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Dynamic parent-of-origin effects on small interfering RNA expression in the developing maize endosperm.

Xin M, Yang R, Yao Y, Ma C, Peng H, Sun Q, Wang X, Ni Z - BMC Plant Biol. (2014)

Bottom Line: Moreover, 13 out of 29 imprinted genes harbored imprinted siRNA loci within their 2-kb flanking regions, a significant higher frequency than expected based on simulation analysis.A subset of siRNAs subjected to imprinted expression pattern in maize developing endosperm, and they are likely correlated with certain imprinted gene expression.Additionally, siRNAs might influence nutrient uptake and allocation processes during maize endosperm development.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In angiosperms, the endosperm plays a crucial placenta-like role in that not only is it necessary for nurturing the embryo, but also regulating embryogenesis through complicated genetic and epigenetic interactions with other seed compartments and is the primary tissue in which genomic imprinting occurs.

Results: We observed a gradual increase of paternal siRNA expression in the early stages of kernels and an expected 2:1 maternal to paternal ratio in 7-DAP endosperm via sequencing of small interfering RNA (siRNA) transcriptomes in developing kernels (0, 3 and 5 days after pollination (DAP)) and endosperms (7, 10 and 15 DAP) from the maize B73 and Mo17 reciprocal crosses. Additionally, 460 imprinted siRNA loci were identified in the endosperm, with the majority (456/460, 99.1%) being maternally expressed at 10 DAP. Moreover, 13 out of 29 imprinted genes harbored imprinted siRNA loci within their 2-kb flanking regions, a significant higher frequency than expected based on simulation analysis. Additionally, gene ontology terms of "response to auxin stimulus", "response to brassinosteroid stimulus" and "regulation of gene expression" were enriched with genes harboring 10-DAP specific siRNAs, whereas those of "nutrient reservoir activity", "protein localization to vacuole" and "secondary metabolite biosynthetic process" were enriched with genes harboring 15-DAP specific siRNAs.

Conclusions: A subset of siRNAs subjected to imprinted expression pattern in maize developing endosperm, and they are likely correlated with certain imprinted gene expression. Additionally, siRNAs might influence nutrient uptake and allocation processes during maize endosperm development.

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Chromosomal distribution of siRNA loci and imprinted genes on maize genome. Lane group a: Chromosomal distribution of siRNA reads abundance. These four lanes indicate differential siRNA abundance along maize chromosomes using perfectly mapped siRNA with unique position, ≤10, ≤100, and ≤1000 positions on maize genome, respectively, from outside to inside. They were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions. Red: high abundance; Yellow: medium abundance; Green: low abundance. Lane b: Chromosomal distribution of protein-coding genes and repeat sequences identified by Repeat-Mask software, and repeat sequences were highly enriched in centromeric and telomeric regions, which exhibited a negative correlation with gene density along chromosomes. Red: high proportion of repeats; Green: high proportion of genes; Yellow: relatively equal proportion of genes and repeats. Lane group c: Chromosomal distributions of siRNA loci identified by using the reads uniquely mapped, mapped with ≤10, ≤100 and ≤1000 positions respectively, from outside to inside, and the trend is similar to the siRNA abundance distribution. Red: high density; Yellow: moderate density; Green: low density. Lane d: Chromosomal distributions of imprinted genes (light gray) and imprinted siRNA loci (dark gray) on maize genome, which were distributed on all 10 chromosomes.
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Figure 1: Chromosomal distribution of siRNA loci and imprinted genes on maize genome. Lane group a: Chromosomal distribution of siRNA reads abundance. These four lanes indicate differential siRNA abundance along maize chromosomes using perfectly mapped siRNA with unique position, ≤10, ≤100, and ≤1000 positions on maize genome, respectively, from outside to inside. They were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions. Red: high abundance; Yellow: medium abundance; Green: low abundance. Lane b: Chromosomal distribution of protein-coding genes and repeat sequences identified by Repeat-Mask software, and repeat sequences were highly enriched in centromeric and telomeric regions, which exhibited a negative correlation with gene density along chromosomes. Red: high proportion of repeats; Green: high proportion of genes; Yellow: relatively equal proportion of genes and repeats. Lane group c: Chromosomal distributions of siRNA loci identified by using the reads uniquely mapped, mapped with ≤10, ≤100 and ≤1000 positions respectively, from outside to inside, and the trend is similar to the siRNA abundance distribution. Red: high density; Yellow: moderate density; Green: low density. Lane d: Chromosomal distributions of imprinted genes (light gray) and imprinted siRNA loci (dark gray) on maize genome, which were distributed on all 10 chromosomes.

Mentions: We identified and classified genomic loci generating siRNAs based on previous methods [24],[25] (Methods), and these siRNA loci were further defined in terms of their dominant siRNA population representing more than 50% of the total siRNAs at a locus. When only using uniquely mapped reads, 416,100 siRNA loci were identified across all ten chromosomes; when multi-reads were included, 644,496, 836,618 and 931,924 siRNA loci were identified with the maximum mapping locations of 10, 100 and 1,000, respectively. The chromosomal distribution demonstrated that siRNA loci were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions (Figure 1), which is consistent with the observation in maize shoots that only a small proportion of siRNAs are generated from the pericentromeric and centromeric regions [26]. To include more information and better reflect the original siRNA situation, 931,924 siRNA loci containing multi-reads (≤1000 locations) were used for further analysis, with more than 90% of the siRNA loci predominantly producing 24-nt siRNAs and 3% and 1% of the loci being enriched with 21- and 22-nt siRNAs, respectively (Additional file 3: Table S2).


Dynamic parent-of-origin effects on small interfering RNA expression in the developing maize endosperm.

Xin M, Yang R, Yao Y, Ma C, Peng H, Sun Q, Wang X, Ni Z - BMC Plant Biol. (2014)

Chromosomal distribution of siRNA loci and imprinted genes on maize genome. Lane group a: Chromosomal distribution of siRNA reads abundance. These four lanes indicate differential siRNA abundance along maize chromosomes using perfectly mapped siRNA with unique position, ≤10, ≤100, and ≤1000 positions on maize genome, respectively, from outside to inside. They were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions. Red: high abundance; Yellow: medium abundance; Green: low abundance. Lane b: Chromosomal distribution of protein-coding genes and repeat sequences identified by Repeat-Mask software, and repeat sequences were highly enriched in centromeric and telomeric regions, which exhibited a negative correlation with gene density along chromosomes. Red: high proportion of repeats; Green: high proportion of genes; Yellow: relatively equal proportion of genes and repeats. Lane group c: Chromosomal distributions of siRNA loci identified by using the reads uniquely mapped, mapped with ≤10, ≤100 and ≤1000 positions respectively, from outside to inside, and the trend is similar to the siRNA abundance distribution. Red: high density; Yellow: moderate density; Green: low density. Lane d: Chromosomal distributions of imprinted genes (light gray) and imprinted siRNA loci (dark gray) on maize genome, which were distributed on all 10 chromosomes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4222485&req=5

Figure 1: Chromosomal distribution of siRNA loci and imprinted genes on maize genome. Lane group a: Chromosomal distribution of siRNA reads abundance. These four lanes indicate differential siRNA abundance along maize chromosomes using perfectly mapped siRNA with unique position, ≤10, ≤100, and ≤1000 positions on maize genome, respectively, from outside to inside. They were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions. Red: high abundance; Yellow: medium abundance; Green: low abundance. Lane b: Chromosomal distribution of protein-coding genes and repeat sequences identified by Repeat-Mask software, and repeat sequences were highly enriched in centromeric and telomeric regions, which exhibited a negative correlation with gene density along chromosomes. Red: high proportion of repeats; Green: high proportion of genes; Yellow: relatively equal proportion of genes and repeats. Lane group c: Chromosomal distributions of siRNA loci identified by using the reads uniquely mapped, mapped with ≤10, ≤100 and ≤1000 positions respectively, from outside to inside, and the trend is similar to the siRNA abundance distribution. Red: high density; Yellow: moderate density; Green: low density. Lane d: Chromosomal distributions of imprinted genes (light gray) and imprinted siRNA loci (dark gray) on maize genome, which were distributed on all 10 chromosomes.
Mentions: We identified and classified genomic loci generating siRNAs based on previous methods [24],[25] (Methods), and these siRNA loci were further defined in terms of their dominant siRNA population representing more than 50% of the total siRNAs at a locus. When only using uniquely mapped reads, 416,100 siRNA loci were identified across all ten chromosomes; when multi-reads were included, 644,496, 836,618 and 931,924 siRNA loci were identified with the maximum mapping locations of 10, 100 and 1,000, respectively. The chromosomal distribution demonstrated that siRNA loci were preferentially enriched in high-density gene regions and chromosomal end regions but devoid in repeat-rich pericentromeric and centromeric regions (Figure 1), which is consistent with the observation in maize shoots that only a small proportion of siRNAs are generated from the pericentromeric and centromeric regions [26]. To include more information and better reflect the original siRNA situation, 931,924 siRNA loci containing multi-reads (≤1000 locations) were used for further analysis, with more than 90% of the siRNA loci predominantly producing 24-nt siRNAs and 3% and 1% of the loci being enriched with 21- and 22-nt siRNAs, respectively (Additional file 3: Table S2).

Bottom Line: Moreover, 13 out of 29 imprinted genes harbored imprinted siRNA loci within their 2-kb flanking regions, a significant higher frequency than expected based on simulation analysis.A subset of siRNAs subjected to imprinted expression pattern in maize developing endosperm, and they are likely correlated with certain imprinted gene expression.Additionally, siRNAs might influence nutrient uptake and allocation processes during maize endosperm development.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In angiosperms, the endosperm plays a crucial placenta-like role in that not only is it necessary for nurturing the embryo, but also regulating embryogenesis through complicated genetic and epigenetic interactions with other seed compartments and is the primary tissue in which genomic imprinting occurs.

Results: We observed a gradual increase of paternal siRNA expression in the early stages of kernels and an expected 2:1 maternal to paternal ratio in 7-DAP endosperm via sequencing of small interfering RNA (siRNA) transcriptomes in developing kernels (0, 3 and 5 days after pollination (DAP)) and endosperms (7, 10 and 15 DAP) from the maize B73 and Mo17 reciprocal crosses. Additionally, 460 imprinted siRNA loci were identified in the endosperm, with the majority (456/460, 99.1%) being maternally expressed at 10 DAP. Moreover, 13 out of 29 imprinted genes harbored imprinted siRNA loci within their 2-kb flanking regions, a significant higher frequency than expected based on simulation analysis. Additionally, gene ontology terms of "response to auxin stimulus", "response to brassinosteroid stimulus" and "regulation of gene expression" were enriched with genes harboring 10-DAP specific siRNAs, whereas those of "nutrient reservoir activity", "protein localization to vacuole" and "secondary metabolite biosynthetic process" were enriched with genes harboring 15-DAP specific siRNAs.

Conclusions: A subset of siRNAs subjected to imprinted expression pattern in maize developing endosperm, and they are likely correlated with certain imprinted gene expression. Additionally, siRNAs might influence nutrient uptake and allocation processes during maize endosperm development.

Show MeSH