A metabolomics study in citrus provides insight into bioactive phenylpropanoid metabolism

Abstract

Citrus fruits are widely consumed worldwide in juices or as fresh and provide a broad range of phytonutrients that are important for human health. Here, a citrus multi-omics resource is presented: comprehensive metabolic profiling of various citrus species was performed and metabolic profiles were compared among species, with a focus on the phenylpropanoid metabolic pathway. A metabolite-based genome-wide association analysis (mGWAS) of 154 pummelo accessions was performed using factored spectrally transformed linear mixed models (FaST-LMM) and efficient mixed-model association eXpedited (EMMAX), and the genetic and biochemical basis of metabolomic variation was comprehensively analysed. A metabolite-single nucleotide polymorphism-gene (metabolite-SNP-gene) interaction network was constructed for pummelo, and many candidate loci controlling the synthesis and regulation of bioactive compounds were identified; among these loci, three BAHD malonyltransferases were involved in the malonylation of flavonoid glycosides. Further investigation revealed that an R2R3-MYB transcription factor CgMYB1 positively controls the metabolism of phenylpropanoid molecules, particularly the flavonoid derivatives. This study provides valuable data resources on the metabolic regulatory networks of bioactive components in citrus, in addition to demonstrating an efficient method for metabolic pathway dissection and providing targets for future breeding work with the aim of improving nutritional value.

Acknowledgements

This work was supported by the National Key R&D Program of China (2021YFA0909600), the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (31821005), the National Science Fund for Distinguished Young Scholars of China (31625021 to J.L.), the National Postdoctoral Program for Innovative Talents (BX20220097), the China Post-doctoral Science Foundation (2022 M710991), the Hainan Provin-cial Academician Innovation Platform Project (HD-YSZX-202003, HD-YSZX-202004), Hainan Provincial Natural Science Founda-tion of China (323MS019), the Hainan Postdoctoral Grant Project, ‘111’Project (No. D20024), the Hainan University Startup Fund (KYQD(ZR)1866).

Author contributions

J.L. conceived the project and supervised this study. S.W., S.S., R.Z., S.Z., and Q.Z. performed the experiments; S.W., S.S., X.W., H.Y., W.Z., X.L., J.X., and X.D. participated in the material preparation; S.W., S.S., C.Y., and J.L. carried out the metabolite analyses; S.W., X.W., C.W., and H.G. performed the GWAS analysis; S.W., S.S., C.W., and J.L analysed the data; S.W., S.S., C.W., and J.L. wrote the paper. All of the authors discussed the results and commented on the manuscript.

Data availability

The genes and gene expression profile data involved in this study can be found on the following website: http://citrus.hzau.edu.cn/.

Conflict of interest statement

All authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

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