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Analysis of Allelic Imbalance in Rice Hybrids Under Water Stress and Association of Asymmetrically Expressed Genes with Drought-Response QTLs

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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.

Electronic supplementary material: The online version of this article (doi:10.1186/s12284-016-0123-4) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus

Genome-wide analysis of ASE in F1 at (left) non- and (right) water-stress conditions (for 2× fold minimum expression). The right side of both graphs starting from the origin 0 (positive) shows FC values when Apo-specific allele is preferentially expressed over IR64-specific allele; the left side (negative values) when IR64-specific allele is preferentially expressed over Apo-specific allele
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Fig1: Genome-wide analysis of ASE in F1 at (left) non- and (right) water-stress conditions (for 2× fold minimum expression). The right side of both graphs starting from the origin 0 (positive) shows FC values when Apo-specific allele is preferentially expressed over IR64-specific allele; the left side (negative values) when IR64-specific allele is preferentially expressed over Apo-specific allele

Mentions: In summary, the hybrid expresses higher number of genes significantly differentially expressed between the two alleles (at P < 0.05) during water-stress conditions as compared to during normal conditions indicating that water stress enhances gene expression. Our results further suggest that genes exhibiting AI is inherent to the organism regardless of the conditions and is not a consequence of stress. On a genome-wide scale, the number of genes favoring each of the parental alleles approaches a normal distribution curve (using 2.0× fold minimum level of expression; P < 0.05) (Fig. 1). However, at water-limiting conditions, the distribution curve is skewed towards IR64-specific allele – a global distortion of preferential expression. This indicates that more genes favor the maternal over the paternal allele under stress conditions in this particular hybrid cross. It is surprising to note that while Apo is the drought-tolerant genotype, IR64-specific allele is preferentially expressed in the hybrid. This is contrary to our initial speculation that the tolerant genotype (Apo) should exhibit preferential expression in the heterozygote.Fig. 1


Analysis of Allelic Imbalance in Rice Hybrids Under Water Stress and Association of Asymmetrically Expressed Genes with Drought-Response QTLs
Genome-wide analysis of ASE in F1 at (left) non- and (right) water-stress conditions (for 2× fold minimum expression). The right side of both graphs starting from the origin 0 (positive) shows FC values when Apo-specific allele is preferentially expressed over IR64-specific allele; the left side (negative values) when IR64-specific allele is preferentially expressed over Apo-specific allele
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5037104&req=5

Fig1: Genome-wide analysis of ASE in F1 at (left) non- and (right) water-stress conditions (for 2× fold minimum expression). The right side of both graphs starting from the origin 0 (positive) shows FC values when Apo-specific allele is preferentially expressed over IR64-specific allele; the left side (negative values) when IR64-specific allele is preferentially expressed over Apo-specific allele
Mentions: In summary, the hybrid expresses higher number of genes significantly differentially expressed between the two alleles (at P < 0.05) during water-stress conditions as compared to during normal conditions indicating that water stress enhances gene expression. Our results further suggest that genes exhibiting AI is inherent to the organism regardless of the conditions and is not a consequence of stress. On a genome-wide scale, the number of genes favoring each of the parental alleles approaches a normal distribution curve (using 2.0× fold minimum level of expression; P < 0.05) (Fig. 1). However, at water-limiting conditions, the distribution curve is skewed towards IR64-specific allele – a global distortion of preferential expression. This indicates that more genes favor the maternal over the paternal allele under stress conditions in this particular hybrid cross. It is surprising to note that while Apo is the drought-tolerant genotype, IR64-specific allele is preferentially expressed in the hybrid. This is contrary to our initial speculation that the tolerant genotype (Apo) should exhibit preferential expression in the heterozygote.Fig. 1

View Article: PubMed Central - PubMed

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&thinsp;&times;&thinsp;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&ndash;60&nbsp;% 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.

Electronic supplementary material: The online version of this article (doi:10.1186/s12284-016-0123-4) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus