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Small RNA and Transcriptome Sequencing Reveals miRNA Regulation of Floral Thermogenesis in Nelumbo nucifera.

ABSTRACT: The sacred lotus (Nelumbo nucifera Gaertn.) can produce heat autonomously and maintain a relatively stable floral chamber temperature for several days when blooming. Floral thermogenesis is critical for flower organ development and reproductive success. However, the regulatory role of microRNA (miRNA) underlying floral thermogenesis in N. nucifera remains unclear. To comprehensively understand the miRNA regulatory mechanism of thermogenesis, we performed small RNA sequencing and transcriptome sequencing on receptacles from five different developmental stages. In the present study, a total of 172 known miRNAs belonging to 39 miRNA families and 126 novel miRNAs were identified. Twenty-nine thermogenesis-related miRNAs and 3024 thermogenesis-related mRNAs were screened based on their expression patterns. Of those, seventeen differentially expressed miRNAs (DEMs) and 1765 differentially expressed genes (DEGs) had higher expression during thermogenic stages. The upregulated genes in the thermogenic stages were mainly associated with mitochondrial function, oxidoreductase activity, and the energy metabolism process. Further analysis showed that miR156_2, miR395a_5, miR481d, and miR319p may play an important role in heat-producing activity by regulating cellular respiration-related genes. This study provides comprehensive miRNA and mRNA expression profile of receptacle during thermogenesis in N. nucifera, which advances our understanding on the regulation of floral thermogenesis mediated by miRNA.

SUBMITTER: Zou Y

PROVIDER: S-EPMC7246644 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Small RNA and Transcriptome Sequencing Reveals miRNA Regulation of Floral Thermogenesis in Nelumbo nucifera.

Zou Yu Y Chen Guanglong G Jin Jing J Wang Ying Y Xu Meiling M Peng Jing J Ding Yi Y

International journal of molecular sciences 20200508 9

The sacred lotus (Nelumbo nucifera Gaertn.) can produce heat autonomously and maintain a relatively stable floral chamber temperature for several days when blooming. Floral thermogenesis is critical for flower organ development and reproductive success. However, the regulatory role of microRNA (miRNA) underlying floral thermogenesis in N. nucifera remains unclear. To comprehensively understand the miRNA regulatory mechanism of thermogenesis, we performed small RNA sequencing and tr ...[more]

PMID: 32397143

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Project description:BACKGROUND: Roses (Rosa sp.), which belong to the family Rosaceae, are the most economically important ornamental plants--making up 30% of the floriculture market. However, given high demand for roses, rose breeding programs are limited in molecular resources which can greatly enhance and speed breeding efforts. A better understanding of important genes that contribute to important floral development and desired phenotypes will lead to improved rose cultivars. For this study, we analyzed rose miRNAs and the rose flower transcriptome in order to generate a database to expound upon current knowledge regarding regulation of important floral characteristics. A rose genetic database will enable comprehensive analysis of gene expression and regulation via miRNA among different Rosa cultivars. RESULTS: We produced more than 0.5 million reads from expressed sequences, totalling more than 110 million bp. From these, we generated 35,657, 31,434, 34,725, and 39,722 flower unigenes from Rosa hybrid: 'Vital', 'Maroussia', and 'Sympathy' and Rosa rugosa Thunb., respectively. The unigenes were assigned functional annotations, domains, metabolic pathways, Gene Ontology (GO) terms, Plant Ontology (PO) terms, and MIPS Functional Catalogue (FunCat) terms. Rose flower transcripts were compared with genes from whole genome sequences of Rosaceae members (apple, strawberry, and peach) and grape. We also produced approximately 40 million small RNA reads from flower tissue for Rosa, representing 267 unique miRNA tags. Among identified miRNAs, 25 of them were novel and 242 of them were conserved miRNAs. Statistical analyses of miRNA profiles revealed both shared and species-specific miRNAs, which presumably effect flower development and phenotypes. CONCLUSIONS: In this study, we constructed a Rose miRNA and transcriptome database, and we analyzed the miRNAs and transcriptome generated from the flower tissues of four Rosa cultivars. The database provides a comprehensive genetic resource which can be used to better understand rose flower development and to identify candidate genes for important phenotypes.

Project description:The flower chambers of sacred lotus (Nelumbo nucifera) can maintain a relatively stable temperature during anthesis despite the large environmental temperature fluctuations. However, the regulatory mechanism of floral thermogenesis remains largely unclear. To further understand the molecular basis of floral thermogenesis in N. nucifera, we obtained a comprehensive protein expression profile from receptacles at five developmental stages using data-independent acquisition (DIA)-based quantitative proteomics technology in the present study. A total of 6913 proteins were identified and quantified, of which 3513 significantly differentially expressed proteins (DEPs) were screened. The expression patterns of the DEPs were classified by time series analysis, and two clusters related to the thermogenesis pattern of receptacles were obtained. Among them, 640 proteins were highly expressed during thermogenesis whose functional annotation showed that they were mainly involved in the tricarboxylic acid cycle, starch and sucrose metabolism, redox processes, and aerobic respiration, etc. Citrate synthase was identified as the top hub protein (highly connected protein) in the protein-protein interaction (PPI) network analysis. Next, the content of alternative oxidase (AOX) and plant uncoupling protein (pUCP) in different tissues was determined and indicated that AOX was specifically expressed in the thermogenic receptacles, while pUCP showed significantly low expression in the receptacles compared to non-thermogenic leaves. Subsequently, a protein module highly related to the thermogenic phenotype was identified by the weighted gene co-expression network analysis (WGCNA), which was mainly involved in metabolic processes, fatty acid degradation and ubiquinone synthesis. In addition, the change of H2O2 content detected from the receptacles at the five stages was highly correlated with the expression trend of AOX. In summary, the mechanism of floral thermogenesis in N. nucifera involves complex regulatory networks including tricarboxylic acid cycle metabolism, starch and sucrose metabolism, active oxygen species signaling, fatty acid degradation, and ubiquinone synthesis, etc.

Project description:BackgroundIn China, lotus is an important cultivated crop with multiple applications in ornaments, food, and environmental purification. Adventitious roots (ARs), a secondary root is necessary for the uptake of nutrition and water as the lotus principle root is underdeveloped. Therefore, AR formation in seedlings is very important for lotus breeding due to its effect on plant early growth. As lotus ARs formation was significantly affected by sucrose treatment, we analyzed the expression of genes and miRNAs upon treatment with differential concentrations of sucrose, and a crosstalk between sucrose and IAA was also identified.ResultsNotably, 20 mg/L sucrose promoted the ARs development, whereas 60 mg/L sucrose inhibited the formation of ARs. To investigate the regulatory pathway during ARs formation, the expression of genes and miRNAs was evaluated by high-throughput tag-sequencing. We observed that the expression of 5438, 5184, and 5345 genes was enhanced in the GL20/CK0, GL60/CK0, and CK1/CK0 libraries, respectively. Further, the expression of 73, 78, and 71 miRNAs was upregulated in the ZT20/MCK0, ZT60/MCK0, and MCK1/MCK0 libraries, respectively. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that most of the differentially expressed genes and miRNAs in the GL20/GL60 and ZT20/ZT60 libraries were involved in signal transduction. A large number of these genes (29) and miRNAs (53) were associated with plant hormone metabolism. We observed an association between five miRNAs (miR160, miR156a-5p, miR397-5p_1, miR396a and miR167d) and nine genes (auxin response factor, protein brassinosteroid insensitive 1, laccase, and peroxidase 27) in the ZT20/ ZT60 libraries during ARs formation. Quantitative polymerase chain reaction (qRT-PCR) was used to validate the high-throughput tag-sequencing data.ConclusionsWe found that the expression of many critical genes involved in IAA synthesis and IAA transport was changed after treatment with various concentration of sucrose. Based on the change of these genes expression, IAA and sucrose content, we concluded that sucrose and IAA cooperatively regulated ARs formation. Sucrose affected ARs formation by improving IAA content at induction stage, and increased sucrose content might be also required for ARs development according to the changes tendency after application of exogenous IAA.

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Small RNA and Transcriptome Sequencing Reveals miRNA Regulation of Floral Thermogenesis in Nelumbo nucifera.

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Small RNA and Transcriptome Sequencing Reveals miRNA Regulation of Floral Thermogenesis in <i>Nelumbo nucifera</i>.

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