Abstract
Miracle fruit (Synsepalum dulcificum) is a rare valuable tropical plant famous for a miraculous sweetening glycoprotein, miraculin, which can modify sour flavors to sweet flavors tasted by humans. Here, we present a chromosome-level high-quality genome of S. dulcificum with an assembly genome size of ∼550 Mb, contig N50 of ∼14.14 Mb, and 37,911 annotated protein-coding genes. Phylogenetic analysis revealed that S. dulcificum was most closely related to Camellia sinensis and Diospyros oleifera, and that S. dulcificum diverged from the Diospyros genus ∼75.8 million years ago (MYA), and that C. sinensis diverged from Synsepalum ∼63.5 MYA. Ks assessment and collinearity analysis with S. dulcificum and other species suggested that a whole-genome duplication (WGD) event occurred in S. dulcificum and that there was good collinearity between S. dulcificum and Vitis vinifera. On the other hand, transcriptome and metabolism analysis with six tissues containing three developmental stages of fleshes and seeds of miracle fruit revealed that Gene Ontology (GO) terms and metabolic pathways of “cellular response to chitin,” “plant–pathogen interaction,” and “plant hormone signal transduction” were significantly enriched during fruit development. Interestingly, the expression of miraculin (Chr10G0299340) progressively increased from vegetative organs to reproductive organs and reached an incredible level in mature fruit flesh, with an fragments per kilobase of transcript per million (FPKM) value of ∼113,515, which was the most highly expressed gene among all detected genes. Combining the unique signal peptide and the presence of the histidine-30 residue together composed the main potential factors impacting miraculin’s unique properties in S. dulcificum. Furthermore, integrated analysis of weighted gene coexpression network analysis (WGCNA), enrichment and metabolite correlation suggested that miraculin plays potential roles in regulating plant growth, seed germination and maturation, resisting pathogen infection, and environmental pressure. In summary, valuable genomic, transcriptomic, and metabolic resources provided in this study will promote the utilization of S. dulcificum and in-depth research on species in the Sapotaceae family.
Highlights
Miracle fruit (Synsepalum dulcificum) is famous for a sweetening glycoprotein, namely, miraculin, which has a taste-modifying activity that converts sour taste to sweet (Kurihara and Beidler, 1968; Misaka, 2013; Niu et al, 2020)
We found that during the evolutionary process, histidine-30 residues and signal peptides were unique to miraculin in miracle fruit, which may have important implications for the production of its function and the evolution of which
We found that the role of miraculin in miracle fruit is mainly to resist germ infection, defend against environmental pressure and regulate plant growth
Summary
Miracle fruit (Synsepalum dulcificum) is famous for a sweetening glycoprotein, namely, miraculin, which has a taste-modifying activity that converts sour taste to sweet (Kurihara and Beidler, 1968; Misaka, 2013; Niu et al, 2020). Miracle fruit is a native plant of tropical west and central Africa, occasionally distributed from West Africa to the Congo (Achigan-Dako et al, 2015). In the 1960s, miracle fruit was introduced to China as the national gift from the Republic of Ghana to Premier Enlai Zhou. Exports of miracle fruit are protected and prohibited in China and West Africa due to its high prize. Miracle fruit is an evergreen shrub belonging to the Synsepalum genus of the Sapotaceae family that has ∼50 genera and 1,100 species. Most species in Sapotaceae are trees and shrubs, which commonly have unique fruit flavors and are widely distributed in tropical and subtropical regions (Khayi et al, 2020)
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