Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.

BACKGROUND:Hybrid weakness, a phenomenon opposite to heterosis, refers to inferior growth and development in a hybrid relative to its pure-line parents. Little attention has been paid to the phenomenological or mechanistic aspect of hybrid weakness, probably due to its rare occurrence. METHODOLOGY/P...

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Main Authors: Shuai Sun, Ying Wu, Xiuyun Lin, Jie Wang, Jiamiao Yu, Yue Sun, Yiling Miao, Qiuping Li, Karen A Sanguinet, Bao Liu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5332110?pdf=render
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spelling doaj-81aa80a2965f4380940edb478ca3d5112020-11-25T01:01:30ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01123e017291910.1371/journal.pone.0172919Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.Shuai SunYing WuXiuyun LinJie WangJiamiao YuYue SunYiling MiaoQiuping LiKaren A SanguinetBao LiuBACKGROUND:Hybrid weakness, a phenomenon opposite to heterosis, refers to inferior growth and development in a hybrid relative to its pure-line parents. Little attention has been paid to the phenomenological or mechanistic aspect of hybrid weakness, probably due to its rare occurrence. METHODOLOGY/PRINCIPAL FINDINGS:Here, using a set of interspecific triploid F1 hybrids between Oryza sativa, ssp. japonica (genome AA) and a tetraploid wild rice species, O. alta (genome, CCDD), we investigated the phenotypic and physiological differences between the F1 hybrids and their parents under normal and nitrogen-limiting conditions. We quantified the expression levels of 21 key genes involved in three important pathways pertinent to the assayed phenotypic and physiological traits by real-time qRT-PCR. Further, we assayed expression partitioning of parental alleles for eight genes in the F1 hybrids relative to the in silico "hybrids" (parental cDNA mixture) under both normal and N-limiting conditions by using locus-specific cDNA pyrosequencing. CONCLUSIONS/SIGNIFICANCE:We report that the F1 hybrids showed weakness in several phenotypic traits at the final seedling-stage compared with their corresponding mid-parent values (MPVs). Nine of the 21 studied genes showed contrasted expression levels between hybrids and parents (MPVs) under normal vs. N-limiting conditions. Interestingly, under N-limiting conditions, the overtly enhanced partitioning of maternal allele expression in the hybrids for eight assayed genes echo their attenuated hybrid weakness in phenotypes, an observation further bolstered by more resemblance of hybrids to the maternal parent under N-limiting conditions compared to normal conditions in a suite of measured physiological traits. Our observations suggest that both overall expression level and differential partitioning of parental alleles of critical genes contribute to condition-specific hybrid weakness.http://europepmc.org/articles/PMC5332110?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Shuai Sun
Ying Wu
Xiuyun Lin
Jie Wang
Jiamiao Yu
Yue Sun
Yiling Miao
Qiuping Li
Karen A Sanguinet
Bao Liu
spellingShingle Shuai Sun
Ying Wu
Xiuyun Lin
Jie Wang
Jiamiao Yu
Yue Sun
Yiling Miao
Qiuping Li
Karen A Sanguinet
Bao Liu
Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
PLoS ONE
author_facet Shuai Sun
Ying Wu
Xiuyun Lin
Jie Wang
Jiamiao Yu
Yue Sun
Yiling Miao
Qiuping Li
Karen A Sanguinet
Bao Liu
author_sort Shuai Sun
title Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
title_short Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
title_full Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
title_fullStr Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
title_full_unstemmed Hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
title_sort hybrid weakness in a rice interspecific hybrid is nitrogen-dependent, and accompanied by changes in gene expression at both total transcript level and parental allele partitioning.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2017-01-01
description BACKGROUND:Hybrid weakness, a phenomenon opposite to heterosis, refers to inferior growth and development in a hybrid relative to its pure-line parents. Little attention has been paid to the phenomenological or mechanistic aspect of hybrid weakness, probably due to its rare occurrence. METHODOLOGY/PRINCIPAL FINDINGS:Here, using a set of interspecific triploid F1 hybrids between Oryza sativa, ssp. japonica (genome AA) and a tetraploid wild rice species, O. alta (genome, CCDD), we investigated the phenotypic and physiological differences between the F1 hybrids and their parents under normal and nitrogen-limiting conditions. We quantified the expression levels of 21 key genes involved in three important pathways pertinent to the assayed phenotypic and physiological traits by real-time qRT-PCR. Further, we assayed expression partitioning of parental alleles for eight genes in the F1 hybrids relative to the in silico "hybrids" (parental cDNA mixture) under both normal and N-limiting conditions by using locus-specific cDNA pyrosequencing. CONCLUSIONS/SIGNIFICANCE:We report that the F1 hybrids showed weakness in several phenotypic traits at the final seedling-stage compared with their corresponding mid-parent values (MPVs). Nine of the 21 studied genes showed contrasted expression levels between hybrids and parents (MPVs) under normal vs. N-limiting conditions. Interestingly, under N-limiting conditions, the overtly enhanced partitioning of maternal allele expression in the hybrids for eight assayed genes echo their attenuated hybrid weakness in phenotypes, an observation further bolstered by more resemblance of hybrids to the maternal parent under N-limiting conditions compared to normal conditions in a suite of measured physiological traits. Our observations suggest that both overall expression level and differential partitioning of parental alleles of critical genes contribute to condition-specific hybrid weakness.
url http://europepmc.org/articles/PMC5332110?pdf=render
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