Java apple (Syzygium samarangense) genome reveals evolution of fruit size, sweetness and seedlessness

NEWS - Researchers have successfully decoded the autotetraploid genome of wax apple or java apple (Syzygium samarangense) revealing the genetic evolution and key factors driving fruit diversity. The study highlights a rich antioxidant profile that promises health benefits and breeding strategies to improve nutritional value.

S. samarangense, with its crisp texture, fresh aroma and health benefits, faces breeding challenges due to complex genetic diversity and limited genomic data. These constraints have hampered efforts to improve fruit qualities such as size and sugar content.

The researchers identified 344 single-copy genes from 12 genomes sequenced using OrthoFinder and then used them to construct a phylogenetic tree. S. samarangense, Eucalyptus grandis, Psidium guajava, Rhodomyrtus tomentosa and Punica granatum belong to the same branch of Myrtales. The divergence of Myrtales occurred 79.4 million years ago.

A much closer genetic relationship was observed between S. samarangense and E. grandis. The two species diverged from each other 26 million years ago. CAFÉ analysis characterized 1328 expanded gene families and 5363 reduced gene families.

Gene Ontology (GO) enrichment analysis showed that the 1328 expanded gene families were mainly enriched in DNA polymerase activity, nucleocapsid retrotransposons and mitochondrial fission. In contrast, 5363 gene families were mainly enriched in serine/threonine kinase protein activity, flower organ senescence, and secondary metabolite biosynthesis processes.

Compared with other species, 537 unique gene families were identified in the S. samarangense genome. These gene families were mainly enriched in a series of functional items, including catalytic activities acting on DNA, retrotransfer, nucleocapsid, transfer, and mediated RNA.

Comparison among the four haplotypes revealed 4.53 million SNPs, 0.49 million short indels, and 10,925 structural variations (SVs). These genetic variations were evenly distributed along the 44 chromosomes. Chromosome-specific 13-mer clustering divided each set of four haplotypes together which was inconsistent with the allotetraploid Miscanthus genome and showed separate subgenome distributions. Smudge plot analysis identified the AAAB pattern as the dominant component accounting for 56% of the examined K-mers.

These results collectively indicate that S. samarangense has an autotetraploid genome with a high degree of heterozygosity. The distribution of synonymous substitutions per synonymous site (Ks) of homologous gene pairs clearly illustrates that the S. samarangense genome has undergone three rounds (WGT-γ, WGD-1, and WGD-2) of whole genome duplication events.

In addition to WGT-γ which is common in the evolutionary history of grape and E. grandis, researchers found that S. samarangense and E. grandis have also undergone an independent whole genome duplication (WGD-1). Compared with the situation in E. grandis, the specific WGD-1 event that occurred in the S. samarangense genome is more complex.

In addition, the synteny relationship between S. samarangense and Vitis vinifera was further analyzed to verify that WGD-1 and WGD-2 occurred after WGT-γ. The collinearity relationship between S. samarangense and V. vinifera was 8:1, indicating the occurrence of two lineage-specific WGDs in S. samarangense.

The research team published chromosome-scale genome and transcriptome data of the species with a focus on genes regulating size, sugar metabolism and male sterility. The findings open up new possibilities for molecular breeding of varieties.

The 1.59 Gb genome reveals three rounds of genome duplication events. Key genes influencing fruit size, including APETALA1 (AP1) and APETALA1 (AP2), drive growth by regulating sepal development. Sweetness has been associated with the expression of sugar transporter genes such as Sugars Will Finally be Exported Transporters (SWEETS) and Sucrose Transporters (SUTs).

Male sterility is a result of the lack of expression of genes such as DYSFUNCTIONAL TAPETUM1 (DYT1), TAPETUM DEVELOPMENT AND FUNCTION1 (TDF1), and ABORTED MICROSPORE (AMS) which are essential for tapetum development and pollen viability. Male sterility contributes to seedless fruit formation, a highly valued trait in the market.

“This is a major advance in understanding the genetic basis of these important fruit traits. The genomic haplotypes are an important resource for exploring genetic diversity and selective breeding to create superior varieties with improved size, sweetness and seedlessness,” said Lihui Zeng from Fujian Agriculture and Forestry University.

This research can accelerate breeding programs focused on developing wax apples with improved fruit size, higher sugar content and seedlessness traits that are in line with consumer demand. These findings also provide a valuable framework for improving other fruits facing breeding challenges and strides in the field of horticultural genomics.

Original research

Xiuqing Wei, Min Chen, Xijuan Zhang, Yinghao Wang, Liang Li, Ling Xu, Huanhuan Wang, Mengwei Jiang, Caihui Wang, Lihui Zeng, Jiahui Xu, The haplotype-resolved autotetraploid genome assembly provides insights into the genomic evolution and fruit divergence in wax apple (Syzygium samarangense (Blume) Merr. and Perry), Horticulture Research, Volume 10, Issue 12, December 2023, uhad214, DOI:10.1093/hr/uhad21

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