Identification of microRNAs and long non-coding RNAs involved in fatty acid biosynthesis in tree peony seeds

Yin, Dandan; Li, Shanshan; Shu, Qingyan; Gu, Zhennan; Wu, Qian; Feng, Chengyong; Xu, Wenzhong; Wang, Liang-Sheng

doi:10.1016/j.gene.2018.05.011

Cited by 50 publications

(45 citation statements)

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“…Transcriptomes have previously been used to study the mechanisms underlying ALA synthesis in tree peony seeds [10][11][12][13][14]. Here, we identified genes associated with the lipid metabolism that were differentially expressed during the development of the seed kernel, testa, and pericarp.…”

Section: Discussionmentioning

confidence: 99%

“…There are nine wild species in section Moutan DC, which differ with respect to preferred habitat, but all rich in unsaturated FAs (>90%) and ALA (26.7-50%) [6,9]. To date, transcriptomic, proteomic, and microRNA sequencing have been used to investigate the mechanisms underlying ALA synthesis in tree peony seeds [10][11][12][13][14]. Previous studies have focused on enzymes that are key to ALA biosynthesis in various tree peony species, including FAD3 in P. rockii, P. potaninii and P. lutea seed [15]; FAD2 and FAD8 in P. ostii [10]; and ACCase, FATA, LPCAT, FADs, and DGAT in the developing endosperm of P. ostii var.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic analysis of a-linolenic acid content and biosynthesis in Paeonia ostii fruits and seeds

Zhang

et al. 2020

Preprint

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Background Paeonia ostii is a potentially important oilseed crop because its seed yield is high and the seeds are rich in α-linolenic acid (ALA). However, the molecular mechanisms underlying ALA biosynthesis during seed kernel, seed testa, and fruit pericarp development in this plant are unclear. We used transcriptome data to address this knowledge gap. Results Gas chromatograph-mass spectrometry indicated that ALA content was highest in the kernel, moderate in the testa, and lowest in the pericarp. Therefore, we used RNA-sequencing to compare ALA synthesis among these three tissues. We identified 227,837 unigenes, with an average length of 755 bp. Of these, 1371 unigenes were associated with lipid metabolism. The fatty acid (FA) biosynthesis and metabolism pathways were significantly enriched during the early stages of oil accumulation in the kernel. ALA biosynthesis was significantly enriched in parallel with increasing ALA content in the testa, but these metabolic pathways were not significantly enriched during pericarp development. By comparing unigene transcription profiles with patterns of ALA accumulation, specific unigenes encoding crucial enzymes and transcription factors (TFs) involved in de novo FA biosynthesis and oil accumulation were identified. Specifically, the bell-shaped expression patterns of genes encoding SAD, FAD2, FAD3, PDCT, PDAT, OLE, CLE, and SLE in the kernel were similar to the patterns of ALA accumulation in this tissue. Genes encoding BCCP, BC, KAS I– III, and FATA were also upregulated during the early stages of oil accumulation in the kernel. In the testa, the upregulation of the genes encoding SAD, FAD2, and FAD3 was followed by a sharp increase in the concentrations of ALA. In contrast, these genes were minimally expressed (and ALA content was low) throughout pericarp development. Conclusions In this study, we used three tissues with high, moderate, and low ALA concentrations as an exemplar system in which to compare tissue-specific ALA accumulation mechanism in P. ostii. The genes and TFs identified herein might be useful targets for future studies of ALA accumulation in the tree peony. This study also provides a framework for future studies of FA biosynthesis in other oilseed plants.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptomic analysis of a-linolenic acid content and biosynthesis in Paeonia ostii fruits and seeds

Zhang

et al. 2020

Preprint

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“…MicroRNAs (miRNAs) are a class of endogenous noncoding small RNAs with lengths of approximately 20-25 nucleotides and play crucial roles in mediating the posttranscriptional regulation of gene expression by targeting mRNA degradation or inhibiting target mRNA translational in eukaryotes. Studies have confirmed the key roles of miRNAs in various biological and metabolic processes in plants, such as fatty acid biosynthesis [6], lipid metabolism [7], growth and development [8], responses to stresses [9], and cellular proliferation and differentiation [10]. To date, a total of 5,141 miRNA sequences have been deposited in the database miRBase [11,12], and many conserved and novel miRNAs have been identified in soybean [13], Arabidopsis [14], Brassica napus [15], rice [16], peony [17] and maize [18].…”

Section: Introductionmentioning

confidence: 89%

Comparative profiling of microRNA expression in the developing seeds of high- and low-oil tea oil camellia (Camellia oleifera) cultivars

Ruan

Zhang

et al. 2019

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KEYWORDStea oil camellia, small RNA sequencing, miRNA-mRNA function modules, lipid metabolism, seed size However, the seed yield of tea oil camellia is unstable, and the seed oil content varies greatly, which seriously restricts the sustainable development of the tea oil camellia industry in China. One 3 important strategy is the cultivation of tea oil camellia cultivars with high seed oil contents and high and stable seed yields. MicroRNAs (miRNAs) are a class of endogenous noncoding small RNAs with lengths of approximately 20-25 nucleotides and play crucial roles in mediating the posttranscriptional regulation of gene expression by targeting mRNA degradation or inhibiting target mRNA translational in eukaryotes. Studies have confirmed the key roles of miRNAs in various biological and metabolic processes in plants, such as fatty acid biosynthesis [6], lipid metabolism [7], growth and development [8], responses to stresses [9], and cellular proliferation and differentiation [10]. To date, a total of 5,141 miRNA sequences have been deposited in the database miRBase [11, 12], and many conserved and novel miRNAs have been identified in soybean [13], Arabidopsis [14], Brassica napus [15], rice [16], peony [17] and maize [18]. miRNAs control and influence a variety of physiological processes by regulating target genes. For example, the KAS and KAR genes targeted by miR159 and miR156, respectively, are important for lipid biosynthesis [19]. The FAD2 gene targeted by miR159b and miR5026 regulates and influences fatty acid biosynthesis [13, 20]. miR160 plays highly important roles in multiple aspects of shoot and root development by modulating ARF targeting [21]. In addition, transcription factors play important roles in regulating lipid biosynthesis [22], such as WRINKLED1 and LEAFY COTYLEDON, MYB, SPL, ARF and AP2 [23], which have been identified to be targeted by the major miRNAs [24]. Based on the high-throughput sRNA and degradome analyses of soybean seeds 15 days after flower, 55 annotated and 26 novel miRNAs, which targeted 145 genes, were identified [13]; 82% of the targeted genes were transcription factors, including the ARF, MYB, TCP, GRF and NAC families [13]. The expression level of TCPs that are targeted by miR319 controls the coordination and regulation of two sequential processes in leaf development: the negative regulation of leaf growth and positive regulation of leaf senescence in A. thaliana [25]. miR160 negatively regulates ARFs that significantly affect seed development in A. thaliana [26]. SPL10 and SPL11 are targeted by miR156 and involved in the early morphogenesis of Arabidopsis embryos [27]. MYBs targeted by miR159 are involved in seed size, and a double mutation of miR159 (miR159ab) increased MYB33 and MYB65 expression, which promoted the formation of small seeds [28]. Currently, miRNA-mediated regulatory networks controlling multiple biological and metabolic processes have been revealed via the functional analysis of some woody oil plants, such as oil palm [29], peony [17] and olive [30]. In d...

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“…One important strategy is the cultivation of tea oil camellia cultivars with high seed oil contents and high and stable seed yields. [6], lipid metabolism [7], growth and development [8], responses to stresses [9], and cellular proliferation and differentiation [10]. To date, a total of 5,141 miRNA sequences have been deposited in the database miRBase [11,12], and many conserved and novel miRNAs have been identified in soybean [13],…”

Section: Introductionmentioning

confidence: 99%

Identification of miRNA-mRNA regulatory modules involved in lipid metabolism and seed development in a woody-oil tree (Camellia oleifera)

Wu¹,

Ruan²,

Shah³

et al. 2020

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BackgroundTea oil camellia ( Camellia oleifera ), an important woody oil tree, is a source of seed oil of high nutritional and medicinal values and has been being widely planted in southern China. However, there is no report on the identification of miRNAs involved in lipid metabolism and seed development in high- and low-oil cultivars of tea oil camellia. Thus, we explored the roles of miRNAs in the critical period of oil formation and accumulation in tea oil camellia, and identified miRNA-mRNA regulatory modules involved in lipid metabolism and seed development. ResultsSixteen small RNA libraries for high- and low-oil cultivars of the critical period of oil biosynthesis were constructed. A total of 196 miRNAs, including 156 known miRNAs from 35 families and 40 novel miRNAs, were identified, and 55 significantly differentially expressed miRNAs were found, which included 34 up-regulated miRNAs and 21 down-regulated miRNAs. An integrated analysis of miRNA and mRNA transcriptome sequence data and qRT-PCR-based information was performed and revealed that nine miRNA-mRNA regulatory modules were related to lipid metabolism, such as the negative regulatory modules of ath-miR858b- MYB82 / MYB3 / MYB44 represses seed oil biosynthesis and a positive regulation module of csi-miR166e-5p- S-ACP - DES6 for formation and accumulation of oleic acid. Twenty-tree miRNA-mRNA regulatory modules were involved in the regulation of seed size, such as a negative regulatory module of hpe-miR162a_L-2- ARF19 involved in early seed development. Twelve miRNA-mRNA regulatory modules regulating growth and development were identified, such as the negative regulatory modules of han-miR156a_L+1- SPL4 / SBP2 promoting early seed development. The targeting relationship of the cpa-miR393_R-1-AFB2 regulatory module were verified by luciferase activity assays. ConclusionMultiple microRNAs (miRNAs) were identified to involve in developing seeds of tea oil camellia, especially discovering several miRNA-mRNA regulatory modules involving in seed development and lipid metabolism. These data provide important theoretical value and a scientific basis for the genetic improvement of new varieties of tea oil camellia in the future.

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Identification of microRNAs and long non-coding RNAs involved in fatty acid biosynthesis in tree peony seeds

Cited by 50 publications

References 56 publications

Transcriptomic analysis of a-linolenic acid content and biosynthesis in Paeonia ostii fruits and seeds

Transcriptomic analysis of a-linolenic acid content and biosynthesis in Paeonia ostii fruits and seeds

Comparative profiling of microRNA expression in the developing seeds of high- and low-oil tea oil camellia (Camellia oleifera) cultivars

Identification of miRNA-mRNA regulatory modules involved in lipid metabolism and seed development in a woody-oil tree (Camellia oleifera)

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