Genomic Evidence for Rediploidization and Adaptive Evolution Following the Whole-genome Triplication

Overview

Journal Nat Commun

Specialty Biology

Date 2024 Feb 22

PMID 38388712

Authors

Xiao Feng

Qipian Chen

Weihong Wu

Jiexin Wang

Guohong Li

Shaohua Xu

Shao Shao

Min Liu

Cairong Zhong

Chung-I Wu

Suhua Shi

Ziwen He

Affiliations

Soon will be listed here.

Abstract

Whole-genome duplication (WGD), or polyploidy, events are widespread and significant in the evolutionary history of angiosperms. However, empirical evidence for rediploidization, the major process where polyploids give rise to diploid descendants, is still lacking at the genomic level. Here we present chromosome-scale genomes of the mangrove tree Sonneratia alba and the related inland plant Lagerstroemia speciosa. Their common ancestor has experienced a whole-genome triplication (WGT) approximately 64 million years ago coinciding with a period of dramatic global climate change. Sonneratia, adapting mangrove habitats, experienced extensive chromosome rearrangements post-WGT. We observe the WGT retentions display sequence and expression divergence, suggesting potential neo- and sub-functionalization. Strong selection acting on three-copy retentions indicates adaptive value in response to new environments. To elucidate the role of ploidy changes in genome evolution, we improve a model of the polyploidization-rediploidization process based on genomic evidence, contributing to the understanding of adaptive evolution during climate change.

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References

He Z, Xu S, Zhang Z, Guo W, Lyu H, Zhong C . Convergent adaptation of the genomes of woody plants at the land-sea interface. Natl Sci Rev. 2021; 7(6):978-993. PMC: 8289059. DOI: 10.1093/nsr/nwaa027. View

Liang Y, Li F, Gao Q, Jin C, Dong L, Wang Q . The genome of Eustoma grandiflorum reveals the whole-genome triplication event contributing to ornamental traits in cultivated lisianthus. Plant Biotechnol J. 2022; 20(10):1856-1858. PMC: 9491457. DOI: 10.1111/pbi.13899. View

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

Rice A, Smarda P, Novosolov M, Drori M, Glick L, Sabath N . The global biogeography of polyploid plants. Nat Ecol Evol. 2019; 3(2):265-273. DOI: 10.1038/s41559-018-0787-9. View

Han E, Petrella D, Blakeslee J . 'Bending' models of halotropism: incorporating protein phosphatase 2A, ABCB transporters, and auxin metabolism. J Exp Bot. 2017; 68(12):3071-3089. DOI: 10.1093/jxb/erx127. View

Jaillon O, Aury J, Noel B, Policriti A, Clepet C, Casagrande A . The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449(7161):463-7. DOI: 10.1038/nature06148. View

Castresana J . Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17(4):540-52. DOI: 10.1093/oxfordjournals.molbev.a026334. View

Ebadi M, Bafort Q, Mizrachi E, Audenaert P, Simoens P, Van Montagu M . The duplication of genomes and genetic networks and its potential for evolutionary adaptation and survival during environmental turmoil. Proc Natl Acad Sci U S A. 2023; 120(41):e2307289120. PMC: 10576144. DOI: 10.1073/pnas.2307289120. View

Vanneste K, Baele G, Maere S, Van de Peer Y . Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 2014; 24(8):1334-47. PMC: 4120086. DOI: 10.1101/gr.168997.113. View

10.

Pont C, Wagner S, Kremer A, Orlando L, Plomion C, Salse J . Paleogenomics: reconstruction of plant evolutionary trajectories from modern and ancient DNA. Genome Biol. 2019; 20(1):29. PMC: 6369560. DOI: 10.1186/s13059-019-1627-1. View

11.

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B . AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34(Web Server issue):W435-9. PMC: 1538822. DOI: 10.1093/nar/gkl200. View

12.

Ou S, Jiang N . LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons. Plant Physiol. 2017; 176(2):1410-1422. PMC: 5813529. DOI: 10.1104/pp.17.01310. View

13.

Iorizzo M, Ellison S, Senalik D, Zeng P, Satapoomin P, Huang J . A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet. 2016; 48(6):657-66. DOI: 10.1038/ng.3565. View

14.

Lyu H, He Z, Wu C, Shi S . Convergent adaptive evolution in marginal environments: unloading transposable elements as a common strategy among mangrove genomes. New Phytol. 2017; 217(1):428-438. DOI: 10.1111/nph.14784. View

15.

Rice A, Glick L, Abadi S, Einhorn M, Kopelman N, Salman-Minkov A . The Chromosome Counts Database (CCDB) - a community resource of plant chromosome numbers. New Phytol. 2014; 206(1):19-26. DOI: 10.1111/nph.13191. View

16.

Song A, Su J, Wang H, Zhang Z, Zhang X, Van de Peer Y . Analyses of a chromosome-scale genome assembly reveal the origin and evolution of cultivated chrysanthemum. Nat Commun. 2023; 14(1):2021. PMC: 10085997. DOI: 10.1038/s41467-023-37730-3. View

17.

Roulin A, Auer P, Libault M, Schlueter J, Farmer A, May G . The fate of duplicated genes in a polyploid plant genome. Plant J. 2012; 73(1):143-53. DOI: 10.1111/tpj.12026. View

18.

Bowers J, Paterson A . Chromosome number is key to longevity of polyploid lineages. New Phytol. 2021; 231(1):19-28. DOI: 10.1111/nph.17361. View

19.

Wang D, Zhang Y, Zhang Z, Zhu J, Yu J . KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics. 2010; 8(1):77-80. PMC: 5054116. DOI: 10.1016/S1672-0229(10)60008-3. View

20.

Bock D, Kane N, Ebert D, Rieseberg L . Genome skimming reveals the origin of the Jerusalem Artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phytol. 2013; 201(3):1021-1030. DOI: 10.1111/nph.12560. View