Integrative lipidomics profile uncovers the mechanisms underlying high-level α-linolenic acid accumulation in Paeonia rockii seeds

Abstract

Tree peony ( Paeonia rockii) is an excellent woody oilseed crop, known for its high α-linolenic acid (ALA, ∼45%) content, which is of great value for human health. However, the mechanisms underlying this high-level ALA accumulation in tree peony seeds are poorly understood. In this study, we evaluated the dynamic changes in the lipidomic profile of P. rockii seeds during development. A total of 760 lipid molecules were identified in P. rockii seeds; triacylglycerol (TAG) lipid molecules showed the highest abundance and diversity, both increasing during seed development. Particularly, ALA was the predominant fatty acid at the TAG sn-3 position. We further characterized two diacylglycerol acyltransferase (DGAT) genes and three phospholipid:diacylglycerol acyltransferase (PDAT) genes involved in the transfer of fatty acids to the TAG sn-3 position. Gene expression and subcellular localization analyses suggested that PrDGATs and PrPDATs may function as endoplasmic reticulum-localized proteins in seed TAG biosynthesis. In vitro functional complementation analysis showed different substrate specificities, with PrPDAT2 having a specific preference for ALA. Multiple biological assays demonstrated that PrDGAT1, PrDGAT2, PrPDAT1-2, and PrPDAT2 promote oil synthesis. Specifically, PrPDAT2 leads to preferential ALA in the oil. Our findings provide novel functional evidence of the roles of PrDGAT1 and PrPDAT2, which are potential targets for increasing the ALA yield in tree peony and other oilseed crops.

Acknowledgements

We thank Man Zhang (Beijing Forestry University) for her guidance in writing, reviewing, and editing. This work was supported by the National Natural Science Foundation of China (31971690, 31901357, and 31972453).

Author contributions

W.Y., investigation, writing, data curation. Z.X., investigation, data curation. L.X. and Y.Z., investigation. YL.Z. and L.N., writing, reviewing, and editing. Q.Z., supervision.

Data availability

All data supporting the conclusions of this work are present in the paper or its Supplementary material files. Sequence data from this article can be obtained in the TAIR/GenBank data libraries under accession numbers AtDGAT1 (AT2G19450), AtDGAT2 (AT3G51520), AtPDAT (AT5G13640), PrDGAT1 (OQ222883), PrDGAT2 (OQ784271), PrPDAT1-1 (OQ784272), PrPDAT1-2 (OQ784273), and PrPDAT2 (OQ222884).

Conflict of interest statement

None declared.

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