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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.

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Related in: MedlinePlus

Conserved miRNA expression pattern during maize kernel and endosperm development in reciprocal crosses. (A) Hierarchical tandem of 57 conserved miRNAs with relatively high expression levels in at least one developmental stage. Diverse and tissue-specific miRNA expression patterns were exhibited, and a large proportion of miRNAs were highly expressed in kernels whereas only a few miRNAs were abundantly expressed during endosperm stages. (B) Dynamic and differential expression patterns of maize miR156 family members. The Zma-miR156a group has the highest expression level compared with other family members during all the developmental stages. (C) Kernel-abundant expression patterns of maize miR166 family members. Despite different expression levels, Zma-miR166 family members showed similar expression trends: they were highly expressed in 0-, 3-, and 5-DAP kernels but not in endosperms. (D) Endosperm-abundant expression patterns of maize miR167 family members. All Zma-miR167 members exhibited higher expression levels in endosperm stages than in the kernel stages. DAP, days after pollination.
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Figure 2: Conserved miRNA expression pattern during maize kernel and endosperm development in reciprocal crosses. (A) Hierarchical tandem of 57 conserved miRNAs with relatively high expression levels in at least one developmental stage. Diverse and tissue-specific miRNA expression patterns were exhibited, and a large proportion of miRNAs were highly expressed in kernels whereas only a few miRNAs were abundantly expressed during endosperm stages. (B) Dynamic and differential expression patterns of maize miR156 family members. The Zma-miR156a group has the highest expression level compared with other family members during all the developmental stages. (C) Kernel-abundant expression patterns of maize miR166 family members. Despite different expression levels, Zma-miR166 family members showed similar expression trends: they were highly expressed in 0-, 3-, and 5-DAP kernels but not in endosperms. (D) Endosperm-abundant expression patterns of maize miR167 family members. All Zma-miR167 members exhibited higher expression levels in endosperm stages than in the kernel stages. DAP, days after pollination.

Mentions: In previous study, we mainly focused on siRNA expression patterns, while here, we paid more attention to miRNA expression trends in the B73 and Mo17 reciprocal endosperms. After removing adaptors and low-quality sequences, the ~163.2 million filtered reads were aligned against mature maize miRNAs registered at miRBase (Release 21), idenfying 57 known miRNA members belonging to 25 families during maize kernel and endosperm developmental stages (Figure 2A). The expression levels of these miRNAs were normalized to the total reads of each library (RPM, Reads Per Million). Among them, Zma-miR168, Zma-miR166, Zma-miR156, Zma-miR528, Zma-miR827, and Zma-miR167 were the top six most abundantly expressed miRNAs in both reciprocal crosses, corresponding to more than 98% of the total number of known miRNAs (Table S2, Figure 2A). As predicted, a proportion of these conserved miRNAs exhibited temporal expression patterns in the kernels and endosperms, e.g., Zma-miR166 was predominantly expressed in 0-, 3-, and 5-DAP kernels, on average, and was ~8.7-fold higher than in 7, 10, 15 DAP endosperms. In contrast, the expression level of Zma-miR156 was significantly higher in the endosperm stages than in the kernel stages. In addition, Zma-miR528 and Zma-miR167 showed dramatically varied expression patterns during endosperm development. While the expression of Zma-miR528 was significantly down-regulated from 7- to 15-DAP endosperms, a rapid up-regulation of Zma-miR167 was observed at 10- and 15-DAP. Although the expression level of Zma-miR827 showed a sharp up-regulation at 15 DAP compared with 7 and 10 DAP, it was more highly expressed in maize kernels than in the endosperms. Unlikely, Zma-miR168 was consistently expressed with high levels during both kernels and endosperms, possibly because of its key role in regulating the production of miRNAs (Mallory and Vaucheret, 2006) (Figure 2A).


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)

Conserved miRNA expression pattern during maize kernel and endosperm development in reciprocal crosses. (A) Hierarchical tandem of 57 conserved miRNAs with relatively high expression levels in at least one developmental stage. Diverse and tissue-specific miRNA expression patterns were exhibited, and a large proportion of miRNAs were highly expressed in kernels whereas only a few miRNAs were abundantly expressed during endosperm stages. (B) Dynamic and differential expression patterns of maize miR156 family members. The Zma-miR156a group has the highest expression level compared with other family members during all the developmental stages. (C) Kernel-abundant expression patterns of maize miR166 family members. Despite different expression levels, Zma-miR166 family members showed similar expression trends: they were highly expressed in 0-, 3-, and 5-DAP kernels but not in endosperms. (D) Endosperm-abundant expression patterns of maize miR167 family members. All Zma-miR167 members exhibited higher expression levels in endosperm stages than in the kernel stages. DAP, days after pollination.
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Figure 2: Conserved miRNA expression pattern during maize kernel and endosperm development in reciprocal crosses. (A) Hierarchical tandem of 57 conserved miRNAs with relatively high expression levels in at least one developmental stage. Diverse and tissue-specific miRNA expression patterns were exhibited, and a large proportion of miRNAs were highly expressed in kernels whereas only a few miRNAs were abundantly expressed during endosperm stages. (B) Dynamic and differential expression patterns of maize miR156 family members. The Zma-miR156a group has the highest expression level compared with other family members during all the developmental stages. (C) Kernel-abundant expression patterns of maize miR166 family members. Despite different expression levels, Zma-miR166 family members showed similar expression trends: they were highly expressed in 0-, 3-, and 5-DAP kernels but not in endosperms. (D) Endosperm-abundant expression patterns of maize miR167 family members. All Zma-miR167 members exhibited higher expression levels in endosperm stages than in the kernel stages. DAP, days after pollination.
Mentions: In previous study, we mainly focused on siRNA expression patterns, while here, we paid more attention to miRNA expression trends in the B73 and Mo17 reciprocal endosperms. After removing adaptors and low-quality sequences, the ~163.2 million filtered reads were aligned against mature maize miRNAs registered at miRBase (Release 21), idenfying 57 known miRNA members belonging to 25 families during maize kernel and endosperm developmental stages (Figure 2A). The expression levels of these miRNAs were normalized to the total reads of each library (RPM, Reads Per Million). Among them, Zma-miR168, Zma-miR166, Zma-miR156, Zma-miR528, Zma-miR827, and Zma-miR167 were the top six most abundantly expressed miRNAs in both reciprocal crosses, corresponding to more than 98% of the total number of known miRNAs (Table S2, Figure 2A). As predicted, a proportion of these conserved miRNAs exhibited temporal expression patterns in the kernels and endosperms, e.g., Zma-miR166 was predominantly expressed in 0-, 3-, and 5-DAP kernels, on average, and was ~8.7-fold higher than in 7, 10, 15 DAP endosperms. In contrast, the expression level of Zma-miR156 was significantly higher in the endosperm stages than in the kernel stages. In addition, Zma-miR528 and Zma-miR167 showed dramatically varied expression patterns during endosperm development. While the expression of Zma-miR528 was significantly down-regulated from 7- to 15-DAP endosperms, a rapid up-regulation of Zma-miR167 was observed at 10- and 15-DAP. Although the expression level of Zma-miR827 showed a sharp up-regulation at 15 DAP compared with 7 and 10 DAP, it was more highly expressed in maize kernels than in the endosperms. Unlikely, Zma-miR168 was consistently expressed with high levels during both kernels and endosperms, possibly because of its key role in regulating the production of miRNAs (Mallory and Vaucheret, 2006) (Figure 2A).

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