Cargando…

Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)

Hybridization in plants results in phenotypic and genotypic perturbations that can have dramatic effects on hybrid physiology, ecology, and overall fitness. Hybridization can also perturb epigenetic control of transposable elements, resulting in their proliferation. Understanding the mechanisms that...

Descripción completa

Detalles Bibliográficos
Autores principales: Heyduk, Karolina, McAssey, Edward V., Grimwood, Jane, Shu, Shengqiang, Schmutz, Jeremy, McKain, Michael R., Leebens-Mack, Jim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843428/
https://www.ncbi.nlm.nih.gov/pubmed/33519836
http://dx.doi.org/10.3389/fpls.2020.573767
_version_ 1783644140224905216
author Heyduk, Karolina
McAssey, Edward V.
Grimwood, Jane
Shu, Shengqiang
Schmutz, Jeremy
McKain, Michael R.
Leebens-Mack, Jim
author_facet Heyduk, Karolina
McAssey, Edward V.
Grimwood, Jane
Shu, Shengqiang
Schmutz, Jeremy
McKain, Michael R.
Leebens-Mack, Jim
author_sort Heyduk, Karolina
collection PubMed
description Hybridization in plants results in phenotypic and genotypic perturbations that can have dramatic effects on hybrid physiology, ecology, and overall fitness. Hybridization can also perturb epigenetic control of transposable elements, resulting in their proliferation. Understanding the mechanisms that maintain genomic integrity after hybridization is often confounded by changes in ploidy that occur in hybrid plant species. Homoploid hybrid species, which have no change in chromosome number relative to their parents, offer an opportunity to study the genomic consequences of hybridization in the absence of change in ploidy. Yucca gloriosa (Asparagaceae) is a young homoploid hybrid species, resulting from a cross between Yucca aloifolia and Yucca filamentosa. Previous analyses of ∼11 kb of the chloroplast genome and nuclear-encoded microsatellites implicated a single Y. aloifolia genotype as the maternal parent of Y. gloriosa. Using whole genome resequencing, we assembled chloroplast genomes from 41 accessions of all three species to re-assess the hybrid origins of Y. gloriosa. We further used re-sequencing data to annotate transposon abundance in the three species and mRNA-seq to analyze transcription of transposons. The chloroplast phylogeny and haplotype analysis suggest multiple hybridization events contributing to the origin of Y. gloriosa, with both parental species acting as the maternal donor. Transposon abundance at the superfamily level was significantly different between the three species; the hybrid was frequently intermediate to the parental species in TE superfamily abundance or appeared more similar to one or the other parent. In only one case—Copia LTR transposons—did Y. gloriosa have a significantly higher abundance relative to either parent. Expression patterns across the three species showed little increased transcriptional activity of transposons, suggesting that either no transposon release occurred in Y. gloriosa upon hybridization, or that any transposons that were activated via hybridization were rapidly silenced. The identification and quantification of transposon families paired with expression evidence paves the way for additional work seeking to link epigenetics with the important trait variation seen in this homoploid hybrid system.
format Online
Article
Text
id pubmed-7843428
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-78434282021-01-30 Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae) Heyduk, Karolina McAssey, Edward V. Grimwood, Jane Shu, Shengqiang Schmutz, Jeremy McKain, Michael R. Leebens-Mack, Jim Front Plant Sci Plant Science Hybridization in plants results in phenotypic and genotypic perturbations that can have dramatic effects on hybrid physiology, ecology, and overall fitness. Hybridization can also perturb epigenetic control of transposable elements, resulting in their proliferation. Understanding the mechanisms that maintain genomic integrity after hybridization is often confounded by changes in ploidy that occur in hybrid plant species. Homoploid hybrid species, which have no change in chromosome number relative to their parents, offer an opportunity to study the genomic consequences of hybridization in the absence of change in ploidy. Yucca gloriosa (Asparagaceae) is a young homoploid hybrid species, resulting from a cross between Yucca aloifolia and Yucca filamentosa. Previous analyses of ∼11 kb of the chloroplast genome and nuclear-encoded microsatellites implicated a single Y. aloifolia genotype as the maternal parent of Y. gloriosa. Using whole genome resequencing, we assembled chloroplast genomes from 41 accessions of all three species to re-assess the hybrid origins of Y. gloriosa. We further used re-sequencing data to annotate transposon abundance in the three species and mRNA-seq to analyze transcription of transposons. The chloroplast phylogeny and haplotype analysis suggest multiple hybridization events contributing to the origin of Y. gloriosa, with both parental species acting as the maternal donor. Transposon abundance at the superfamily level was significantly different between the three species; the hybrid was frequently intermediate to the parental species in TE superfamily abundance or appeared more similar to one or the other parent. In only one case—Copia LTR transposons—did Y. gloriosa have a significantly higher abundance relative to either parent. Expression patterns across the three species showed little increased transcriptional activity of transposons, suggesting that either no transposon release occurred in Y. gloriosa upon hybridization, or that any transposons that were activated via hybridization were rapidly silenced. The identification and quantification of transposon families paired with expression evidence paves the way for additional work seeking to link epigenetics with the important trait variation seen in this homoploid hybrid system. Frontiers Media S.A. 2021-01-15 /pmc/articles/PMC7843428/ /pubmed/33519836 http://dx.doi.org/10.3389/fpls.2020.573767 Text en Copyright © 2021 Heyduk, McAssey, Grimwood, Shu, Schmutz, McKain and Leebens-Mack. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Heyduk, Karolina
McAssey, Edward V.
Grimwood, Jane
Shu, Shengqiang
Schmutz, Jeremy
McKain, Michael R.
Leebens-Mack, Jim
Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title_full Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title_fullStr Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title_full_unstemmed Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title_short Hybridization History and Repetitive Element Content in the Genome of a Homoploid Hybrid, Yucca gloriosa (Asparagaceae)
title_sort hybridization history and repetitive element content in the genome of a homoploid hybrid, yucca gloriosa (asparagaceae)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843428/
https://www.ncbi.nlm.nih.gov/pubmed/33519836
http://dx.doi.org/10.3389/fpls.2020.573767
work_keys_str_mv AT heydukkarolina hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT mcasseyedwardv hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT grimwoodjane hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT shushengqiang hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT schmutzjeremy hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT mckainmichaelr hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae
AT leebensmackjim hybridizationhistoryandrepetitiveelementcontentinthegenomeofahomoploidhybridyuccagloriosaasparagaceae