Dataset Information

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

ABSTRACT:

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

We used three tissues with high, moderate, and low ALA concentrations as an exemplar system in which to investigate tissue-specific ALA accumulation mechanisms 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.

SUBMITTER: Yu SY

PROVIDER: S-EPMC8063412 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Tree peony (Paeonia section Moutan DC.) seeds are an excellent source of beneficial natural compounds that promote health, and they contain high levels of alpha-linolenic acid (ALA). In recent years, tree peony has been emerging as an oil crop. Therefore, combined analysis of the transcriptome and proteome of tree peony (P. ostii) seeds at 25, 32, 39, 53, 67, 81, 88, 95, and 109 days after pollination (DAP) was conducted to better understand the transcriptional and translational regulation of seed development and oil biosynthesis. A total of 38,482 unigenes and 2841 proteins were identified. A total of 26,912 differentially expressed genes (DEGs) and 592 differentially expressed proteins (DEPs) were clustered into three groups corresponding to the rapid growth, seed inclusion enrichment and conversion, and late dehydration and mature stages of seed development. Fifteen lipid metabolism pathways were identified at both the transcriptome and proteome levels. Pathway enrichment analysis revealed that a period of rapid fatty acid biosynthesis occurred at 53-88 DAP. Furthermore, 211 genes and 35 proteins associated with the fatty acid metabolism pathway, 63 genes and 11 proteins associated with the biosynthesis of unsaturated fatty acids (UFAs), and 115 genes and 24 proteins associated with ALA metabolism were identified. Phylogenetic analysis revealed that 16 putative fatty acid desaturase (FAD)-encoding genes clustered into four FAD groups, eight of which exhibited the highest expression at 53 DAP, suggesting that they play an important role in ALA accumulation. RT-qPCR analysis indicated that the temporal expression patterns of oil biosynthesis genes were largely similar to the RNA-seq results. The expression patterns of fatty acid metabolism- and seed development-related proteins determined by MRM were also highly consistent with the results obtained in the proteomic analysis. Correlation analysis indicated significant differences in the number and abundance of DEGs and DEPs but a high level of consistency in expression patterns and metabolic pathways. The results of the present study represent the first combined transcriptomic and proteomic analysis of tree peony seeds and provide insight into tree peony seed development and oil accumulation.