Integrated mRNA and small RNA sequencing reveals microRNA regulatory network associated with internode elongation in sugarcane (Saccharum officinarum L.)

- Background: Internode elongation is one of the most important traits in sugarcane because of its relation to crop productivity.
- Further analysis revealed that the differentially expressed genes were enriched in the GO terms oxidoreductase activity and tetrapyrrole binding.
- nitrogen metabolism ” and “ plant hormone signal transduction.
- which might be participating in internode elongation.
- By pairwise comparison, 11, 42 and 26 differentially expressed miRNAs were identified from EI and EII, EI and EIII, and EII and EIII comparisons, respectively.
- nitrogen metabolism ” and “ plant hormone signal transduction ” pathways are targets of the miRNAs.
- We found that the known miRNAs miR2592-y, miR1520-x, miR390-x, miR5658-x, miR6169-x and miR8154-x were likely regulators of genes with internode elongation in sugarcane..
- Conclusions: The results of this study provided a global view of mRNA and miRNA regulation during sugarcane internode elongation.
- A genetic network of miRNA-mRNA was identified with miRNA-mediated gene expression as a mechanism in sugarcane internode elongation.
- Thus, the genetics and the regulatory mechanisms of internode elongation in crop plants have been exten- sively investigated.
- Genetic and environmental factors such as gene expression [2–4], genomic variation [5, 6], hormonal regulation [7, 8], nutrients [9, 10], light [11], water [12] and temperature [13] control internode elongation.
- Complex hormonal mechanisms are associated with internode elongation.
- For example, auxin [14], gibberel- lin [17] and brassinosteroids [18] induce internode elongation.
- and jasmonic acid [21] suppress internode elongation in plants.
- 269 differentially expressed miRNAs were identified [31]..
- Transcriptome sequencing approaches promise increased understanding of the expression patterns and molecular regulatory mechanisms in gene expression [34].
- These studies provide basic information about the functional genes involved in internode elongation.
- 64 differentially expressed miRNAs were identified during the fiber elongation process [37].
- By comparing the differential ex- pression, the candidate genes and miRNAs involved in internode elongation were identified.
- To understand the molecular mechanism of internode elongation in sugarcane, nine cDNA libraries from the pre-elongation stage (EI), early elongation stage (EII) and rapid elongation stage (EIII) were sequenced.
- The gene expression in the present study was calculated by the RPKM method.
- position of the EI, EII and EIII stages, indicating sig- nificant changes among the stages in the transcrip- tome (Additional file 1).
- Differentially expressed genes in different stages of internode development.
- To compare the gene expression in different stages of internode elongation, the RSEM package was used to identify differentially expressed genes.
- In the compari- sons between EI and EII, EI and EIII, and EII and EIII and 3041 differentially expressed genes were identified, respectively (Fig.
- The most differentially expressed genes were in the comparison between EI and EIII stages, which included 1601 up-regulated and 3434 down- regulated genes at EIII stage.
- The Venn plot showed that 17 differentially expressed genes overlapped among the three comparisons (Fig.
- EIII had 226 differentially expressed genes (Fig.
- Functional annotation of the differentially expressed genes.
- To reveal the function of differentially expressed genes in different stages from internodes, GO and KEGG en- richment analyses were performed.
- 0.05) in the comparison EI vs..
- 0.05) in the EI vs.
- “zeatin biosynthesis”, “nitrogen metabolism” and “plant hormone signal transduction” pathways were investi- gated by qPCR.
- The sequencing of small RNAs was investigated to un- veil the dynamic regulation of miRNAs on gene expres- sion during internode elongation in sugarcane.
- A total of 241 known miRNAs were detected in the internode tissues from sugarcane.
- From all the Table 1 Summary of the RNA-Seq Data.
- A total of 245 novel candidate miRNAs were found in the internodes from sugarcane (Table 3, Additional file 4).
- Differentially expressed miRNAs and their targets.
- To understand the miRNA regulatory mechanism in internode elongation, the differentially expressed miR- NAs were identified by the TPM method.
- In the com- parisons between EI and EII, EI and EIII, and EII and EIII, 11, 42 and 26 differentially expressed miRNAs were found, respectively.
- Finally, 5 up-regulated and 21 down-regulated miRNAs were found in the comparison EII vs.
- In the EII vs.
- The principal component ana- lysis indicated a distinct position of the EI, EII and EIII stages (Fig.
- Targets of the differentially expressed miRNAs were detected.
- For 8 of the total differentially expressed miR- NAs in the EI and EII comparison, the target unigenes were identified (78 in total), whereas no targets were identified for the other 3 miRNAs.
- In the EI and EIII comparison, 204 targets for 31 miRNAs were identified (Additional file 6)..
- 1 Overview of mRNA Expression Profiles at Different Stages of Internode Elongation in Sugarcane.
- a Heat map comparison of the pre- elongation stage (EI), early elongation stage (EII) and rapid elongation stage (EIII).
- b Two-component principal component analysis of the nine transcriptomes from the pre-elongation stage (EI), early elongation stage (EII) and rapid elongation stage (EIII).
- 2 Differential Expression of Genes in Different Stages of Internode Elongation in Sugarcane.
- a Volcano plot shows the differentially expressed genes (green dot: down-regulated genes, red dot: up-regulated genes, black dot: unchanged genes).
- b Number of differentially expressed genes in the comparisons of EI vs.
- c Venn diagram shows overlap of differentially expressed genes among the comparisons.
- 3 GO (a) and KEGG (b) Enrichment Analyses of Differentially Expressed Genes in Different Samples.
- Differentially expressed mRNA and miRNA pairs related to internode elongation.
- Internode elongation is a tissue growth process, and there- fore, the mRNA and miRNA network related to tissue growth were identified.
- As found in the present analysis,.
- The expression profiles from qPCR were consistent with the results of the sequencing ana- lysis (Fig.
- 5 Differential Expression of miRNAs in Different Stages of Internode Elongation in Sugarcane.
- a Number of differentially expressed miRNAs in the comparisons of EI vs.
- b Two-component principal component analysis of the nine miRNA libraries from the pre-elongation stage (EI), early elongation stage (EII) and rapid elongation stage (EIII)..
- 6 Differentially Expressed miRNAs and their Targets in “ Zeatin Biosynthesis.
- Nitrogen Metabolism ” and “ Plant Hormone Signal Transduction ” Pathways.
- Right: Heat map of the targets of miRNAs.
- nitrogen metabolism ” and “ plant hormone signal transduction ” pathways, respectively.
- The number of differentially expressed genes in the EI vs.
- Compared with the differentially expressed genes, a significantly higher ratio of unigenes showed similar expression among all the groups, strongly suggesting that the differentially expressed genes were involved in sugarcane internode elongation..
- Oxidoreductase activity and tetrapyrrole binding were highly enriched in EI compared with those in the other two groups, indicating the function of these genes in sug- arcane internode elongation.
- transduction” pathways were enriched with differentially expressed genes.
- The differentially expressed genes in “ze- atin biosynthesis” pathways included CKX3, CKX5, CKX9, CKX10 and CKO2 at EII and EIII compared with EI.
- Low expression of the genes in these pathways might be related to high growth activities at EII and EIII stages during internode elongation via cyto- kinin accumulation [48].
- The changing of “plant hormone signal transduction” during internode elongation was also expected.
- The observations that several differentially expressed genes were related to internode elongation in the present study indicated that the sugarcane internode elongation was induced by the changes in gene expres- sion in key pathways, suggesting a complex network of the relationships between hormone secretion and inter- node elongation in sugarcane..
- development, flowering and internode elongation.
- Here, small RNA sequencing was performed in the stems from the pre-elongation stage, early elongation stage and rapid elongation stage in the present study.
- Subsequently, the miRNAs involved in control of the gene expression that was related to internode elongation was analyzed.
- and “plant hormone signal transduction” pathways par- ticipated in sugarcane internode elongation.
- In the.
- Several differentially expressed genes involved in internode elongation related to “zeatin biosyn- thesis”, “nitrogen metabolism” and “plant hormone signal transduction” pathways were identified.
- This evidence provides valuable information for further functional characterization of the miRNAs and their targets in sugarcane internode elongation..
- Identification of differentially expressed genes.
- The adjustment of the P -value for multiple testing by FDR correction was performed for identifica- tion of differentially expressed genes with FDR cutoff<.
- The differentially expressed genes were identified using the standard as |log2Ratio.
- 8 A miRNA-Regulated mRNA Model in Sugarcane Internode Elongation.
- nitrogen metabolism ” and “ plant hormone signal transduction ” pathways participate in sugarcane internode elongation.
- Gene Ontology (GO) was used to reflect the gene function of the large unigene set.
- Prediction of the targets of miRNAs.
- Identification of differentially expressed miRNAs.
- Ten of the differentially expressed genes from.
- GO analysis of differentially expressed genes..
- KEGG pathway of differentially expressed genes..
- The differentially expressed mRNA and miRNA pairs in.
- nitrogen metabolism ” and “ plant hormone signal transduction ” pathways..
- Temperature-dependent internode elongation in vegetative plants of Arabidopsis thaliana lacking phytochrome B and cryptochrome 1.
- Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice.
- miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin.
- Transcriptome sequencing and analysis for culm elongation of the world ’ s largest bamboo (Dendrocalamus sinicus).
- Transcriptome sequencing and analysis of the fast growing shoots of moso bamboo (Phyllostachys edulis).
- The biochemistry and medical significance of the flavonoids..
- Global analysis of the sugarcane microtranscriptome reveals a unique composition of small RNAs associated with axillary bud outgrowth

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