Analysis of the chromosomal clustering of Fusarium-responsive wheat genes uncovers new players in the defence against head blight disease

AbstractThere is increasing evidence that some functionally related, co-expressed genes cluster within eukaryotic genomes. We present a novel pipeline that delineates such eukaryotic gene clusters. Using this tool for bread wheat, we uncovered 44 clusters of genes that are responsive to the fungal pathogen Fusarium graminearum. As expected, these Fusarium-responsive gene clusters (FRGCs) included metabolic gene clusters, many of which are associated with disease resistance, but hitherto not described for wheat. However, the majority of the FRGCs are non-metabolic, many of which contain clusters of paralogues, including those implicated in plant disease responses, such as glutathione transferases, MAP kinases, and germin-like proteins. 20 of the FRGCs encode nonhomologous, non-metabolic genes (including defence-related genes). One of these clusters includes the characterised Fusarium resistance orphan gene, TaFROG. Eight of the FRGCs map within 6 FHB resistance loci. One small QTL on chromosome 7D (4.7 Mb) encodes eight Fusarium-responsive genes, five of which are within a FRGC. This study provides a new tool to identify genomic regions enriched in genes responsive to specific traits of interest and applied herein it highlighted gene families, genetic loci and biological pathways of importance in the response of wheat to disease.

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Comparative Phylogenomic Synteny Network Analysis of Mammalian and Angiosperm Genomes

10.1101/246736 ◽

2018 ◽

Cited By ~ 1

Author(s):

Tao Zhao ◽

M. Eric Schranz

Keyword(s):

Large Scale ◽

Homeobox Gene ◽

Gene Families ◽

Gene Clusters ◽

Parahox Gene ◽

Family Networks ◽

Plant Genomes ◽

Eukaryotic Gene ◽

Syntenic Gene ◽

Phylogenetic Profiling

AbstractBackgroundSynteny analysis is a valuable approach for understanding eukaryotic gene and genome evolution, but still relies largely on pairwise or reference-based comparisons. Network approaches can be utilized to expand large-scale phylogenomic microsynteny studies. There is now a wealth of completed mammalian (animal) and angiosperm (plant) genomes, two very important lineages that have evolved and radiated over the last ~170 million years. Genomic organization and conservation differs greatly between these two groups; however, a systematic and comparative characterization of synteny between the two lineages using the same approaches and metrics has not been undertaken.ResultsWe have built complete microsynteny networks for 87 mammalian and 107 angiosperm genomes, which contain 1,464,753 nodes (genes) and 49,426,268 edges (syntenic connections between genes) for mammals, and 2,234,461 nodes and 46,938,272 edges for angiosperms, respectively. Exploiting network statistics, we present the functional characteristics of extremely conserved and diversified gene families. We summarize the features of all syntenic gene clusters and present lineage-wide phylogenetic profiling, revealing intriguing sub-clade lineage-specific clusters. We depict several representative clusters of important developmental genes in humans, such as CENPJ, p53 and NFE2. Finally, we present the complete homeobox gene family networks for both mammals (including Hox and ParaHox gene clusters) and angiosperms.ConclusionsOur results illustrate and quantify overall synteny conservation and diversification properties of all annotated genes for mammals and angiosperms and show that plant genomes are in general more dynamic.

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Specialized plant biochemistry drives gene clustering in fungi

10.1101/184242 ◽

2017 ◽

Author(s):

Emile Gluck-Thaler ◽

Jason C. Slot

Keyword(s):

Spatial Scales ◽

Gene Families ◽

Gene Clusters ◽

Gene Organization ◽

Gene Clustering ◽

Environmental Selection ◽

Plant Biochemistry ◽

Eukaryotic Gene ◽

Fungal Genomes ◽

Fungal Genes

AbstractThe fitness and evolution of both prokaryotes and eukaryotes are affected by the organization of their genomes. In particular, the physical clustering of functionally related genes can facilitate coordinated gene expression and can prevent the breakup of co-adapted alleles in recombining populations. While clustering may thus result from selection for phenotype optimization and persistence, the extent to which eukaryotic gene organization in particular is driven by specific environmental selection pressures has rarely been systematically explored. Here, we investigated the genetic architecture of fungal genes involved in the degradation of phenylpropanoids, a class of plant-produced secondary metabolites that mediate many ecological interactions between plants and fungi. Using a novel gene cluster detection method, we identified over one thousand gene clusters, as well as many conserved combinations of clusters, in a phylogenetically and ecologically diverse set of fungal genomes. We demonstrate that congruence in gene organization over small spatial scales in fungal genomes is often associated with similarities in ecological lifestyle. Additionally, we find that while clusters are often structured as independent modules with little overlap in content, certain gene families merge multiple modules in a common network, suggesting they are important components of phenylpropanoid degradation strategies. Together, our results suggest that phenylpropanoids have repeatedly selected for gene clustering in fungi, and highlight the interplay between gene organization and ecological evolution in this ancient eukaryotic lineage.

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Apicidin biosynthesis is linked to accessory chromosomes in Fusarium poae isolates

BMC Genomics ◽

10.1186/s12864-021-07617-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Thomas E. Witte ◽

Linda J. Harris ◽

Hai D. T. Nguyen ◽

Anne Hermans ◽

Anne Johnston ◽

...

Keyword(s):

Fusarium Head Blight ◽

Crop Yields ◽

High Resolution Mass Spectrometry ◽

Gene Clusters ◽

Biosynthetic Gene ◽

Metabolome Analysis ◽

Head Blight ◽

Eastern Canada ◽

Fusarium Poae ◽

Accessory Chromosomes

Abstract Background Fusarium head blight is a disease of global concern that reduces crop yields and renders grains unfit for consumption due to mycotoxin contamination. Fusarium poae is frequently associated with cereal crops showing symptoms of Fusarium head blight. While previous studies have shown F. poae isolates produce a range of known mycotoxins, including type A and B trichothecenes, fusarins and beauvericin, genomic analysis suggests that this species may have lineage-specific accessory chromosomes with secondary metabolite biosynthetic gene clusters awaiting description. Methods We examined the biosynthetic potential of 38 F. poae isolates from Eastern Canada using a combination of long-read and short-read genome sequencing and untargeted, high resolution mass spectrometry metabolome analysis of extracts from isolates cultured in multiple media conditions. Results A high-quality assembly of isolate DAOMC 252244 (Fp157) contained four core chromosomes as well as seven additional contigs with traits associated with accessory chromosomes. One of the predicted accessory contigs harbours a functional biosynthetic gene cluster containing homologs of all genes associated with the production of apicidins. Metabolomic and genomic analyses confirm apicidins are produced in 4 of the 38 isolates investigated and genomic PCR screening detected the apicidin synthetase gene APS1 in approximately 7% of Eastern Canadian isolates surveyed. Conclusions Apicidin biosynthesis is linked to isolate-specific putative accessory chromosomes in F. poae. The data produced here are an important resource for furthering our understanding of accessory chromosome evolution and the biosynthetic potential of F. poae.

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Genomic Characteristics and Comparative Genomics Analysis of Two Chinese Corynespora cassiicola Strains Causing Corynespora Leaf Fall (CLF) Disease

Journal of Fungi ◽

10.3390/jof7060485 ◽

2021 ◽

Vol 7 (6) ◽

pp. 485

Author(s):

Boxun Li ◽

Yang Yang ◽

Jimiao Cai ◽

Xianbao Liu ◽

Tao Shi ◽

...

Keyword(s):

Comparative Genomics ◽

Single Molecule ◽

Rubber Tree ◽

Gene Families ◽

Gene Clusters ◽

The Philippines ◽

Tree Plantations ◽

Comparative Genomic ◽

Corynespora Cassiicola ◽

Leaf Fall

Rubber tree Corynespora leaf fall (CLF) disease, caused by the fungus Corynespora cassiicola, is one of the most damaging diseases in rubber tree plantations in Asia and Africa, and this disease also threatens rubber nurseries and young rubber plantations in China. C. cassiicola isolates display high genetic diversity, and virulence profiles vary significantly depending on cultivar. Although one phytotoxin (cassicolin) has been identified, it cannot fully explain the diversity in pathogenicity between C. cassiicola species, and some virulent C. cassiicola strains do not contain the cassiicolin gene. In the present study, we report high-quality gapless genome sequences, obtained using short-read sequencing and single-molecule long-read sequencing, of two Chinese C. cassiicola virulent strains. Comparative genomics of gene families in these two stains and a virulent CPP strain from the Philippines showed that all three strains experienced different selective pressures, and metabolism-related gene families vary between the strains. Secreted protein analysis indicated that the quantities of secreted cell wall-degrading enzymes were correlated with pathogenesis, and the most aggressive CCP strain (cassiicolin toxin type 1) encoded 27.34% and 39.74% more secreted carbohydrate-active enzymes (CAZymes) than Chinese strains YN49 and CC01, respectively, both of which can only infect rubber tree saplings. The results of antiSMASH analysis showed that all three strains encode ~60 secondary metabolite biosynthesis gene clusters (SM BGCs). Phylogenomic and domain structure analyses of core synthesis genes, together with synteny analysis of polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) gene clusters, revealed diversity in the distribution of SM BGCs between strains, as well as SM polymorphisms, which may play an important role in pathogenic progress. The results expand our understanding of the C. cassiicola genome. Further comparative genomic analysis indicates that secreted CAZymes and SMs may influence pathogenicity in rubber tree plantations. The findings facilitate future exploration of the molecular pathogenic mechanism of C. cassiicola.

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Unravelling population structure heterogeneity within the genome of the malaria vector Anopheles gambiae

BMC Genomics ◽

10.1186/s12864-021-07722-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Melina Campos ◽

Luisa D. P. Rona ◽

Katie Willis ◽

George K. Christophides ◽

Robert M. MacCallum

Keyword(s):

Population Structure ◽

Anopheles Gambiae ◽

Malaria Vector ◽

Mosquito Species ◽

Gene Clusters ◽

Selective Sweeps ◽

Structure Heterogeneity ◽

Genomic Studies ◽

Time Required ◽

Genomic Regions

Abstract Background Whole genome re-sequencing provides powerful data for population genomic studies, allowing robust inferences of population structure, gene flow and evolutionary history. For the major malaria vector in Africa, Anopheles gambiae, other genetic aspects such as selection and adaptation are also important. In the present study, we explore population genetic variation from genome-wide sequencing of 765 An. gambiae and An. coluzzii specimens collected from across Africa. We used t-SNE, a recently popularized dimensionality reduction method, to create a 2D-map of An. gambiae and An. coluzzii genes that reflect their population structure similarities. Results The map allows intuitive navigation among genes distributed throughout the so-called “mainland” and numerous surrounding “island-like” gene clusters. These gene clusters of various sizes correspond predominantly to low recombination genomic regions such as inversions and centromeres, and also to recent selective sweeps. Because this mosquito species complex has been studied extensively, we were able to support our interpretations with previously published findings. Several novel observations and hypotheses are also made, including selective sweeps and a multi-locus selection event in Guinea-Bissau, a known intense hybridization zone between An. gambiae and An. coluzzii. Conclusions Our results present a rich dataset that could be utilized in functional investigations aiming to shed light onto An. gambiae s.l genome evolution and eventual speciation. In addition, the methodology presented here can be used to further characterize other species not so well studied as An. gambiae, shortening the time required to progress from field sampling to the identification of genes and genomic regions under unique evolutionary processes.

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Identification of multiple male reproductive tract-specific proteins that regulate sperm migration through the oviduct in mice

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1908736116 ◽

2019 ◽

Vol 116 (37) ◽

pp. 18498-18506 ◽

Cited By ~ 13

Author(s):

Yoshitaka Fujihara ◽

Taichi Noda ◽

Kiyonori Kobayashi ◽

Asami Oji ◽

Sumire Kobayashi ◽

...

Keyword(s):

Membrane Protein ◽

Male Fertility ◽

Reproductive Tract ◽

Gene Families ◽

Gene Clusters ◽

Mutant Mice ◽

Male Reproductive Tract ◽

Sperm Migration ◽

Specific Proteins ◽

Multiple Male

CRISPR/Cas9-mediated genome editing technology enables researchers to efficiently generate and analyze genetically modified animals. We have taken advantage of this game-changing technology to uncover essential factors for fertility. In this study, we generated knockouts (KOs) of multiple male reproductive organ-specific genes and performed phenotypic screening of these null mutant mice to attempt to identify proteins essential for male fertility. We focused on making large deletions (dels) within 2 gene clusters encoding cystatin (CST) and prostate and testis expressed (PATE) proteins and individual gene mutations in 2 other gene families encoding glycerophosphodiester phosphodiesterase domain (GDPD) containing and lymphocyte antigen 6 (Ly6)/Plaur domain (LYPD) containing proteins. These gene families were chosen because many of the genes demonstrate male reproductive tract-specific expression. AlthoughGdpd1andGdpd4mutant mice were fertile, disruptions ofCstandPategene clusters andLypd4resulted in male sterility or severe fertility defects secondary to impaired sperm migration through the oviduct. While absence of the epididymal protein families CST and PATE affect the localization of the sperm membrane protein A disintegrin and metallopeptidase domain 3 (ADAM3), the sperm acrosomal membrane protein LYPD4 regulates sperm fertilizing ability via an ADAM3-independent pathway. Thus, use of CRISPR/Cas9 technologies has allowed us to quickly rule in and rule out proteins required for male fertility and expand our list of male-specific proteins that function in sperm migration through the oviduct.

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Trichothecene Genotypes of Fusarium graminearum Populations Isolated from Winter Wheat Crops in Serbia

Toxins ◽

10.3390/toxins10110460 ◽

2018 ◽

Vol 10 (11) ◽

pp. 460 ◽

Cited By ~ 1

Author(s):

Vesna Krnjaja ◽

Slavica Stanković ◽

Ana Obradović ◽

Tanja Petrović ◽

Violeta Mandić ◽

...

Keyword(s):

Fusarium Graminearum ◽

Gene Clusters ◽

Sensu Stricto ◽

Molecular Techniques ◽

Weather Data ◽

Morphological Observation ◽

Specific Primer ◽

Head Blight ◽

As Species ◽

Species Specific

Fusarium graminearum as the main causal agent of Fusarium head blight (FHB) and its ability to produce trichothecenes was investigated by molecular techniques. A total of 37 strains isolated from the wheat, harvested in Serbia in 2005, 2008 and 2015, and previously designated by morphological observation as F. graminearum, were used for trichothecene genotypes characterization. The strains were identified using the species-specific primer set FG16R/FG16F while genotypic characterization was done using specific TRI13 and TRI3 sequences of the trichothecene gene clusters. The PCR assays identified all strains as species of F. graminearum sensu stricto with the DON/15-ADON genotype. The quantification of the mycotoxin (DON) was performed using the biochemical assay. The high levels of DON (>20,000 µg kg−1) were recorded in all of the strains from 2005, four strains from 2008 and two strains from 2015. Weather data of the investigated seasons, showed that the optimal temperature, frequent rains and high relative humidity (RH) was very favourable for the development of F. graminearum, affecting the DON biosynthesis.

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Giant African snail genomes provide insights into molluscan whole-genome duplication and aquatic-terrestrial transition

10.1101/2020.02.02.930693 ◽

2020 ◽

Cited By ~ 2

Author(s):

Conghui Liu ◽

Yuwei Ren ◽

Zaiyuan Li ◽

Qi Hu ◽

Lijuan Yin ◽

...

Keyword(s):

Whole Genome Duplication ◽

Genome Duplication ◽

Terrestrial Ecosystems ◽

Gene Families ◽

Gene Clusters ◽

Immune Defense ◽

Whole Genome ◽

Genomic Plasticity ◽

Ecological Adaptability ◽

Chromosome Level

AbstractWhole-genome duplication (WGD) has been observed across a wide variety of eukaryotic groups, contributing to evolutionary diversity and environmental adaptability. Mollusks are the second largest group of animals, and are among the organisms that have successfully adapted to the nonmarine realm through aquatic-terrestrial (A-T) transition, and no comprehensive research on WGD has been reported in this group. To explore WGD and the A-T transition in Mollusca, we assembled a chromosome-level reference genome for the giant African snail Achatina immaculata, a global invasive species, and compared the genomes of two giant African snails (A. immaculata and Achatina fulica) to the other available mollusk genomes. The chromosome-level macrosynteny, colinearity blocks, Ks peak and Hox gene clusters collectively suggested the occurrence of a WGD event shared by A. immaculata and A. fulica. The estimated timing of this WGD event (∼70 MYA) was close to the speciation age of the Sigmurethra-Orthurethra (within Stylommatophora) lineage and the Cretaceous-Tertiary (K-T) mass extinction, indicating that the WGD reported herein may have been a common event shared by all Sigmurethra-Orthurethra species and could have conferred ecological adaptability and genomic plasticity allowing the survival of the K-T extinction. Based on macrosynteny, we deduced an ancestral karyotype containing 8 conserved clusters for the Gastropoda-Bivalvia lineage. To reveal the mechanism of WGD in shaping adaptability to terrestrial ecosystems, we investigated gene families related to the respiration, aestivation and immune defense of giant African snails. Several mucus-related gene families expanded early in the Stylommatophora lineage, functioning in water retention, immune defense and wound healing. The hemocyanins, PCK and FBP families were doubled and retained after WGD, enhancing the capacity for gas exchange and glucose homeostasis in aestivation. After the WGD, zinc metalloproteinase genes were highly tandemly duplicated to protect tissue against ROS damage. This evidence collectively suggests that although the WGD may not have been the direct driver of the A-T transition, it provided an important legacy for the terrestrial adaptation of the giant African snail.

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Fusarium graminearum Possesses Virulence Factors Common to Fusarium Head Blight of Wheat and Seedling Rot of Soybean but Differing in Their Impact on Disease Severity

Phytopathology ◽

10.1094/phyto-12-13-0355-r ◽

2014 ◽

Vol 104 (11) ◽

pp. 1201-1207 ◽

Cited By ~ 23

Author(s):

Luca Sella ◽

Katia Gazzetti ◽

Carla Castiglioni ◽

Wilhelm Schäfer ◽

Francesco Favaron

Keyword(s):

Fusarium Head Blight ◽

Disease Severity ◽

Fusarium Graminearum ◽

Map Kinases ◽

Early Stage ◽

Single Gene ◽

Crown Rot ◽

Head Blight ◽

Soybean Seedlings ◽

Seedling Rot

Fusarium graminearum is a toxigenic fungal pathogen that causes Fusarium head blight (FHB) and crown rot on cereal crops worldwide. This fungus also causes damping-off and crown and root rots at the early stage of crop development in soybean cultivated in North and South America. Several F. graminearum genes were investigated for their contribution to FHB in cereals but no inherent study is reported for the dicotyledonous soybean host. In this study we determined the disease severity on soybean seedlings of five single gene disrupted mutants of F. graminearum, previously characterized in wheat spike infection. Three of these mutants are impaired on a specific function as the production of deoxynivalenol (DON, Δtri5), lipase (ΔFgl1), and xylanase (Δxyl03624), while the remaining two are MAP kinase mutants (ΔFgOS-2, Δgpmk1), which are altered in signaling pathways. The mutants that were reduced in virulence (Δtri5, ΔFgl1, and ΔFgOS-2) or are avirulent (Δgpmk1) on wheat were correspondently less virulent or avirulent in soybean seedlings, as shown by the extension of lesions and seedling lengths. The Δxyl03624 mutant was as virulent as the wild type mirroring the behavior observed in wheat. However, a different ranking of symptom severity occurred in the two hosts: the ΔFgOS-2 mutant, that infects wheat spikelets similarly to Δtri5 and ΔFgl1 mutants, provided much reduced symptoms in soybean. Differently from the other mutants, we observed that the ΔFgOS-2 mutant was several fold more sensitive to the glyceollin phytoalexin suggesting that its reduced virulence may be due to its hypersensitivity to this phytoalexin. In conclusion, lipase and DON seem important for full disease symptom development in soybean seedlings, OS-2 and Gpmk1 MAP kinases are essential for virulence, and OS-2 is involved in conferring resistance to the soybean phytoalexin.

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