Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants

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Abstract

Background

The sharp increase of plant genome and transcriptome data provide valuable resources to investigate evolutionary consequences of gene duplication in a range of taxa, and unravel common principles underlying duplicate gene retention.

Results

We survey 141 sequenced plant genomes to elucidate consequences of gene and genome duplication, processes central to the evolution of biodiversity. We develop a pipeline named DupGen_finder to identify different modes of gene duplication in plants. Genes derived from whole-genome, tandem, proximal, transposed, or dispersed duplication differ in abundance, selection pressure, expression divergence, and gene conversion rate among genomes. The number of WGD-derived duplicate genes decreases exponentially with increasing age of duplication events—transposed duplication- and dispersed duplication-derived genes declined in parallel. In contrast, the frequency of tandem and proximal duplications showed no significant decrease over time, providing a continuous supply of variants available for adaptation to continuously changing environments. Moreover, tandem and proximal duplicates experienced stronger selective pressure than genes formed by other modes and evolved toward biased functional roles involved in plant self-defense. The rate of gene conversion among WGD-derived gene pairs declined over time, peaking shortly after polyploidization. To provide a platform for accessing duplicated gene pairs in different plants, we constructed the Plant Duplicate Gene Database.

Conclusions

We identify a comprehensive landscape of different modes of gene duplication across the plant kingdom by comparing 141 genomes, which provides a solid foundation for further investigation of the dynamic evolution of duplicate genes.

Electronic supplementary material

The online version of this article (10.1186/s13059-019-1650-2) contains supplementary material, which is available to authorized users.

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Kazutaka Katoh, Daron Standley (2013)

We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.

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Nicolas Bray, Harold Pimentel, Páll Melsted … (2016)

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MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity

Yupeng Wang, Haibao Tang, Jeremy D. DeBarry … (2012)

MCScan is an algorithm able to scan multiple genomes or subgenomes in order to identify putative homologous chromosomal regions, and align these regions using genes as anchors. The MCScanX toolkit implements an adjusted MCScan algorithm for detection of synteny and collinearity that extends the original software by incorporating 14 utility programs for visualization of results and additional downstream analyses. Applications of MCScanX to several sequenced plant genomes and gene families are shown as examples. MCScanX can be used to effectively analyze chromosome structural changes, and reveal the history of gene family expansions that might contribute to the adaptation of lineages and taxa. An integrated view of various modes of gene duplication can supplement the traditional gene tree analysis in specific families. The source code and documentation of MCScanX are freely available at http://chibba.pgml.uga.edu/mcscan2/.

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Author and article information

Contributors

Xin Qiao: 2014204010@njau.edu.cn

Qionghou Li: 2017104043@njau.edu.cn

Hao Yin: yinhao@njau.edu.cn

Kaijie Qi: qikaijie@njau.edu.cn

Leiting Li: lileiting@gmail.com

Runze Wang: 2016204009@njau.edu.cn

Shaoling Zhang: slzhang@njau.edu.cn

Andrew H. Paterson: paterson@uga.edu

Journal

Journal ID (nlm-ta): Genome Biol

Journal ID (iso-abbrev): Genome Biol

Title: Genome Biology

Publisher: BioMed Central (London )

ISSN (Print): 1474-7596

ISSN (Electronic): 1474-760X

Publication date (Electronic): 21 February 2019

Publication date PMC-release: 21 February 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 38

Affiliations

[1 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Centre of Pear Engineering Technology Research, State Key Laboratory of Crop Genetics and Germplasm Enhancement, , Nanjing Agricultural University, ; Nanjing, 210095 China

[2 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Plant Genome Mapping Laboratory, , University of Georgia, ; Athens, GA 30605 USA

Article

Publisher ID: 1650

DOI: 10.1186/s13059-019-1650-2

PMC ID: 6383267

PubMed ID: 30791939

SO-VID: 5ecf68a8-d284-4948-a17f-d1e68ceb13de

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 May 2018

Date accepted : 8 February 2019