recently provided unprecedented insights into the biology and evolution of the fungal lineage. In the post-genomics era, a major research interest focuses now on detailing the functions of fungal genomes, i.e. how genomic information manifests into complex phenotypes. Emerging evidence across diverse eukaryotes has revealed that the organization of DNA within the nucleus is critically important. Here, we discuss the current knowledge on the fungal genome organization, from the association of chromosomes within the nucleus to topological structures at individual genes and the genetic factors required for this hierarchical organization. Chromosome conformation capture followed by high-throughput sequencing (Hi-C) has elucidated how fungal genomes are globally organized in Rabl configuration, in which centromere or telomere bundles are associated with opposite faces of the nuclear envelope. Further, fungal genomes are regionally organized into Topologically Associated Domain-like (TAD-like) chromatin structures. We discuss how chromatin organization impacts the proper function of DNA-templated processes across the fungal genome. Nevertheless, this view is limited to a few fungal taxa given the paucity of fungal Hi-C experiments. We advocate for exploring genome organization across diverse fungal lineages to ensure the future understanding of the impact of nuclear organization on fungal genome function.

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Folding Features and Dynamics of 3D Genome Architecture in Plant Fungal Pathogens

Abstract: Previously, our understanding of 3D genome architecture has mainly come from model mammals, insects, and plants. However, the organization and regulatory functions of 3D genomes in fungi are largely unknown.

Cited by 8 publications

References 59 publications

The jet-like chromatin structure defines active secondary metabolism in fungi

The jet-like chromatin structure defines active secondary metabolism in fungi

Population genomic analyses reveal extensive genomic regions within selective sweeps associated with adaptation and demographic history of a wheat fungal pathogen

Nuclear genome organization in fungi: from gene folding to Rabl chromosomes

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