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

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.

Genome‐wide diversity analysis suggests divergence among Upper Guinea and the Dahomey Gap populations of the Sisrè berry (Syn: miracle fruit) plant (Synsepalum dulcificum [Schumach. & Thonn.] Daniell) in West Africa

“…Although there have been commendable efforts to conduct systematic phenotypic characterizations of various species within the Sapotaceae (Gwali et al., 2012; Sanou et al., 2006; Tchokponhoué et al., 2020), genomic studies remain rare in the family, particularly those in service to understanding patterns of diversity to support genetic improvement. Recent works on Vitellaria paradoxa (Hale et al., 2021), Argania spinosa L. Skeels (Khayi et al., 2020; Slimane et al., 2020), and S. dulcificum (Yang et al., 2022) are notable in terms of bringing high‐resolution sequencing methods to bear in a family for which SSRs remain the most common marker platform to date (Mouhaddab et al., 2017; Pakhrou et al., 2017; Sanou et al., 2005). This study, the first to employ SNP markers to understand population structure and genetic variation in S. dulcificum , lays the groundwork for the systematic, genomics‐assisted conservation and breeding of the species.…”

“…(Foster et al., 2019; Garcia‐Seco et al., 2015), all of which benefit from long breeding histories and extensive genomic resources, Sisrè berry is an orphan crop with no systematic history of breeding or readily available genetic resources or information to facilitate its improvement. Despite the very recent publication of a reference genome for S. dulcificum (Yang et al., 2022), basic information on genetic diversity within the species, though fundamental to implementing an effective breeding program, is scanty and limited to a single low‐resolution assessment of a geographically narrow collection (Chibuzor et al., 2017). Although three distinct phenotypic groups are reported in the species in West Africa (Tchokponhoué et al., 2020), such groups are yet to be corroborated by molecular evidence.…”

Inclusive Overview of Sweeteners Trends: Nutritional Safety and Commercialization

“…The methanolic extract of berry fruit has been screened and characterized for anthocyanins, phytoceuticals, bioactive compounds, luteins and tocopherols. The pharmaceutical advantages of miracle fruit include anti-diabetic, anticancer, anti-hyperuricaemic, anticonvulsant, antioxidant and anti-cholesterolemic properties. − …”

Exploring the diversity, bioactivity of endophytes, and metabolome in Synsepalum dulcificum

“…The extracts of S . dulcificum exhibit several biological activities, including antioxidant, antimicrobial, antitumor, cholesterol-lowing, and antidiabetic effects ( Inglett and Chen, 2011 ; Yang et al, 2022 ). However, studies on the endophytes of S. dulcificum remain scarce.…”

“…S. dulcificum belongs to the family Sapotaceae; after the 1960s, it was introduced to Hainan, Sichuan, Yunnan (Xishuangbanna), and other places in China for cultivation (Tchokponhoue et al, 2021). The extracts of S. dulcificum exhibit several biological activities, including antioxidant, antimicrobial, antitumor, cholesterol-lowing, and antidiabetic effects (Inglett and Chen, 2011;Yang et al, 2022). However, studies on the endophytes of S. dulcificum remain scarce.…”