The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut

Abstract Background The ascomycete fungus Anisogramma anomala causes Eastern Filbert Blight (EFB) on hazelnut (Corylus spp.) trees. It is a minor disease on its native host, the American hazelnut (C. americana), but is highly destructive on the commercially important European hazelnut (C. avellana)....

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Main Authors: Alanna B. Cohen, Guohong Cai, Dana C. Price, Thomas J. Molnar, Ning Zhang, Bradley I. Hillman
Format: Article
Language:English
Published: BMC 2024-04-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10198-1
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author Alanna B. Cohen
Guohong Cai
Dana C. Price
Thomas J. Molnar
Ning Zhang
Bradley I. Hillman
author_facet Alanna B. Cohen
Guohong Cai
Dana C. Price
Thomas J. Molnar
Ning Zhang
Bradley I. Hillman
author_sort Alanna B. Cohen
collection DOAJ
description Abstract Background The ascomycete fungus Anisogramma anomala causes Eastern Filbert Blight (EFB) on hazelnut (Corylus spp.) trees. It is a minor disease on its native host, the American hazelnut (C. americana), but is highly destructive on the commercially important European hazelnut (C. avellana). In North America, EFB has historically limited commercial production of hazelnut to west of the Rocky Mountains. A. anomala is an obligately biotrophic fungus that has not been grown in continuous culture, rendering its study challenging. There is a 15-month latency before symptoms appear on infected hazelnut trees, and only a sexual reproductive stage has been observed. Here we report the sequencing, annotation, and characterization of its genome. Results The genome of A. anomala was assembled into 108 scaffolds totaling 342,498,352 nt with a GC content of 34.46%. Scaffold N50 was 33.3 Mb and L50 was 5. Nineteen scaffolds with lengths over 1 Mb constituted 99% of the assembly. Telomere sequences were identified on both ends of two scaffolds and on one end of another 10 scaffolds. Flow cytometry estimated the genome size of A. anomala at 370 Mb. The genome exhibits two-speed evolution, with 93% of the assembly as AT-rich regions (32.9% GC) and the other 7% as GC-rich (57.1% GC). The AT-rich regions consist predominantly of repeats with low gene content, while 90% of predicted protein coding genes were identified in GC-rich regions. Copia-like retrotransposons accounted for more than half of the genome. Evidence of repeat-induced point mutation (RIP) was identified throughout the AT-rich regions, and two copies of the rid gene and one of dim-2, the key genes in the RIP mutation pathway, were identified in the genome. Consistent with its homothallic sexual reproduction cycle, both MAT1-1 and MAT1-2 idiomorphs were found. We identified a large suite of genes likely involved in pathogenicity, including 614 carbohydrate active enzymes, 762 secreted proteins and 165 effectors. Conclusions This study reveals the genomic structure, composition, and putative gene function of the important pathogen A. anomala. It provides insight into the molecular basis of the pathogen’s life cycle and a solid foundation for studying EFB.
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spelling doaj.art-b4cdfa542dac4e33a24a56318ef0c2582024-04-07T11:09:15ZengBMCBMC Genomics1471-21642024-04-0125112010.1186/s12864-024-10198-1The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnutAlanna B. Cohen0Guohong Cai1Dana C. Price2Thomas J. Molnar3Ning Zhang4Bradley I. Hillman5Department of Plant Biology, Rutgers The State University of New JerseyCrop Production and Pest Control Research Unit, USDA-ARSDepartment of Entomology, Rutgers The State University of New JerseyDepartment of Plant Biology, Rutgers The State University of New JerseyDepartment of Plant Biology, Rutgers The State University of New JerseyDepartment of Plant Biology, Rutgers The State University of New JerseyAbstract Background The ascomycete fungus Anisogramma anomala causes Eastern Filbert Blight (EFB) on hazelnut (Corylus spp.) trees. It is a minor disease on its native host, the American hazelnut (C. americana), but is highly destructive on the commercially important European hazelnut (C. avellana). In North America, EFB has historically limited commercial production of hazelnut to west of the Rocky Mountains. A. anomala is an obligately biotrophic fungus that has not been grown in continuous culture, rendering its study challenging. There is a 15-month latency before symptoms appear on infected hazelnut trees, and only a sexual reproductive stage has been observed. Here we report the sequencing, annotation, and characterization of its genome. Results The genome of A. anomala was assembled into 108 scaffolds totaling 342,498,352 nt with a GC content of 34.46%. Scaffold N50 was 33.3 Mb and L50 was 5. Nineteen scaffolds with lengths over 1 Mb constituted 99% of the assembly. Telomere sequences were identified on both ends of two scaffolds and on one end of another 10 scaffolds. Flow cytometry estimated the genome size of A. anomala at 370 Mb. The genome exhibits two-speed evolution, with 93% of the assembly as AT-rich regions (32.9% GC) and the other 7% as GC-rich (57.1% GC). The AT-rich regions consist predominantly of repeats with low gene content, while 90% of predicted protein coding genes were identified in GC-rich regions. Copia-like retrotransposons accounted for more than half of the genome. Evidence of repeat-induced point mutation (RIP) was identified throughout the AT-rich regions, and two copies of the rid gene and one of dim-2, the key genes in the RIP mutation pathway, were identified in the genome. Consistent with its homothallic sexual reproduction cycle, both MAT1-1 and MAT1-2 idiomorphs were found. We identified a large suite of genes likely involved in pathogenicity, including 614 carbohydrate active enzymes, 762 secreted proteins and 165 effectors. Conclusions This study reveals the genomic structure, composition, and putative gene function of the important pathogen A. anomala. It provides insight into the molecular basis of the pathogen’s life cycle and a solid foundation for studying EFB.https://doi.org/10.1186/s12864-024-10198-1AscomycetePlant pathogenRepeat-induced point mutationMating type geneTransposonEffector
spellingShingle Alanna B. Cohen
Guohong Cai
Dana C. Price
Thomas J. Molnar
Ning Zhang
Bradley I. Hillman
The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
BMC Genomics
Ascomycete
Plant pathogen
Repeat-induced point mutation
Mating type gene
Transposon
Effector
title The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
title_full The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
title_fullStr The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
title_full_unstemmed The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
title_short The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut
title_sort massive 340 megabase genome of anisogramma anomala a biotrophic ascomycete that causes eastern filbert blight of hazelnut
topic Ascomycete
Plant pathogen
Repeat-induced point mutation
Mating type gene
Transposon
Effector
url https://doi.org/10.1186/s12864-024-10198-1
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