Understanding Brassicaceae Evolution Through Ancestral Genome Reconstruction

Overview

Journal Genome Biol

Specialties Biology
Genetics

Date 2015 Dec 15

PMID 26653025

Citations 39

Authors

Florent Murat

Alexandra Louis

Florian Maumus

Alix Armero

Richard Cooke

Hadi Quesneville

Hugues Roest Crollius

Jerome Salse

Affiliations

Soon will be listed here.

Abstract

Background: Brassicaceae is a family of green plants of high scientific and economic interest, including thale cress (Arabidopsis thaliana), cruciferous vegetables (cabbages) and rapeseed.

Results: We reconstruct an evolutionary framework of Brassicaceae composed of high-resolution ancestral karyotypes using the genomes of modern A. thaliana, Arabidopsis lyrata, Capsella rubella, Brassica rapa and Thellungiella parvula. The ancestral Brassicaceae karyotype (Brassicaceae lineages I and II) is composed of eight protochromosomes and 20,037 ordered and oriented protogenes. After speciation, it evolved into the ancestral Camelineae karyotype (eight protochromosomes and 22,085 ordered protogenes) and the proto-Calepineae karyotype (seven protochromosomes and 21,035 ordered protogenes) genomes.

Conclusions: The three inferred ancestral karyotype genomes are shown here to be powerful tools to unravel the reticulated evolutionary history of extant Brassicaceae genomes regarding the fate of ancestral genes and genomic compartments, particularly centromeres and evolutionary breakpoints. This new resource should accelerate research in comparative genomics and translational research by facilitating the transfer of genomic information from model systems to species of agronomic interest.

Citing Articles

Altering cold-regulated gene expression decouples the salicylic acid-growth trade-off in Arabidopsis.

Ortega M, Celoy R, Chacon F, Yuan Y, Xue L, Pandey S Plant Cell. 2024; 36(10):4293-4308.

PMID: 39056470 PMC: 11448890. DOI: 10.1093/plcell/koae210.

Genome-wide identification and evolution of the tubulin gene family in Camelina sativa.

Blume R, Rabokon A, Pydiura M, Yemets A, Pirko Y, Blume Y BMC Genomics. 2024; 25(1):599.

PMID: 38877397 PMC: 11177405. DOI: 10.1186/s12864-024-10503-y.

First draft reference genome and annotation of the alternative oil species Physaria fendleri.

Johnston C, Horn P, Alonso A G3 (Bethesda). 2024; 14(9).

PMID: 38805698 PMC: 11373644. DOI: 10.1093/g3journal/jkae114.

A pan-genome of 69 Arabidopsis thaliana accessions reveals a conserved genome structure throughout the global species range.

Lian Q, Huettel B, Walkemeier B, Mayjonade B, Lopez-Roques C, Gil L Nat Genet. 2024; 56(5):982-991.

PMID: 38605175 PMC: 11096106. DOI: 10.1038/s41588-024-01715-9.

Genomes of Meniocus linifolius and Tetracme quadricornis reveal the ancestral karyotype and genomic features of core Brassicaceae.

Liu J, Zhou S, Liu Y, Zhao B, Yu D, Zhong M Plant Commun. 2024; 5(7):100878.

PMID: 38475995 PMC: 11287156. DOI: 10.1016/j.xplc.2024.100878.

References

Haudry A, Platts A, Vello E, Hoen D, Leclercq M, Williamson R . An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet. 2013; 45(8):891-8. DOI: 10.1038/ng.2684. View

Murat F, Xu J, Tannier E, Abrouk M, Guilhot N, Pont C . Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 2010; 20(11):1545-57. PMC: 2963818. DOI: 10.1101/gr.109744.110. View

Cheng F, Wu J, Fang L, Wang X . Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci. 2012; 3:198. PMC: 3430884. DOI: 10.3389/fpls.2012.00198. View

Louis A, Murat F, Salse J, Crollius H . GenomicusPlants: a web resource to study genome evolution in flowering plants. Plant Cell Physiol. 2014; 56(1):e4. PMC: 4301744. DOI: 10.1093/pcp/pcu177. View

Wallace I, OSullivan O, Higgins D, Notredame C . M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res. 2006; 34(6):1692-9. PMC: 1410914. DOI: 10.1093/nar/gkl091. View

Wang X, Wang H, Sun R, Wu J, Liu S, Bai Y . The genome of the mesopolyploid crop species Brassica rapa. Nat Genet. 2011; 43(10):1035-9. DOI: 10.1038/ng.919. View

Kersey P, Staines D, Lawson D, Kulesha E, Derwent P, Humphrey J . Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res. 2011; 40(Database issue):D91-7. PMC: 3245118. DOI: 10.1093/nar/gkr895. View

Edger P, Pires J . Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res. 2009; 17(5):699-717. DOI: 10.1007/s10577-009-9055-9. View

Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J . Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011; 43(10):956-63. DOI: 10.1038/ng.911. View

10.

Fang L, Cheng F, Wu J, Wang X . The Impact of Genome Triplication on Tandem Gene Evolution in Brassica rapa. Front Plant Sci. 2012; 3:261. PMC: 3509317. DOI: 10.3389/fpls.2012.00261. View

11.

Papp B, Pal C, Hurst L . Dosage sensitivity and the evolution of gene families in yeast. Nature. 2003; 424(6945):194-7. DOI: 10.1038/nature01771. View

12.

Lysak M, Cheung K, Kitschke M, Bures P . Ancestral chromosomal blocks are triplicated in Brassiceae species with varying chromosome number and genome size. Plant Physiol. 2007; 145(2):402-10. PMC: 2048728. DOI: 10.1104/pp.107.104380. View

13.

Bailey C, Koch M, Mayer M, Mummenhoff K, OKane Jr S, Warwick S . Toward a global phylogeny of the Brassicaceae. Mol Biol Evol. 2006; 23(11):2142-60. DOI: 10.1093/molbev/msl087. View

14.

Koenig D, Weigel D . Beyond the thale: comparative genomics and genetics of Arabidopsis relatives. Nat Rev Genet. 2015; 16(5):285-98. DOI: 10.1038/nrg3883. View

15.

Yang Z . PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24(8):1586-91. DOI: 10.1093/molbev/msm088. View

16.

Koch M, Kiefer M . Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species--Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am J Bot. 2011; 92(4):761-7. DOI: 10.3732/ajb.92.4.761. View

17.

Yang J, Osman K, Iqbal M, Stekel D, Luo Z, Armstrong S . Inferring the Brassica rapa Interactome Using Protein-Protein Interaction Data from Arabidopsis thaliana. Front Plant Sci. 2013; 3:297. PMC: 3537189. DOI: 10.3389/fpls.2012.00297. View

18.

Lysak M, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I . Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci U S A. 2006; 103(13):5224-9. PMC: 1458822. DOI: 10.1073/pnas.0510791103. View

19.

Beilstein M, Al-Shehbaz I, Kellogg E . Brassicaceae phylogeny and trichome evolution. Am J Bot. 2011; 93(4):607-19. DOI: 10.3732/ajb.93.4.607. View

20.

Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B . The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun. 2014; 5:3657. PMC: 4071752. DOI: 10.1038/ncomms4657. View