Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs

NC Ereful, L-Y Liu, E Tsai, S-M Kao, S Dixit, R Mauleon, K Malabanan, M Thomson, A Laurena, D Lee, I Mackay, A Greenland, W Powell, H Leung

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    Abstract

    Background
    Information on the effect of stress on the allele-specific expression (ASE) profile of rice hybrids is limited. More so, the association of allelically imbalanced genes to important traits is yet to be understood. Here we assessed allelic imbalance (AI) in the heterozygote state of rice under non- and water-stress treatments and determined association of asymmetrically expressed genes with grain yield (GY) under drought stress by in-silico co-localization analysis and selective genotyping. The genotypes IR64, Apo and their F1 hybrid (IR64 × Apo) were grown under normal and water-limiting conditions. We sequenced the total RNA transcripts for all genotypes then reconstructed the two chromosomes in the heterozygote.

    Results
    We are able to estimate the transcript abundance of and the differential expression (DE) between the two parent-specific alleles in the rice hybrids. The magnitude and direction of AI are classified into two categories: (1) symmetrical or biallelic and (2) asymmetrical. The latter can be further classified as either IR64- or Apo-favoring gene. Analysis showed that in the hybrids grown under non-stress conditions, 179 and 183 favor Apo- and IR64-specific alleles, respectively. Hence, the number of IR64- and Apo-favoring genes is relatively equal. Under water-stress conditions, 179 and 255 favor Apo- and IR64-specific alleles, respectively, indicating that the number of allelically imbalanced genes is skewed towards IR64. This is nearly 40–60 % preference for Apo and IR64 alleles, respectively, to the hybrid transcriptome. We also observed genes which exhibit allele preference switching when exposed to water-stress conditions. Results of in-silico co-localization procedure and selective genotyping of Apo/IR64 F3:5 progenies revealed significant association of several asymmetrically expressed genes with GY under drought stress conditions.

    Conclusion
    Our data suggest that water stress skews AI on a genome-wide scale towards the IR64 allele, the cross-specific maternal allele. Several asymmetrically expressed genes are strongly associated with GY under drought stress which may shed hints that genes associated with important traits are allelically imbalanced. Our approach of integrating hybrid expression analysis and QTL mapping analysis may be an efficient strategy for shortlisting candidate genes for gene discovery.
    Original languageEnglish
    Number of pages15
    JournalRice
    Volume9
    Issue number50
    Early online date26 Sep 2016
    DOIs
    Publication statusPrint publication - 2016

    Fingerprint

    Allelic Imbalance
    Drought
    Droughts
    Dehydration
    water stress
    quantitative trait loci
    rice
    Genes
    drought
    allele
    Alleles
    Water
    gene
    alleles
    genes
    drought stress
    Heterozygote
    grain yield
    Computer Simulation
    genotyping

    Keywords

    • Allele-specific expression (ASE)
    • Allelic imbalance (AI)
    • Co-localization analysis
    • Drought
    • Quantitative trait loci (QTL)
    • RNA-seq
    • Rice (Oryza sativa L.)
    • Selective genotyping

    Cite this

    Ereful, NC ; Liu, L-Y ; Tsai, E ; Kao, S-M ; Dixit, S ; Mauleon, R ; Malabanan, K ; Thomson, M ; Laurena, A ; Lee, D ; Mackay, I ; Greenland, A ; Powell, W ; Leung, H. / Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs. In: Rice. 2016 ; Vol. 9, No. 50.
    @article{0e5018b9ed474de98177d18c78ee9b4d,
    title = "Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs",
    abstract = "BackgroundInformation on the effect of stress on the allele-specific expression (ASE) profile of rice hybrids is limited. More so, the association of allelically imbalanced genes to important traits is yet to be understood. Here we assessed allelic imbalance (AI) in the heterozygote state of rice under non- and water-stress treatments and determined association of asymmetrically expressed genes with grain yield (GY) under drought stress by in-silico co-localization analysis and selective genotyping. The genotypes IR64, Apo and their F1 hybrid (IR64 × Apo) were grown under normal and water-limiting conditions. We sequenced the total RNA transcripts for all genotypes then reconstructed the two chromosomes in the heterozygote.ResultsWe are able to estimate the transcript abundance of and the differential expression (DE) between the two parent-specific alleles in the rice hybrids. The magnitude and direction of AI are classified into two categories: (1) symmetrical or biallelic and (2) asymmetrical. The latter can be further classified as either IR64- or Apo-favoring gene. Analysis showed that in the hybrids grown under non-stress conditions, 179 and 183 favor Apo- and IR64-specific alleles, respectively. Hence, the number of IR64- and Apo-favoring genes is relatively equal. Under water-stress conditions, 179 and 255 favor Apo- and IR64-specific alleles, respectively, indicating that the number of allelically imbalanced genes is skewed towards IR64. This is nearly 40–60 {\%} preference for Apo and IR64 alleles, respectively, to the hybrid transcriptome. We also observed genes which exhibit allele preference switching when exposed to water-stress conditions. Results of in-silico co-localization procedure and selective genotyping of Apo/IR64 F3:5 progenies revealed significant association of several asymmetrically expressed genes with GY under drought stress conditions.ConclusionOur data suggest that water stress skews AI on a genome-wide scale towards the IR64 allele, the cross-specific maternal allele. Several asymmetrically expressed genes are strongly associated with GY under drought stress which may shed hints that genes associated with important traits are allelically imbalanced. Our approach of integrating hybrid expression analysis and QTL mapping analysis may be an efficient strategy for shortlisting candidate genes for gene discovery.",
    keywords = "Allele-specific expression (ASE), Allelic imbalance (AI), Co-localization analysis, Drought, Quantitative trait loci (QTL), RNA-seq, Rice (Oryza sativa L.), Selective genotyping",
    author = "NC Ereful and L-Y Liu and E Tsai and S-M Kao and S Dixit and R Mauleon and K Malabanan and M Thomson and A Laurena and D Lee and I Mackay and A Greenland and W Powell and H Leung",
    year = "2016",
    doi = "10.1186/s12284-016-0123-4",
    language = "English",
    volume = "9",
    journal = "Rice",
    issn = "1939-8425",
    publisher = "SpringerOpen",
    number = "50",

    }

    Ereful, NC, Liu, L-Y, Tsai, E, Kao, S-M, Dixit, S, Mauleon, R, Malabanan, K, Thomson, M, Laurena, A, Lee, D, Mackay, I, Greenland, A, Powell, W & Leung, H 2016, 'Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs', Rice, vol. 9, no. 50. https://doi.org/10.1186/s12284-016-0123-4

    Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs. / Ereful, NC; Liu, L-Y; Tsai, E; Kao, S-M; Dixit, S; Mauleon, R; Malabanan, K; Thomson, M; Laurena, A; Lee, D; Mackay, I; Greenland, A; Powell, W; Leung, H.

    In: Rice, Vol. 9, No. 50, 2016.

    Research output: Contribution to journalArticleResearchpeer-review

    TY - JOUR

    T1 - Analysis of allelic imbalance in rice hybrids under water stress and association of asymmetrically expressed genes with drought-response QTLs

    AU - Ereful, NC

    AU - Liu, L-Y

    AU - Tsai, E

    AU - Kao, S-M

    AU - Dixit, S

    AU - Mauleon, R

    AU - Malabanan, K

    AU - Thomson, M

    AU - Laurena, A

    AU - Lee, D

    AU - Mackay, I

    AU - Greenland, A

    AU - Powell, W

    AU - Leung, H

    PY - 2016

    Y1 - 2016

    N2 - BackgroundInformation on the effect of stress on the allele-specific expression (ASE) profile of rice hybrids is limited. More so, the association of allelically imbalanced genes to important traits is yet to be understood. Here we assessed allelic imbalance (AI) in the heterozygote state of rice under non- and water-stress treatments and determined association of asymmetrically expressed genes with grain yield (GY) under drought stress by in-silico co-localization analysis and selective genotyping. The genotypes IR64, Apo and their F1 hybrid (IR64 × Apo) were grown under normal and water-limiting conditions. We sequenced the total RNA transcripts for all genotypes then reconstructed the two chromosomes in the heterozygote.ResultsWe are able to estimate the transcript abundance of and the differential expression (DE) between the two parent-specific alleles in the rice hybrids. The magnitude and direction of AI are classified into two categories: (1) symmetrical or biallelic and (2) asymmetrical. The latter can be further classified as either IR64- or Apo-favoring gene. Analysis showed that in the hybrids grown under non-stress conditions, 179 and 183 favor Apo- and IR64-specific alleles, respectively. Hence, the number of IR64- and Apo-favoring genes is relatively equal. Under water-stress conditions, 179 and 255 favor Apo- and IR64-specific alleles, respectively, indicating that the number of allelically imbalanced genes is skewed towards IR64. This is nearly 40–60 % preference for Apo and IR64 alleles, respectively, to the hybrid transcriptome. We also observed genes which exhibit allele preference switching when exposed to water-stress conditions. Results of in-silico co-localization procedure and selective genotyping of Apo/IR64 F3:5 progenies revealed significant association of several asymmetrically expressed genes with GY under drought stress conditions.ConclusionOur data suggest that water stress skews AI on a genome-wide scale towards the IR64 allele, the cross-specific maternal allele. Several asymmetrically expressed genes are strongly associated with GY under drought stress which may shed hints that genes associated with important traits are allelically imbalanced. Our approach of integrating hybrid expression analysis and QTL mapping analysis may be an efficient strategy for shortlisting candidate genes for gene discovery.

    AB - BackgroundInformation on the effect of stress on the allele-specific expression (ASE) profile of rice hybrids is limited. More so, the association of allelically imbalanced genes to important traits is yet to be understood. Here we assessed allelic imbalance (AI) in the heterozygote state of rice under non- and water-stress treatments and determined association of asymmetrically expressed genes with grain yield (GY) under drought stress by in-silico co-localization analysis and selective genotyping. The genotypes IR64, Apo and their F1 hybrid (IR64 × Apo) were grown under normal and water-limiting conditions. We sequenced the total RNA transcripts for all genotypes then reconstructed the two chromosomes in the heterozygote.ResultsWe are able to estimate the transcript abundance of and the differential expression (DE) between the two parent-specific alleles in the rice hybrids. The magnitude and direction of AI are classified into two categories: (1) symmetrical or biallelic and (2) asymmetrical. The latter can be further classified as either IR64- or Apo-favoring gene. Analysis showed that in the hybrids grown under non-stress conditions, 179 and 183 favor Apo- and IR64-specific alleles, respectively. Hence, the number of IR64- and Apo-favoring genes is relatively equal. Under water-stress conditions, 179 and 255 favor Apo- and IR64-specific alleles, respectively, indicating that the number of allelically imbalanced genes is skewed towards IR64. This is nearly 40–60 % preference for Apo and IR64 alleles, respectively, to the hybrid transcriptome. We also observed genes which exhibit allele preference switching when exposed to water-stress conditions. Results of in-silico co-localization procedure and selective genotyping of Apo/IR64 F3:5 progenies revealed significant association of several asymmetrically expressed genes with GY under drought stress conditions.ConclusionOur data suggest that water stress skews AI on a genome-wide scale towards the IR64 allele, the cross-specific maternal allele. Several asymmetrically expressed genes are strongly associated with GY under drought stress which may shed hints that genes associated with important traits are allelically imbalanced. Our approach of integrating hybrid expression analysis and QTL mapping analysis may be an efficient strategy for shortlisting candidate genes for gene discovery.

    KW - Allele-specific expression (ASE)

    KW - Allelic imbalance (AI)

    KW - Co-localization analysis

    KW - Drought

    KW - Quantitative trait loci (QTL)

    KW - RNA-seq

    KW - Rice (Oryza sativa L.)

    KW - Selective genotyping

    U2 - 10.1186/s12284-016-0123-4

    DO - 10.1186/s12284-016-0123-4

    M3 - Article

    VL - 9

    JO - Rice

    JF - Rice

    SN - 1939-8425

    IS - 50

    ER -