Modular assembly of transposable element arrays by microsatellite targeting in the guayule and rice genomes

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Abstract

Background

Guayule ( Parthenium argentatum A. Gray) is a rubber-producing desert shrub native to Mexico and the United States. Guayule represents an alternative to Hevea brasiliensis as a source for commercial natural rubber. The efficient application of modern molecular/genetic tools to guayule improvement requires characterization of its genome.

Results

The 1.6 Gb guayule genome was sequenced, assembled and annotated. The final 1.5 Gb assembly, while fragmented (N ₅₀ = 22 kb), maps > 95% of the shotgun reads and is essentially complete. Approximately 40,000 transcribed, protein encoding genes were annotated on the assembly. Further characterization of this genome revealed 15 families of small, microsatellite-associated, transposable elements (TEs) with unexpected chromosomal distribution profiles. These SaTar ( Satellite Targeted) elements, which are non-autonomous Mu-like elements (MULEs), were frequently observed in multimeric linear arrays of unrelated individual elements within which no individual element is interrupted by another. This uniformly non-nested TE multimer architecture has not been previously described in either eukaryotic or prokaryotic genomes. Five families of similarly distributed non-autonomous MULEs (microsatellite associated, modularly assembled) were characterized in the rice genome. Families of TEs with similar structures and distribution profiles were identified in sorghum and citrus.

Conclusion

The sequencing and assembly of the guayule genome provides a foundation for application of current crop improvement technologies to this plant. In addition, characterization of this genome revealed SaTar elements with distribution profiles unique among TEs. Satar targeting appears based on an alternative MULE recombination mechanism with the potential to impact gene evolution.

Electronic supplementary material

The online version of this article (10.1186/s12864-018-4653-6) contains supplementary material, which is available to authorized users.

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Most cited references 33

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The Sorghum bicolor genome and the diversification of grasses.

Andrew Paterson, John Bowers, Rémy Bruggmann … (2009)

Sorghum, an African grass related to sugar cane and maize, is grown for food, feed, fibre and fuel. We present an initial analysis of the approximately 730-megabase Sorghum bicolor (L.) Moench genome, placing approximately 98% of genes in their chromosomal context using whole-genome shotgun sequence validated by genetic, physical and syntenic information. Genetic recombination is largely confined to about one-third of the sorghum genome with gene order and density similar to those of rice. Retrotransposon accumulation in recombinationally recalcitrant heterochromatin explains the approximately 75% larger genome size of sorghum compared with rice. Although gene and repetitive DNA distributions have been preserved since palaeopolyploidization approximately 70 million years ago, most duplicated gene sets lost one member before the sorghum-rice divergence. Concerted evolution makes one duplicated chromosomal segment appear to be only a few million years old. About 24% of genes are grass-specific and 7% are sorghum-specific. Recent gene and microRNA duplications may contribute to sorghum's drought tolerance.

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A draft sequence of the rice genome (Oryza sativa L. ssp. indica).

J. Yu (2002)

We have produced a draft sequence of the rice genome for the most widely cultivated subspecies in China, Oryza sativa L. ssp. indica, by whole-genome shotgun sequencing. The genome was 466 megabases in size, with an estimated 46,022 to 55,615 genes. Functional coverage in the assembled sequences was 92.0%. About 42.2% of the genome was in exact 20-nucleotide oligomer repeats, and most of the transposons were in the intergenic regions between genes. Although 80.6% of predicted Arabidopsis thaliana genes had a homolog in rice, only 49.4% of predicted rice genes had a homolog in A. thaliana. The large proportion of rice genes with no recognizable homologs is due to a gradient in the GC content of rice coding sequences.

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How important are transposons for plant evolution?

Damon Lisch (2013)

For decades, transposable elements have been known to produce a wide variety of changes in plant gene expression and function. This has led to the idea that transposable element activity has played a key part in adaptive plant evolution. This Review describes the kinds of changes that transposable elements can cause, discusses evidence that those changes have contributed to plant evolution and suggests future strategies for determining the extent to which these changes have in fact contributed to plant adaptation and evolution. Recent advances in genomics and phenomics for a range of plant species, particularly crops, have begun to allow the systematic assessment of these questions.

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Author and article information

Contributors

José A. Valdes Franco: jav246@cornell.edu

Yi Wang: yi.wang@ars.usda.gov

Naxin Huo: nhuo@ucdavis.edu

Grisel Ponciano: Grisel.Ponciano@ars.usda.gov

Howard A. Colvin: HAColvin@coopertire.com

Colleen M. McMahan: Colleen.McMahan@ars.usda.gov

Yong Q. Gu: yong.gu@ars.usda.gov

William R. Belknap: williamrbelknap32@gmail.com

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 19 April 2018

Publication date PMC-release: 19 April 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 271

Affiliations

[1 ]ISNI 0000 0001 2203 0321, GRID grid.411455.0, Universidad Autónoma de Nuevo León, ; Monterrey, NL Mexico

[2 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, USDA-Agricultural Research Service, Western Regional Research Center, ; Albany, CA USA

[3 ]GRID grid.426887.7, Cooper Tire & Rubber Company, ; Findlay, OH USA

[4 ]ISNI 000000041936877X, GRID grid.5386.8, Present Address: Plant Breeding and Genetics Section, School of Integrative Plant Science, , Cornell University, ; Ithaca, NY USA

Article

Publisher ID: 4653

DOI: 10.1186/s12864-018-4653-6

PMC ID: 5907723

PubMed ID: 29673330

SO-VID: 78ca91a4-fe47-43b7-9650-1784159f5ddc

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 : 30 August 2017

Date accepted : 10 April 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;

Award ID: 2012-10006

Award Recipient : Colleen M. McMahan

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: natural rubber,genome,assembly,annotation,class ii transposable element,non-autonomous,transposon

Data availability:

ScienceOpen disciplines: Genetics

Keywords: natural rubber, genome, assembly, annotation, class ii transposable element, non-autonomous, transposon

Modular assembly of transposable element arrays by microsatellite targeting in the guayule and rice genomes

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Abstract

Background

Results

Conclusion

Electronic supplementary material

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Genome Integrity

Most cited references 33

The Sorghum bicolor genome and the diversification of grasses.

A draft sequence of the rice genome (Oryza sativa L. ssp. indica).

How important are transposons for plant evolution?

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