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Metabolome and transcriptome profiling of Theobroma cacao provides insights into the molecular basis of pod color variation

Abstract

The Theobroma cacao presents a wide diversity in pod color among different cultivars. Although flavonoid biosynthesis has been studied in many plants, molecular mechanisms governing the diversity of coloration in cacao pods are largely unknown. The flavonoid metabolite profiles and flavonoid biosynthetic gene expression in the pod exocarps of light green pod ‘TAS 410’ (GW), green pod ‘TAS 166’ (GF), and mauve pod ‘TAS 168’ (PF) were determined. Changes in flavonoid metabolites, particularly the anthocyanins (cyanidin 3-O-galactoside, cyanidin 3-O-glucoside, and cyanidin O-syringic acid) were significantly up-accumulated in the mauve phenotype (PF) compared to the light green or green phenotypes, endowing the pod color change from light green or green to mauve. Consistently, the PF phenotype showed different expression patterns of flavonoid biosynthetic structural genes in comparison with GW/GF phenotypes. The expression level of LAR and ANR in GW/GF was significantly higher than PF, while the expression level of UFGT in GW/GF was lower than PF. These genes likely generated more anthocyanins in the exocarps samples of PF than that of GW/GF. Simultaneously, colorless flavan-3-ols (catechin, epicatechin and proanthocyanidin) content in the exocarp samples of PF was lower than GW/GF. Additionally, MYB (gene18079) and bHLH (gene5045 and gene21575) may participate in the regulation of the pod color. This study sheds light on the molecular basis of cacao pod color variation, which will contribute to breeding cacao varieties with enhanced flavonoid profiles for nutritional applications.

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Availability of data and materials

All RNA-seq data contributing to this study have been deposited in NCBI under BioProject: PRJNA613342 (http://www.ncbi.nlm.nih.gov/sra).

Abbreviations

ANS:

Anthocyanidin synthase

ANR:

Anthocyanidin reductase

LAR:

Leucoanthocyanidin reductase

CHS:

Chalcone synthase

FLS:

Flavonol synthase

UFGT:

UDP-glucose:flavonoid 3-O-glucosyltransferase

CHI:

Chalcone isomerase

F3H:

Flavanone 3-hydroxylase

DFR:

Dihydroflavonol 4-reductase

4CL:

4-Coumaroyl-CoA ligase

TPM:

Transcripts Per Kilobase of exon model per Million mapped reads

GO:

Gene ontology

TFs:

Transcription factors

bHLH:

Basic helix-loop-helix

NCBI:

National Center for Biotechnology Information

qRT-PCR:

Quantitative real-time polymerase chain reaction

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Acknowledgements

We thank the specialists from the MetWare Biotechnology Co., Ltd. for the identification and quantification of the metabolites of cacao exocarps samples.

Funding

This work was funded by the National Natural Science Foundation of China (Grant no. 31670684), the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (Grant no. 1630142019003).

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FL and JL conceived and designed the research. LY prepared the experimental materials. FL and BW performed the experiments. FL and XQ analyzed the data and wrote the manuscript. JL provided intellectual input and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Jianxiong Lai.

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Li, F., Wu, B., Yan, L. et al. Metabolome and transcriptome profiling of Theobroma cacao provides insights into the molecular basis of pod color variation. J Plant Res 134, 1323–1334 (2021). https://doi.org/10.1007/s10265-021-01338-9

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Keywords

  • Anthocyanins
  • Flavonoid biosynthesis
  • Flavonols
  • Pod color
  • Theobroma cacao