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Temporal small RNA transcriptome profiling unraveled partitioned miRNA expression in developing maize endosperms between reciprocal crosses.

Xin M, Yang G, Yao Y, Peng H, Hu Z, Sun Q, Wang X, Ni Z - Front Plant Sci (2015)

Bottom Line: In addition, we found a subset of distinct tandem miRNAs are generated from a single stem-loop structure in maize that might be conserved in monocots.Furthermore, a SNP variation of Zma-miR408-5p at 11th base position was characterized between B73 and Mo17 which might lead to completely different functions in repressing targets.Together, this study suggests that miRNA plays a crucial role in regulating endosperm development, and exhibited distinct expression patterns in developing endosperm between maize reciprocal crosses.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University Beijing, China.

ABSTRACT
In angiosperms, the endosperm nurtures the embryo and provides nutrients for seed germination. To identify the expression pattern of small interfering RNA in the developing maize endosperm, we have performed high-throughput small RNA transcriptome sequencing of kernels at 0, 3, and 5 days after pollination (DAP) and endosperms at 7, 10, and 15 DAP using B73 and Mo17 reciprocal crosses in previous study. Here, we further explored these small RNA-seq data to investigate the potential roles of miRNAs in regulating the gene expression process. In total, 57 conserved miRNAs and 18 novel miRNAs were observed highly expressed in maize endosperm. Temporal expression profiling indicated that these miRNAs exhibited dynamic and partitioned expression patterns at different developmental stages between maize reciprocal crosses, and quantitative RT-PCR results further confirmed our observation. In addition, we found a subset of distinct tandem miRNAs are generated from a single stem-loop structure in maize that might be conserved in monocots. Furthermore, a SNP variation of Zma-miR408-5p at 11th base position was characterized between B73 and Mo17 which might lead to completely different functions in repressing targets. More interestingly, Zma-miR408-5p exhibited B73-biased expression pattern in the B73 and Mo17 reciprocal hybrid endosperms at 7, 10, and 15 DAP according to the reads abundance with SNPs and CAPS experiment. Together, this study suggests that miRNA plays a crucial role in regulating endosperm development, and exhibited distinct expression patterns in developing endosperm between maize reciprocal crosses.

No MeSH data available.


Related in: MedlinePlus

Phenotypic difference and temporal expression patterns of miRNAs in 0-, 3-, 5-DAP kernels and 7-, 10-, 15-DAP endosperms between B73 and Mo17 reciprocal crosses. (A) The kernel and endosperm of Mo17 × B73 grow faster than in B73 × Mo17 at all six stages. (B)Zma-miR528, Zma-miR397, and Zma-miR408 were more highly expressed in Mo17 × B73 compared to B73 × Mo17 in 5-DAP kernel and 7-DAP endosperm. (C) Newly identified Zma-miR2002, Zma-miR2017, Zma-miR2001, and Zma-miR2010 exhibited differential expression patterns between reciprocal crosses.
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Figure 4: Phenotypic difference and temporal expression patterns of miRNAs in 0-, 3-, 5-DAP kernels and 7-, 10-, 15-DAP endosperms between B73 and Mo17 reciprocal crosses. (A) The kernel and endosperm of Mo17 × B73 grow faster than in B73 × Mo17 at all six stages. (B)Zma-miR528, Zma-miR397, and Zma-miR408 were more highly expressed in Mo17 × B73 compared to B73 × Mo17 in 5-DAP kernel and 7-DAP endosperm. (C) Newly identified Zma-miR2002, Zma-miR2017, Zma-miR2001, and Zma-miR2010 exhibited differential expression patterns between reciprocal crosses.

Mentions: Parental alleles are immediately activated in their filial genomes after fertilization, and their gene expression pattern, level, and timing are undoubtedly associated with plant development (Xin et al., 2013; Li et al., 2014). However, how miRNAs are expressed between reciprocal crosses during maize endosperm development remains undetermined. Our cytological analysis revealed that the endosperm in Mo17 × B73 undergoes faster development than that in B73 × Mo17 (Figure 4A), which led us to determine whether there are differences in the miRNA expression patterns between them. Not surprisingly, a proportion of miRNAs exhibited partitioned expression levels during kernel and endosperm developmental stages between B73 × Mo17 and Mo17 × B73, including both conserved and novel ones. For example, the expression levels of Zma-miR528 and Zma-miR397 were clearly higher in the Mo17 × B73 cross than in B73 × Mo17 in 5-DAP kernels and 7-DAP endosperms (Figure 4B). Similarly, Zma-miR408 also exhibited similar expression trends to Zma-miR528 and Zma-miR397, which might contribute to the phenotypic difference between these two reciprocal crosses (Figure 4B). It has been predicted that one target of miR528 and miR397 is the L-ascorbate oxidases (AO) gene, which would increase the accumulation of dehydroascorbate (DHA) and in turn restrict cell-division ability (Potters et al., 2000; Pignocchi et al., 2006). Therefore, a high abundance of miR397 and miR528 would directly repress the expression of AO and indirectly repress that of DHA, maintain a high rate of cell division, and thereby promote plant growth. Furthermore, the over-expression of miR408 promotes vegetative growth, but the knockdown of miR408 results in impaired growth in Arabidopsis; both of these trends are consistent with the rapid development of Mo17 × B73 kernels and endosperms (Zhang and Li, 2013).


Temporal small RNA transcriptome profiling unraveled partitioned miRNA expression in developing maize endosperms between reciprocal crosses.

Xin M, Yang G, Yao Y, Peng H, Hu Z, Sun Q, Wang X, Ni Z - Front Plant Sci (2015)

Phenotypic difference and temporal expression patterns of miRNAs in 0-, 3-, 5-DAP kernels and 7-, 10-, 15-DAP endosperms between B73 and Mo17 reciprocal crosses. (A) The kernel and endosperm of Mo17 × B73 grow faster than in B73 × Mo17 at all six stages. (B)Zma-miR528, Zma-miR397, and Zma-miR408 were more highly expressed in Mo17 × B73 compared to B73 × Mo17 in 5-DAP kernel and 7-DAP endosperm. (C) Newly identified Zma-miR2002, Zma-miR2017, Zma-miR2001, and Zma-miR2010 exhibited differential expression patterns between reciprocal crosses.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4584948&req=5

Figure 4: Phenotypic difference and temporal expression patterns of miRNAs in 0-, 3-, 5-DAP kernels and 7-, 10-, 15-DAP endosperms between B73 and Mo17 reciprocal crosses. (A) The kernel and endosperm of Mo17 × B73 grow faster than in B73 × Mo17 at all six stages. (B)Zma-miR528, Zma-miR397, and Zma-miR408 were more highly expressed in Mo17 × B73 compared to B73 × Mo17 in 5-DAP kernel and 7-DAP endosperm. (C) Newly identified Zma-miR2002, Zma-miR2017, Zma-miR2001, and Zma-miR2010 exhibited differential expression patterns between reciprocal crosses.
Mentions: Parental alleles are immediately activated in their filial genomes after fertilization, and their gene expression pattern, level, and timing are undoubtedly associated with plant development (Xin et al., 2013; Li et al., 2014). However, how miRNAs are expressed between reciprocal crosses during maize endosperm development remains undetermined. Our cytological analysis revealed that the endosperm in Mo17 × B73 undergoes faster development than that in B73 × Mo17 (Figure 4A), which led us to determine whether there are differences in the miRNA expression patterns between them. Not surprisingly, a proportion of miRNAs exhibited partitioned expression levels during kernel and endosperm developmental stages between B73 × Mo17 and Mo17 × B73, including both conserved and novel ones. For example, the expression levels of Zma-miR528 and Zma-miR397 were clearly higher in the Mo17 × B73 cross than in B73 × Mo17 in 5-DAP kernels and 7-DAP endosperms (Figure 4B). Similarly, Zma-miR408 also exhibited similar expression trends to Zma-miR528 and Zma-miR397, which might contribute to the phenotypic difference between these two reciprocal crosses (Figure 4B). It has been predicted that one target of miR528 and miR397 is the L-ascorbate oxidases (AO) gene, which would increase the accumulation of dehydroascorbate (DHA) and in turn restrict cell-division ability (Potters et al., 2000; Pignocchi et al., 2006). Therefore, a high abundance of miR397 and miR528 would directly repress the expression of AO and indirectly repress that of DHA, maintain a high rate of cell division, and thereby promote plant growth. Furthermore, the over-expression of miR408 promotes vegetative growth, but the knockdown of miR408 results in impaired growth in Arabidopsis; both of these trends are consistent with the rapid development of Mo17 × B73 kernels and endosperms (Zhang and Li, 2013).

Bottom Line: In addition, we found a subset of distinct tandem miRNAs are generated from a single stem-loop structure in maize that might be conserved in monocots.Furthermore, a SNP variation of Zma-miR408-5p at 11th base position was characterized between B73 and Mo17 which might lead to completely different functions in repressing targets.Together, this study suggests that miRNA plays a crucial role in regulating endosperm development, and exhibited distinct expression patterns in developing endosperm between maize reciprocal crosses.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University Beijing, China.

ABSTRACT
In angiosperms, the endosperm nurtures the embryo and provides nutrients for seed germination. To identify the expression pattern of small interfering RNA in the developing maize endosperm, we have performed high-throughput small RNA transcriptome sequencing of kernels at 0, 3, and 5 days after pollination (DAP) and endosperms at 7, 10, and 15 DAP using B73 and Mo17 reciprocal crosses in previous study. Here, we further explored these small RNA-seq data to investigate the potential roles of miRNAs in regulating the gene expression process. In total, 57 conserved miRNAs and 18 novel miRNAs were observed highly expressed in maize endosperm. Temporal expression profiling indicated that these miRNAs exhibited dynamic and partitioned expression patterns at different developmental stages between maize reciprocal crosses, and quantitative RT-PCR results further confirmed our observation. In addition, we found a subset of distinct tandem miRNAs are generated from a single stem-loop structure in maize that might be conserved in monocots. Furthermore, a SNP variation of Zma-miR408-5p at 11th base position was characterized between B73 and Mo17 which might lead to completely different functions in repressing targets. More interestingly, Zma-miR408-5p exhibited B73-biased expression pattern in the B73 and Mo17 reciprocal hybrid endosperms at 7, 10, and 15 DAP according to the reads abundance with SNPs and CAPS experiment. Together, this study suggests that miRNA plays a crucial role in regulating endosperm development, and exhibited distinct expression patterns in developing endosperm between maize reciprocal crosses.

No MeSH data available.


Related in: MedlinePlus