The Chromosome-Level Genome of Miracle Fruit (Synsepalum dulcificum) Provides New Insights Into the Evolution and Function of Miraculin

Abstract

Miracle fruit (<i>Synsepalum dulcificum</i>) 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 <i>S. dulcificum</i> 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 <i>S. dulcificum</i> was most closely related to <i>Camellia sinensis</i> and <i>Diospyros oleifera</i>, and that <i>S. dulcificum</i> diverged from the <i>Diospyros</i> genus ∼75.8 million years ago (MYA), and that <i>C. sinensis</i> diverged from <i>Synsepalum</i> ∼63.5 MYA. Ks assessment and collinearity analysis with <i>S. dulcificum</i> and other species suggested that a whole-genome duplication (WGD) event occurred in <i>S. dulcificum</i> and that there was good collinearity between <i>S. dulcificum</i> and <i>Vitis vinifera</i>. 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 <i>S. dulcificum</i>. 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 <i>S. dulcificum</i> and in-depth research on species in the Sapotaceae family.