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. 2023 Oct 25;10(12):uhad214.
doi: 10.1093/hr/uhad214. eCollection 2023 Dec.

The haplotype-resolved autotetraploid genome assembly provides insights into the genomic evolution and fruit divergence in wax apple (Syzygium samarangense (Blume) Merr. and Perry)

Xiuqing Wei  1   2 , Min Chen  3 , Xijuan Zhang  1 , Yinghao Wang  2 , Liang Li  1 , Ling Xu  1 , Huanhuan Wang  2 , Mengwei Jiang  2 , Caihui Wang  1 , Lihui Zeng  2 , Jiahui Xu  1
Affiliations

The haplotype-resolved autotetraploid genome assembly provides insights into the genomic evolution and fruit divergence in wax apple (Syzygium samarangense (Blume) Merr. and Perry)

Xiuqing Wei et al. Hortic Res. .

Abstract

Wax apple (Syzygium samarangense) is an economically important fruit crop with great potential value to human health because of its richness in antioxidant substances. Here, we present a haplotype-resolved autotetraploid genome assembly of the wax apple with a size of 1.59 Gb. Comparative genomic analysis revealed three rounds of whole-genome duplication (WGD) events, including two independent WGDs after WGT-γ. Resequencing analysis of 35 accessions partitioned these individuals into two distinct groups, including 28 landraces and seven cultivated species, and several genes subject to selective sweeps possibly contributed to fruit growth, including the KRP1-like, IAA17-like, GME-like, and FLACCA-like genes. Transcriptome analysis of three different varieties during flower and fruit development identified key genes related to fruit size, sugar content, and male sterility. We found that AP2 also affected fruit size by regulating sepal development in wax apples. The expression of sugar transport-related genes (SWEETs and SUTs) was high in 'ZY', likely contributing to its high sugar content. Male sterility in 'Tub' was associated with tapetal abnormalities due to the decreased expression of DYT1, TDF1, and AMS, which affected early tapetum development. The chromosome-scale genome and large-scale transcriptome data presented in this study offer new valuable resources for biological research on S. samarangense and shed new light on fruit size control, sugar metabolism, and male sterility regulatory metabolism in wax apple.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Alignment of the Syzygium samarangense monoploid genome with the S. samarangense genome and summary of the genome assembly. (a) A set of four homologous chromosomes aligned to a single monoploid chromosome. (b) From the outermost to innermost layer, the rings indicate the haplotype genomes in Mbp (i), GC content (ii), gene density (iii), SNP density (iv), SV density (v), expression (iv) and synteny blocks, respectively.
Figure 2
Figure 2
Phylogenetic and comparative analysis of Syzygium samarangense. (a) Phylogenetic tree of S. samarangense, Eucalyptus grandis, Punica granatum, Arabidopsis thaliana, Vitis vinifera, Oryza sativa, Nyctophila colorata, Solanum lycopersicum, Psidium guajava, Prunus persica, Rhodomyrtus tomentosa, and Amborella trichopoda. Gene family expansion/contraction analysis of the S. samarangense genome. The divergence times of S. samarangense and the other species are labelled at the bottom. (b) Orthologous and species-specific gene families in S. samarangense and the other species. (c) Distribution of synonymous substitution rates (Ks) among S. samarangense paralogues and orthologues with other species. (d) Alignment of the S. samarangense genome with the V. vinifera genome.
Figure 3
Figure 3
Phylogenetic splits and population genetic structure of 35 Syzygium samarangense accessions. (a) Maximum-likelihood tree of 35 resequenced S. samarangense individuals constructed based on 2 630 417 SNPs. (b) PCA plots of S. samarangense accessions showed two subgroups (Group_2, cultivars; Group_1, landraces). PC, principal component. (c) ADMIXTRUE analysis among the accessions revealed the distribution of K = 2 genetic clusters with the lowest cross-validation error. (d) Comparison of fruit weight between landraces and cultivars.
Figure 4
Figure 4
. Genes related to fruit growth and sugar content. (a) The expression of sepal development homologues (AP1 and AP2) in ‘DK’, ‘ZY’, and ‘Tub’ during fruit development. (b) Comparison of fruit weight among ‘DK’, ‘ZY’, and ‘Tub’. ****P-value <0.0001, t-test, n = 10. (c) Comparison of sugar content between ‘Tub’ and ‘ZY’ fruit at maturity. ***P-value <0.001, t-test. (d) Expression of the candidate genes related to sugar transport (SWEETs, ERDLs, and TST) in the pink module in ‘DK’ and ‘Tub’ during fruit development. ‘DK’: ‘Dongkeng’; ‘Tub’: ‘Tub Ting Jiang’. FrT1, FrT2, FrT3, FrT4, and FrT5 represent 10 to 50 DAFB (days after full bloom) at approximately 10-day intervals.
Figure 5
Figure 5
Anther development, pollen germination rate, and expression of anther and pollen development-related genes in ‘DK’, ‘ZY’, and ‘Tub’. (a) Anther development and dehiscence in ‘DK’. T1-T5 are consistent with FlT1-FlT5, and T6 represents 12 hours after blooming. (b) Anther development in ‘Tub’. T1-T5 are consistent with FlT1-FlT5, and T6 represents 12 hours after blooming. (c) Pollen germination rate of ‘Tub’, ‘ZY’, and ‘DK’. ****P-value <0.0001, t-test, n = 10. (d) Expression (FPKM) of anther and pollen development-related genes in ‘DK’, ‘ZY’, and ‘Tub’ from flowers at different stages, including FlT1, FlT2, FlT3, FlT4, and FlT5.
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