Abstract

BackgroundPaeonia 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.ResultsGas 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.ConclusionsWe 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.

Highlights

  • Paeonia ostii is a potentially important oilseed crop because its seed yield is high, and the seeds are rich in α-linolenic acid (ALA)

  • A previous study concluded that the high concentrations of ALA in P. ostii seeds were due to FAD8 activity and abundance [10], our results suggested that high concentrations of ALA in the kernel might be associated with the activity and abundance of Linoleate desaturase (FAD3), not FAD8

  • Many fatty acid (FA) biosynthesis and metabolism pathways were significantly enriched in these Differentially expressed gene (DEG) in the kernel at the early stages of rapid oil accumulation

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Summary

Introduction

Paeonia ostii is a potentially important oilseed crop because its seed yield is high, and the seeds are rich in α-linolenic acid (ALA). The high ratio of ω-6 to ω-3 FAs (~ 15:1) in the typical modern human diet is thought to be a major factor contributing to the high rates of cardiovascular disease in modern human societies [5]. One explanation for this imbalance is that the bulk of the oil seed crops consumed by modern humans, including soybean (Glycine max), peanut (Arachis hypogaea), maize (Zea mays), sunflower (Helianthus annuus), and rape (Brassica napus), have relatively low levels of ω-3 FAs, such as ALA [5]. Tree peony seed oil has been recognized as a high-quality edible oil and was identified as a new food resource by the Chinese Ministry of Health in 2011 [7]

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