Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors

Sean P Gordon; Bruno Contreras-Moreira; Joshua J Levy; Armin Djamei; Angelika Czedik-Eysenberg; Virginia S Tartaglio; Adam Session; Joel Martin; Amy Cartwright; Andrew Katz; Vasanth R Singan; Eugene Goltsman; Kerrie Barry; Vinh Ha Dinh-Thi; Boulos Chalhoub; Antonio Diaz-Perez; Ruben Sancho; Joanna Lusinska; Elzbieta Wolny; Candida Nibau; John H Doonan; Luis A J Mur; Chris Plott; Jerry Jenkins; Samuel P Hazen; Scott J Lee; Shengqiang Shu; David Goodstein; Daniel Rokhsar; Jeremy Schmutz; Robert Hasterok; Pilar Catalan; John P Vogel

doi:10.1038/s41467-020-17302-5

Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors

Sean P Gordon, Bruno Contreras-Moreira, Joshua J Levy, Armin Djamei, Angelika Czedik-Eysenberg, Virginia S Tartaglio, Adam Session, Joel Martin, Amy Cartwright, Andrew Katz, Vasanth R Singan, Eugene Goltsman, Kerrie Barry, Vinh Ha Dinh-Thi, Boulos Chalhoub, Antonio Diaz-Perez, Ruben Sancho, Joanna Lusinska, Elzbieta Wolny, Candida NibauJohn H Doonan, Luis A J Mur, Chris Plott, Jerry Jenkins, Samuel P Hazen, Scott J Lee, Shengqiang Shu, David Goodstein, Daniel Rokhsar, Jeremy Schmutz, Robert Hasterok, Pilar Catalan, John P Vogel

Department of Life Sciences

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Abstract

Our understanding of polyploid genome evolution is constrained because we cannot know the exact founders of a particular polyploid. To differentiate between founder effects and post polyploidization evolution, we use a pan-genomic approach to study the allotetraploid Brachypodium hybridum and its diploid progenitors. Comparative analysis suggests that most B. hybridum whole gene presence/absence variation is part of the standing variation in its diploid progenitors. Analysis of nuclear single nucleotide variants, plastomes and k-mers associated with retrotransposons reveals two independent origins for B. hybridum, ~1.4 and ~0.14 million years ago. Examination of gene expression in the younger B. hybridum lineage reveals no bias in overall subgenome expression. Our results are consistent with a gradual accumulation of genomic changes after polyploidization and a lack of subgenome expression dominance. Significantly, if we did not use a pan-genomic approach, we would grossly overestimate the number of genomic changes attributable to post polyploidization evolution.

Original language	English
Article number	3670
Number of pages	16
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-17302-5
Publication status	Published - 29 Jul 2020

Keywords

Brachypodium/genetics
Chromosomes, Plant/genetics
Diploidy
Evolution, Molecular
Genome, Chloroplast
Genome, Plant
Genomics
Hybridization, Genetic
Phylogeny
Polymorphism, Single Nucleotide
Polyploidy
Retroelements/genetics
Species Specificity

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ArticleFinal published version, 2.94 MBLicence: CC BY
Supplementary InformationFinal published version, 2.02 MBLicence: CC BY
Description of Supplementary dataFinal published version, 120 KBLicence: CC BY
Supplementary DataFinal published version, 76.1 MBLicence: CC BY
Source DataFinal published version, 12.5 MBLicence: CC BY

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Gordon, S. P., Contreras-Moreira, B., Levy, J. J., Djamei, A., Czedik-Eysenberg, A., Tartaglio, V. S., Session, A., Martin, J., Cartwright, A., Katz, A., Singan, V. R., Goltsman, E., Barry, K., Dinh-Thi, V. H., Chalhoub, B., Diaz-Perez, A., Sancho, R., Lusinska, J., Wolny, E., ... Vogel, J. P. (2020). Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors. Nature Communications, 11(1), [3670]. https://doi.org/10.1038/s41467-020-17302-5

@article{bdbfcb57e36b4eefa82df207d03b92bb,

title = "Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors",

abstract = "Our understanding of polyploid genome evolution is constrained because we cannot know the exact founders of a particular polyploid. To differentiate between founder effects and post polyploidization evolution, we use a pan-genomic approach to study the allotetraploid Brachypodium hybridum and its diploid progenitors. Comparative analysis suggests that most B. hybridum whole gene presence/absence variation is part of the standing variation in its diploid progenitors. Analysis of nuclear single nucleotide variants, plastomes and k-mers associated with retrotransposons reveals two independent origins for B. hybridum, ~1.4 and ~0.14 million years ago. Examination of gene expression in the younger B. hybridum lineage reveals no bias in overall subgenome expression. Our results are consistent with a gradual accumulation of genomic changes after polyploidization and a lack of subgenome expression dominance. Significantly, if we did not use a pan-genomic approach, we would grossly overestimate the number of genomic changes attributable to post polyploidization evolution.",

keywords = "Brachypodium/genetics, Chromosomes, Plant/genetics, Diploidy, Evolution, Molecular, Genome, Chloroplast, Genome, Plant, Genomics, Hybridization, Genetic, Phylogeny, Polymorphism, Single Nucleotide, Polyploidy, Retroelements/genetics, Species Specificity",

author = "Gordon, {Sean P} and Bruno Contreras-Moreira and Levy, {Joshua J} and Armin Djamei and Angelika Czedik-Eysenberg and Tartaglio, {Virginia S} and Adam Session and Joel Martin and Amy Cartwright and Andrew Katz and Singan, {Vasanth R} and Eugene Goltsman and Kerrie Barry and Dinh-Thi, {Vinh Ha} and Boulos Chalhoub and Antonio Diaz-Perez and Ruben Sancho and Joanna Lusinska and Elzbieta Wolny and Candida Nibau and Doonan, {John H} and Mur, {Luis A J} and Chris Plott and Jerry Jenkins and Hazen, {Samuel P} and Lee, {Scott J} and Shengqiang Shu and David Goodstein and Daniel Rokhsar and Jeremy Schmutz and Robert Hasterok and Pilar Catalan and Vogel, {John P}",

note = "Funding Information: We thank Jeremy Phillips and Joseph Carlson for assistance with setting up analysis pipelines, Dovetail Genomics for improving the ABR113 genome assembly and Madison Dunlap for assistance with HipMer assembly. The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231 and User Agreement No. FP00006675 between the University of Zaragoza (User) and the DOE (Community Science Program 503504 proposal); S.J. was supported by the DOE Office of Science Graduate Student Research Program; P.C., B.C.-M., A.D.P., and R.S. were supported by a Spanish Ministry of Economy and Competitiveness grant CGL2016-79790-P; P.C., A.D.P., and R.S. were supported by a Bioflora A01-17 grant co-funded by the Spanish Aragon Government and the European Social Fund. R.H., E.W., and J.L. were supported by the National Science Centre Poland (grants DEC-2012/04/A/NZ3/00572 and DEC-2014/14/M/NZ2/00519). J.H.D. and C.N. were supported by Leverhulme Trust (grant no. 10754). A.C.E. and A.D. were supported by the European Research Council under the European Union{\textquoteright}s Seventh Framework Program (FP7/2007-2013)/ERC grant agreement no [GA335691 “Effec-tomics”], the Austrian Science Fund (FWF): [P27429-B22, P27818-B22, I 3033-B22], and the Austrian Academy of Science (OEAW). Publisher Copyright: {\textcopyright} 2020, This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.",

year = "2020",

month = jul,

day = "29",

doi = "10.1038/s41467-020-17302-5",

language = "English",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

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Gordon, SP, Contreras-Moreira, B, Levy, JJ, Djamei, A, Czedik-Eysenberg, A, Tartaglio, VS, Session, A, Martin, J, Cartwright, A, Katz, A, Singan, VR, Goltsman, E, Barry, K, Dinh-Thi, VH, Chalhoub, B, Diaz-Perez, A, Sancho, R, Lusinska, J, Wolny, E, Nibau, C , Doonan, JH , Mur, LAJ, Plott, C, Jenkins, J, Hazen, SP, Lee, SJ, Shu, S, Goodstein, D, Rokhsar, D, Schmutz, J, Hasterok, R, Catalan, P & Vogel, JP 2020, 'Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors', Nature Communications, vol. 11, no. 1, 3670. https://doi.org/10.1038/s41467-020-17302-5

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T1 - Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors

AU - Gordon, Sean P

AU - Contreras-Moreira, Bruno

AU - Levy, Joshua J

AU - Djamei, Armin

AU - Czedik-Eysenberg, Angelika

AU - Tartaglio, Virginia S

AU - Session, Adam

AU - Martin, Joel

AU - Cartwright, Amy

AU - Katz, Andrew

AU - Singan, Vasanth R

AU - Goltsman, Eugene

AU - Barry, Kerrie

AU - Dinh-Thi, Vinh Ha

AU - Chalhoub, Boulos

AU - Diaz-Perez, Antonio

AU - Sancho, Ruben

AU - Lusinska, Joanna

AU - Wolny, Elzbieta

AU - Nibau, Candida

AU - Doonan, John H

AU - Mur, Luis A J

AU - Plott, Chris

AU - Jenkins, Jerry

AU - Hazen, Samuel P

AU - Lee, Scott J

AU - Shu, Shengqiang

AU - Goodstein, David

AU - Rokhsar, Daniel

AU - Schmutz, Jeremy

AU - Hasterok, Robert

AU - Catalan, Pilar

AU - Vogel, John P

N1 - Funding Information: We thank Jeremy Phillips and Joseph Carlson for assistance with setting up analysis pipelines, Dovetail Genomics for improving the ABR113 genome assembly and Madison Dunlap for assistance with HipMer assembly. The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231 and User Agreement No. FP00006675 between the University of Zaragoza (User) and the DOE (Community Science Program 503504 proposal); S.J. was supported by the DOE Office of Science Graduate Student Research Program; P.C., B.C.-M., A.D.P., and R.S. were supported by a Spanish Ministry of Economy and Competitiveness grant CGL2016-79790-P; P.C., A.D.P., and R.S. were supported by a Bioflora A01-17 grant co-funded by the Spanish Aragon Government and the European Social Fund. R.H., E.W., and J.L. were supported by the National Science Centre Poland (grants DEC-2012/04/A/NZ3/00572 and DEC-2014/14/M/NZ2/00519). J.H.D. and C.N. were supported by Leverhulme Trust (grant no. 10754). A.C.E. and A.D. were supported by the European Research Council under the European Union’s Seventh Framework Program (FP7/2007-2013)/ERC grant agreement no [GA335691 “Effec-tomics”], the Austrian Science Fund (FWF): [P27429-B22, P27818-B22, I 3033-B22], and the Austrian Academy of Science (OEAW). Publisher Copyright: © 2020, This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.

PY - 2020/7/29

Y1 - 2020/7/29

N2 - Our understanding of polyploid genome evolution is constrained because we cannot know the exact founders of a particular polyploid. To differentiate between founder effects and post polyploidization evolution, we use a pan-genomic approach to study the allotetraploid Brachypodium hybridum and its diploid progenitors. Comparative analysis suggests that most B. hybridum whole gene presence/absence variation is part of the standing variation in its diploid progenitors. Analysis of nuclear single nucleotide variants, plastomes and k-mers associated with retrotransposons reveals two independent origins for B. hybridum, ~1.4 and ~0.14 million years ago. Examination of gene expression in the younger B. hybridum lineage reveals no bias in overall subgenome expression. Our results are consistent with a gradual accumulation of genomic changes after polyploidization and a lack of subgenome expression dominance. Significantly, if we did not use a pan-genomic approach, we would grossly overestimate the number of genomic changes attributable to post polyploidization evolution.

AB - Our understanding of polyploid genome evolution is constrained because we cannot know the exact founders of a particular polyploid. To differentiate between founder effects and post polyploidization evolution, we use a pan-genomic approach to study the allotetraploid Brachypodium hybridum and its diploid progenitors. Comparative analysis suggests that most B. hybridum whole gene presence/absence variation is part of the standing variation in its diploid progenitors. Analysis of nuclear single nucleotide variants, plastomes and k-mers associated with retrotransposons reveals two independent origins for B. hybridum, ~1.4 and ~0.14 million years ago. Examination of gene expression in the younger B. hybridum lineage reveals no bias in overall subgenome expression. Our results are consistent with a gradual accumulation of genomic changes after polyploidization and a lack of subgenome expression dominance. Significantly, if we did not use a pan-genomic approach, we would grossly overestimate the number of genomic changes attributable to post polyploidization evolution.

KW - Brachypodium/genetics

KW - Chromosomes, Plant/genetics

KW - Diploidy

KW - Evolution, Molecular

KW - Genome, Chloroplast

KW - Genome, Plant

KW - Genomics

KW - Hybridization, Genetic

KW - Phylogeny

KW - Polymorphism, Single Nucleotide

KW - Polyploidy

KW - Retroelements/genetics

KW - Species Specificity

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U2 - 10.1038/s41467-020-17302-5

DO - 10.1038/s41467-020-17302-5

M3 - Article

C2 - 32728126

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3670

ER -

Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors

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BBSRC Core Strategic Programme in Resilient Crops: Oats

Bioinformatics and genomic and phenomic platform development

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Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors

Abstract

Keywords

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BBSRC Core Strategic Programme in Resilient Crops: Oats

Bioinformatics and genomic and phenomic platform development

Cite this