Living apart together

Crosstalk between the core and supernumerary genomes in a fungal plant pathogen

Adriaan Vanheule, Kris Audenaert, Sven Warris, Henri van de Geest, Elio Schijlen, Monica Höfte, Sarah De Saeger, Geert Haesaert, Cees Waalwijk, Theo van der Lee*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

21 Citations (Scopus)

Abstract

Background: Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this. Results: Here we use single-molecule real-time (SMRT) sequencing to assemble the genome of a prominent fungal wheat pathogen, Fusarium poae, including at least one supernumerary chromosome. The core genome contains limited transposable elements (TEs) and no gene duplications, while the supernumerary genome holds up to 25 % TEs and multiple gene duplications. The core genome shows all hallmarks of repeat-induced point mutation (RIP), a defense mechanism against TEs, specific for fungi. The absence of RIP on the supernumerary genome accounts for the differences between the two (sub)genomes, and results in a functional crosstalk between them. The supernumerary genome is a reservoir for TEs that migrate to the core genome, and even large blocks of supernumerary sequence (>200 kb) have recently translocated to the core. Vice versa, the supernumerary genome acts as a refuge for genes that are duplicated from the core genome. Conclusions: For the first time, a mechanism was determined that explains the differences that exist between the core and supernumerary genome in fungi. Different biology rather than origin was shown to be responsible. A "living apart together" crosstalk exists between the core and supernumerary genome, accelerating chromosomal and organismal evolution.

Original languageEnglish
Article number670
Number of pages18
JournalBMC Genomics
Volume17
DOIs
Publication statusPublished - 2016

Fingerprint

Genome
DNA Transposable Elements
Chromosomes
Gene Duplication
Fungi
Point Mutation
Fusarium
Eukaryota
Triticum
DNA

Keywords

  • Fusarium
  • Gene duplications
  • Repeat-induced point mutation
  • Single-molecule real-time sequencing
  • Supernumerary chromosomes
  • Translocation
  • Transposable elements

Cite this

Vanheule, Adriaan ; Audenaert, Kris ; Warris, Sven ; van de Geest, Henri ; Schijlen, Elio ; Höfte, Monica ; De Saeger, Sarah ; Haesaert, Geert ; Waalwijk, Cees ; van der Lee, Theo. / Living apart together : Crosstalk between the core and supernumerary genomes in a fungal plant pathogen. In: BMC Genomics. 2016 ; Vol. 17.
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title = "Living apart together: Crosstalk between the core and supernumerary genomes in a fungal plant pathogen",
abstract = "Background: Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this. Results: Here we use single-molecule real-time (SMRT) sequencing to assemble the genome of a prominent fungal wheat pathogen, Fusarium poae, including at least one supernumerary chromosome. The core genome contains limited transposable elements (TEs) and no gene duplications, while the supernumerary genome holds up to 25 {\%} TEs and multiple gene duplications. The core genome shows all hallmarks of repeat-induced point mutation (RIP), a defense mechanism against TEs, specific for fungi. The absence of RIP on the supernumerary genome accounts for the differences between the two (sub)genomes, and results in a functional crosstalk between them. The supernumerary genome is a reservoir for TEs that migrate to the core genome, and even large blocks of supernumerary sequence (>200 kb) have recently translocated to the core. Vice versa, the supernumerary genome acts as a refuge for genes that are duplicated from the core genome. Conclusions: For the first time, a mechanism was determined that explains the differences that exist between the core and supernumerary genome in fungi. Different biology rather than origin was shown to be responsible. A {"}living apart together{"} crosstalk exists between the core and supernumerary genome, accelerating chromosomal and organismal evolution.",
keywords = "Fusarium, Gene duplications, Repeat-induced point mutation, Single-molecule real-time sequencing, Supernumerary chromosomes, Translocation, Transposable elements",
author = "Adriaan Vanheule and Kris Audenaert and Sven Warris and {van de Geest}, Henri and Elio Schijlen and Monica H{\"o}fte and {De Saeger}, Sarah and Geert Haesaert and Cees Waalwijk and {van der Lee}, Theo",
year = "2016",
doi = "10.1186/s12864-016-2941-6",
language = "English",
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Living apart together : Crosstalk between the core and supernumerary genomes in a fungal plant pathogen. / Vanheule, Adriaan; Audenaert, Kris; Warris, Sven; van de Geest, Henri; Schijlen, Elio; Höfte, Monica; De Saeger, Sarah; Haesaert, Geert; Waalwijk, Cees; van der Lee, Theo.

In: BMC Genomics, Vol. 17, 670, 2016.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Living apart together

T2 - Crosstalk between the core and supernumerary genomes in a fungal plant pathogen

AU - Vanheule, Adriaan

AU - Audenaert, Kris

AU - Warris, Sven

AU - van de Geest, Henri

AU - Schijlen, Elio

AU - Höfte, Monica

AU - De Saeger, Sarah

AU - Haesaert, Geert

AU - Waalwijk, Cees

AU - van der Lee, Theo

PY - 2016

Y1 - 2016

N2 - Background: Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this. Results: Here we use single-molecule real-time (SMRT) sequencing to assemble the genome of a prominent fungal wheat pathogen, Fusarium poae, including at least one supernumerary chromosome. The core genome contains limited transposable elements (TEs) and no gene duplications, while the supernumerary genome holds up to 25 % TEs and multiple gene duplications. The core genome shows all hallmarks of repeat-induced point mutation (RIP), a defense mechanism against TEs, specific for fungi. The absence of RIP on the supernumerary genome accounts for the differences between the two (sub)genomes, and results in a functional crosstalk between them. The supernumerary genome is a reservoir for TEs that migrate to the core genome, and even large blocks of supernumerary sequence (>200 kb) have recently translocated to the core. Vice versa, the supernumerary genome acts as a refuge for genes that are duplicated from the core genome. Conclusions: For the first time, a mechanism was determined that explains the differences that exist between the core and supernumerary genome in fungi. Different biology rather than origin was shown to be responsible. A "living apart together" crosstalk exists between the core and supernumerary genome, accelerating chromosomal and organismal evolution.

AB - Background: Eukaryotes display remarkable genome plasticity, which can include supernumerary chromosomes that differ markedly from the core chromosomes. Despite the widespread occurrence of supernumerary chromosomes in fungi, their origin, relation to the core genome and the reason for their divergent characteristics are still largely unknown. The complexity of genome assembly due to the presence of repetitive DNA partially accounts for this. Results: Here we use single-molecule real-time (SMRT) sequencing to assemble the genome of a prominent fungal wheat pathogen, Fusarium poae, including at least one supernumerary chromosome. The core genome contains limited transposable elements (TEs) and no gene duplications, while the supernumerary genome holds up to 25 % TEs and multiple gene duplications. The core genome shows all hallmarks of repeat-induced point mutation (RIP), a defense mechanism against TEs, specific for fungi. The absence of RIP on the supernumerary genome accounts for the differences between the two (sub)genomes, and results in a functional crosstalk between them. The supernumerary genome is a reservoir for TEs that migrate to the core genome, and even large blocks of supernumerary sequence (>200 kb) have recently translocated to the core. Vice versa, the supernumerary genome acts as a refuge for genes that are duplicated from the core genome. Conclusions: For the first time, a mechanism was determined that explains the differences that exist between the core and supernumerary genome in fungi. Different biology rather than origin was shown to be responsible. A "living apart together" crosstalk exists between the core and supernumerary genome, accelerating chromosomal and organismal evolution.

KW - Fusarium

KW - Gene duplications

KW - Repeat-induced point mutation

KW - Single-molecule real-time sequencing

KW - Supernumerary chromosomes

KW - Translocation

KW - Transposable elements

U2 - 10.1186/s12864-016-2941-6

DO - 10.1186/s12864-016-2941-6

M3 - Article

VL - 17

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

M1 - 670

ER -