Whole-Genome Sequence of Synthesized Allopolyploids in Reveals Insights into the Genome Evolution of Allopolyploidization

Overview

Journal Adv Sci (Weinh)

Specialty Biomedical Engineering

Date 2021 May 12

PMID 33977063

Citations 13

Authors

Xiaqing Yu

Panqiao Wang

Ji Li

Qinzheng Zhao

Changmian Ji

Zaobing Zhu

Yufei Zhai

Xiaodong Qin

Junguo Zhou

Haiyan Yu

Xinchao Cheng

Shiro Isshiki

Molly Jahn

Jeff J Doyle

Carl-Otto Ottosen

Yuling Bai

Qinsheng Cai

Chunyan Cheng

Qunfeng Lou

Sanwen Huang

Jinfeng Chen

Affiliations

Soon will be listed here.

Abstract

The importance of allopolyploidy in plant evolution has been widely recognized. The genetic changes triggered by allopolyploidy, however, are not yet fully understood due to inconsistent phenomena reported across diverse species. The construction of synthetic polyploids offers a controlled approach to systematically reveal genomic changes that occur during the process of polyploidy. This study reports the first fully sequenced synthetic allopolyploid constructed from a cross between and , with high-quality assembly. The two subgenomes are confidently partitioned and the -originated subgenome predominates over the -originated subgenome, retaining more sequences and showing higher homeologous gene expression. Most of the genomic changes emerge immediately after interspecific hybridization. Analysis of a series of genome sequences from several generations (S, S-S) of . × confirms that genomic changes occurred in the very first generations, subsequently slowing down as the process of diploidization is initiated. The duplicated genome of the allopolyploid with double genes from both parents broadens the genetic base of . ×, resulting in enhanced phenotypic plasticity. This study provides novel insights into plant polyploid genome evolution and demonstrates a promising strategy for the development of a wide array of novel plant species and varieties through artificial polyploidization.

Citing Articles

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References

Wang Y, Zhao Q, Qin X, Yang S, Li Z, Li J . Identification of all homoeologous chromosomes of newly synthetic allotetraploid Cucumis × hytivus and its wild parent reveals stable subgenome structure. Chromosoma. 2017; 126(6):713-728. DOI: 10.1007/s00412-017-0635-8. View

Lowe T, Eddy S . tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25(5):955-64. PMC: 146525. DOI: 10.1093/nar/25.5.955. View

Kagale S, Koh C, Nixon J, Bollina V, Clarke W, Tuteja R . The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Commun. 2014; 5:3706. PMC: 4015329. DOI: 10.1038/ncomms4706. View

Leitch A, Leitch I . Genomic plasticity and the diversity of polyploid plants. Science. 2008; 320(5875):481-3. DOI: 10.1126/science.1153585. View

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. 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

Cave-Radet A, Salmon A, Lima O, Ainouche M, El Amrani A . Increased tolerance to organic xenobiotics following recent allopolyploidy in Spartina (Poaceae). Plant Sci. 2019; 280:143-154. DOI: 10.1016/j.plantsci.2018.11.005. View

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

Fopa Fomeju B, Falentin C, Lassalle G, Manzanares-Dauleux M, Delourme R . Homoeologous duplicated regions are involved in quantitative resistance of Brassica napus to stem canker. BMC Genomics. 2014; 15:498. PMC: 4082613. DOI: 10.1186/1471-2164-15-498. View

10.

Buggs R, Chamala S, Wu W, Tate J, Schnable P, Soltis D . Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr Biol. 2012; 22(3):248-52. DOI: 10.1016/j.cub.2011.12.027. View

11.

Boetzer M, Henkel C, Jansen H, Butler D, Pirovano W . Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2010; 27(4):578-9. DOI: 10.1093/bioinformatics/btq683. View

12.

Lam E, Hastie A, Lin C, Ehrlich D, Das S, Austin M . Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat Biotechnol. 2012; 30(8):771-6. PMC: 3817024. DOI: 10.1038/nbt.2303. View

13.

Goulas Y, Cerovic Z, Cartelat A, Moya I . Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence. Appl Opt. 2004; 43(23):4488-96. DOI: 10.1364/ao.43.004488. View

14.

Cerovic Z, Masdoumier G, Ben Ghozlen N, Latouche G . A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant. 2012; 146(3):251-60. PMC: 3666089. DOI: 10.1111/j.1399-3054.2012.01639.x. View

15.

Hegarty M, Barker G, Wilson I, Abbott R, Edwards K, Hiscock S . Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Curr Biol. 2006; 16(16):1652-9. DOI: 10.1016/j.cub.2006.06.071. View

16.

Lynch M, Conery J . The evolutionary fate and consequences of duplicate genes. Science. 2000; 290(5494):1151-5. DOI: 10.1126/science.290.5494.1151. View

17.

Yu X, Wang P, Li J, Zhao Q, Ji C, Zhu Z . Whole-Genome Sequence of Synthesized Allopolyploids in Reveals Insights into the Genome Evolution of Allopolyploidization. Adv Sci (Weinh). 2021; 8(9):2004222. PMC: 8097326. DOI: 10.1002/advs.202004222. View

18.

Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J . SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2013; 1(1):18. PMC: 3626529. DOI: 10.1186/2047-217X-1-18. View

19.

Tham C, Tirado-Magallanes R, Goh Y, Fullwood M, Koh B, Wang W . NanoVar: accurate characterization of patients' genomic structural variants using low-depth nanopore sequencing. Genome Biol. 2020; 21(1):56. PMC: 7055087. DOI: 10.1186/s13059-020-01968-7. View

20.

Keilwagen J, Wenk M, Erickson J, Schattat M, Grau J, Hartung F . Using intron position conservation for homology-based gene prediction. Nucleic Acids Res. 2016; 44(9):e89. PMC: 4872089. DOI: 10.1093/nar/gkw092. View