The American Cherimoya Genome reveals insights into the intra-specific divergence, the evolution of magnoliales, and a putative gene cluster for acetogenin biosynthesis

Authors: LI, TANG - University Of Nebraska; NOUSIAS, ORESTIS - University Of Nebraska; ZHENG, JINFANG - University Of Nebraska; Meinhardt, Lyndel; Goenaga, Ricardo; Zhang, Dapeng; YIN, YANBIN - University Of Nebraska

Submitted to: Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/21/2024
Publication Date: 2/26/2024
Citation: Li, T., Nousias, O., Zheng, J., Meinhardt, L.W., Goenaga, R.J., Zhang, D., Yin, Y. 2024. The American Cherimoya Genome reveals insights into the intra-specific divergence, the evolution of magnoliales, and a putative gene cluster for acetogenin biosynthesis. Plants. 13(5):636. https://doi.org/10.3390/plants13050636.
DOI: https://doi.org/10.3390/plants13050636

Interpretive Summary: Despite the rapid progress in draft genome sequencing, development and application of genomic tools in tropical fruit still lagged the temperate fruits. Majority of the tropical fruit species are still in the orphanage status in terms of genomic research tools. Here, we report the draft genome of Annona cherimola (cherimoya, or custard apple), a species of the Annonaceae family within the magnoliid clade. Cherimoya is renowned for its delectable fruit and valuable bioactive compounds used in traditional medicines. In this study, we developed a chromosome-level genome assembly for the cherimoya 'Booth' cultivar from the United States. The draft genome of cherimoya contains seven pseudo-chromosomes assembled at the chromosomal level. We found that cherimoya has a unique whole genome duplication event that is distinct from other species of magnoliids. Genome comparison revealed that the US cultivar ‘Booth’ has 25% more repeats than the Spanish cultivar ‘Fino de Jete’, despite their highly similar (> 99%) genome sequence identity. These two cultivars were found to be diverged during the early Pleistocene, which suggests a different origin and domestication of the cherimoya cultivars. We have also identified a potential gene cluster that is responsible for the biosynthesis of acetogenins, a potential anticancer agents which is exclusively found in Annonaceae species. These results will be used by researchers and horticultural industry to develop new research tools for supporting characterization, conservation and utilization of Annona genetic resources.

Technical Abstract: Annona cherimola (cherimoya or custard apple) is a species renowned for its delectable fruit and medicinal properties. In this study, we developed a chromosome-level genome assembly for the cherimoya 'Booth' cultivar from the United States. The genome assembly has a size of 794 Mb with a N50 = 97.59 Mb. The seven longest scaffolds account for 87.6% of the total genome length, which corresponds to the seven pseudo-chromosomes. A total of 45,272 protein-coding genes (>=30 aa) were predicted with 92.9% gene content completeness. A unique whole genome duplication (WGD) event was identified in cherimoya, which distinguishes it from other magnoliids. Phylogenetic analysis supports that eudicots and magnoliids are more closely related to each other than to monocots. Moreover, the Magnoliales was found to be more closely related to the Laurales than the Piperales. Genome comparison revealed that the ‘Booth’ cultivar has 200Mb more repeats than the Spanish cultivar ‘Fino de Jete’, despite their highly similar (> 99%) genome sequence identity and collinearity. These two cultivars were diverged during the early Pleistocene (1.93 Mya), which suggests a different origin and domestication of the cherimoya cultivars. Prediction of resistance gene analogs showed that terpene/terpenoid metabolism functions are enriched in Magnoliales, while TNL (Toll/Interleukin-1-NBS-LRR) disease resistance gene has been lost in Magnoliales during evolution. We have also identified a potential gene cluster that is responsible for the biosynthesis of acetogenins, which is found exclusively in Annonaceae. The cherimoya genome provides an invaluable resource for supporting characterization, conservation and utilization of Annona genetic resources.