Chromosome-scale genome assembly provides insights into the evolution and flavor synthesis of passion fruit (Passiflora edulis Sims)

Zhiqiang Xia , Dongmei Huang , Shengkui Zhang , Wenquan Wang , Funing Ma , Bin Wu , Yi Xu , Bingqiang Xu , Di Chen , Meiling Zou , Huanyu Xu , Xincheng Zhou , Rulin Zhan , Shun Song

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 14

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :14 DOI: 10.1038/s41438-020-00455-1
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Chromosome-scale genome assembly provides insights into the evolution and flavor synthesis of passion fruit (Passiflora edulis Sims)
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Abstract

Passion fruit (Passiflora edulis Sims) is an economically valuable fruit that is cultivated in tropical and subtropical regions of the world. Here, we report an ~1341.7 Mb chromosome-scale genome assembly of passion fruit, with 98.91% (~1327.18 Mb) of the assembly assigned to nine pseudochromosomes. The genome includes 23,171 protein-coding genes, and most of the assembled sequences are repetitive sequences, with long-terminal repeats (LTRs) being the most abundant. Phylogenetic analysis revealed that passion fruit diverged after Brassicaceae and before Euphorbiaceae. Ks analysis showed that two whole-genome duplication events occurred in passion fruit at 65 MYA and 12 MYA, which may have contributed to its large genome size. An integrated analysis of genomic, transcriptomic, and metabolomic data showed that ‘alpha-linolenic acid metabolism’, ‘metabolic pathways’, and ‘secondary metabolic pathways’ were the main pathways involved in the synthesis of important volatile organic compounds (VOCs) in passion fruit, and this analysis identified some candidate genes, including GDP-fucose Transporter 1-like, Tetratricopeptide repeat protein 33, protein NETWORKED 4B isoform X1, and Golgin Subfamily A member 6-like protein 22. In addition, we identified 13 important gene families in fatty acid pathways and eight important gene families in terpene pathways. Gene family analysis showed that the ACX, ADH, ALDH, and HPL gene families, especially ACX13/14/15/20, ADH13/26/33, ALDH1/4/21, and HPL4/6, were the key genes for ester synthesis, while the TPS gene family, especially PeTPS2/3/4/24, was the key gene family for terpene synthesis. This work provides insights into genome evolution and flavor trait biology and offers valuable resources for the improved cultivation of passion fruit.

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Zhiqiang Xia, Dongmei Huang, Shengkui Zhang, Wenquan Wang, Funing Ma, Bin Wu, Yi Xu, Bingqiang Xu, Di Chen, Meiling Zou, Huanyu Xu, Xincheng Zhou, Rulin Zhan, Shun Song. Chromosome-scale genome assembly provides insights into the evolution and flavor synthesis of passion fruit (Passiflora edulis Sims). Horticulture Research, 2021, 8 (1) : 14 DOI:10.1038/s41438-020-00455-1

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References

[1]

Ortiz, D. C. et al. Evaluating purple passion fruit (Passiflora edulis Sims f. edulis) genetic variability in individuals from commercial plantations in Colombia. Genet. Resour. Crop Evol. 59, 1089-1099 (2012).

[2]

Kugler, E. E. & King, L. A. A Brief History of the Passionflower (Timber Press, Portland, Oregon, 2004).

[3]

Feuillet, C. & Macdougal, J. M. A new infrageneric classification of Passiflora L. (Passifloraceae). Passiflora 13, 34-38 (2003).

[4]

Cerqueira-Silva, C. B. M., Jesus, O. N., Santos, E. S. L., Corrêa, R. X. & Souza, A. P. Genetic breeding and diversity of the genus Passiflora: progress and perspectives in molecular and genetic studies. Int. J. Mol. Sci. 15, 14122-14152 (2014).

[5]

Abreu, P. P. et al. Passion flower hybrids and their use in the ornamental plant market: perspectives for sustainable development with emphasis on Brazil. Euphytica 166, 307-315 (2009).

[6]

Santos, E. A. et al. Confirmation and characterization of interspecific hybrids of Passiflora L. (Passifloraceae) for ornamental use. Euphytica 184, 389-399 (2012).

[7]

Costa, J. L., Jesus, O. N. D., Oliveira, G. A. F. & Oliveira, E. J. D. Effect of selection on genetic variability in yellow passion fruit. Crop Breed. Appl. Biotechnol. 12, 253-260 (2012).

[8]

Deng, J., Zhou, Y., Bai, M., Li, H. & Li, L. Anxiolytic and sedative activities of Passiflora edulis f. flavicarpa. J. Ethnopharmacol. 128, 148-153 (2010).

[9]

García-Rui, A. et al. Banana passion fruit (Passiflora mollissima (Kunth) L.H. Bailey): microencapsulation, phytochemical composition and antioxidant capacity. Molecules 22, 85 (2017).

[10]

Gadioli et al. A systematic review on phenolic compounds in Passiflora plants: exploring biodiversity for food, nutrition, and popular medicine. Crit. Rev. Food Sci. Nutr. 58, 785-807 (2018).

[11]

Foudah, A. I., Alam, P., Kamal, Y. T., Alqasoumi, S. I. & Yusufoglu, H. S. Development and validation of a high-performance thin-layer chromatographic method for the quantitative analysis of vitexin in Passiflora foetida herbal formulations. Saudi Pharm. J. 27, 1157-1163 (2019).

[12]

Rudnicki, M., Silveira, M. M., Pereira, T. V., Oliveira, M. R. & Moreira, J. C. F. Protective effects of Passiflora alata extract pretreatment on carbon tetrachloride induced oxidative damage in rats. Food Chem. Toxicol. 45, 656-661 (2007).

[13]

Santos, A. et al. Begin at the beginning: A BAC-end view of the passion fruit (Passiflora) genome. BMC Genomics 15, 816 (2014).

[14]

Susan, A. et al. Microsatellite marker development by partial sequencing of the sour passion fruit genome (Passiflora edulis Sims). BMC Genomics 18, 549 (2017).

[15]

Costa, Z. P. D., Munhoz, C. D. F. & Vieira, M. L. C. Report on the development of putative functional SSR and SNP markers in passion fruits. BMC Res. Notes 10, 445 (2017).

[16]

Melo, N. F. D., Cervi, A. C. & Guerra, M. Karyology and cytotaxonomy of the genus Passiflora L. (Passifloraceae). Plant Systemat. Evol. 226, 69-84 (2001).

[17]

Li, R. et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20, 265-272 (2010).

[18]

Burton, J. N. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119 (2013).

[19]

Waterhouse, R. M. et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 35, 543-548 (2017).

[20]

Heng, L., Durbin & Richard Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).

[21]

Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094-3100 (2018).

[22]

Mario, S. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, 435-439 (2006).

[23]

Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

[24]

Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).

[25]

Lagesen, K. et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100 (2007).

[26]

Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 (1997).

[27]

Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933-2935 (2013).

[28]

Philip, J. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240 (2014).

[29]

Chen, X. et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, 316-322 (2011).

[30]

Zheng, Y. et al. iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol. Plant 9, 1667-1670 (2016).

[31]

Li, L. Jr, S., C. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003).

[32]

Price et al. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

[33]

Sudhir, K., Glen, S., Michael, S. & Blair, H. S. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 7, 1812 (2017).

[34]

Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

[35]

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).

[36]

Varet, H., Brillet-Guéguen, L., Coppée, J. Y. & Dillies, M. A. SARTools: a DESeq2-and EdgeR-based R pipeline for comprehensive differential analysis of RNA-seq data. PLoS ONE 11, e0157022 (2016).

[37]

Eddy, R. S. Accelerated profile HMM searches. PLoS Comp. Biol. 7, e1002195 (2011).

[38]

Tuskan, G. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604 (2006).

[39]

Argout, X. et al. The genome of Theobroma cacao. Nat. Genet. 43, 101-108 (2010).

[40]

Chan, A. P. et al. Draft genome sequence of the oilseed species Ricinus communis. Nat. Biotechnol. 28, 951-956 (2010).

[41]

Cauz-Santos, L. A. et al. The chloroplast genome of Passiflora edulis (Passifloraceae) assembled from long sequence reads: structural organization and phylogenomic studies in Malpighiales. Front. Plant Sci. 8, 334 (2017).

[42]

Coelho, G. L. V., Mendes, M. F. & Pessoa, F. L. P. Handbook of Fruit and Vegetable Flavors (John Wiley & Sons, Hoboken, NJ, 2010).

[43]

Aubourg, S., Lecharny, A. & Bohlmann, J. Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol. Genet. Genomics 267, 730-745 (2002).

[44]

Wu, H. et al. A high-quality Actinidia chinensis (kiwifruit) genome. Hortic. Res. 6, 117 (2019).

[45]

Fan, Y. et al. Dissecting the genome of star fruit (Averrhoa carambola L.). Hortic. Res. 7, 94 (2020).

[46]

Belser, C. et al. Chromosome-scale assemblies of plant genomes using nanopore long reads and optical maps. Nat. Plants 4, 879-887 (2018).

[47]

Jain, M. et al. Nanopore sequencing and assembly of a human genome with ultra-long reads. Nat. Biotechnol. 36, 338-345 (2018).

[48]

Jiao, W. B. et al. Improving and correcting the contiguity of long-read genome assemblies of three plant species using optical mapping and chromosome conformation capture data. Genome Res. 27, 778 (2017).

[49]

Munhoz, C. F., Costa, Z. P., Cauz-Santos, L. A., Reátegui, A. C. E. & Vieira, M. L. C. A gene-rich fraction analysis of the Passiflora edulis genome reveals highly conserved microsyntenic regions with two related Malpighiales species. Sci. Rep. 8, 13024 (2018).

[50]

Bredeson, J. V. et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat. Biotechnol. 34, 562-570 (2016).

[51]

Moaine, E. B. & Olivier, P. Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol. Evol. 5, 954-965 (2013).

[52]

Janzantti, N. S. & Monteiro, M. HS-GC-MS-O analysis and sensory acceptance of passion fruit during maturation. J. Food Sci. Technol. 54, 2594-2601 (2017).

[53]

Echeverrı́a, G., Graell, J., López, M. L. & Lara, I. Volatile production, quality and aroma-related enzyme activities during maturation of ‘Fuji’ apples. Postharvest Biol. Technol. 31, 217-227 (2004).

[54]

Song, J. & Bangerth, F. Fatty acids as precursors for aroma volatile biosynthesis in pre-climacteric and climacteric apple fruit. Postharvest Biol. Technol. 30, 113-121 (2003).

[55]

Li, X., Tieman, D., Liu, Z., Chen, K. & Klee, H. J. Identification of a lipase gene with a role in tomato fruit short-chain fatty acid-derived flavor volatiles by genome-wide association. Plant J. 104, 631-644 (2020).

[56]

Jordan, M. J., Goodner, K. & Shaw, P. E. Volatile components in banana (Musa acuminata colla cv. Cavendish) and yellow passion fruit (Passiflora edulis Sims flavicarpa Degner) as determined by GC-MS and GC-olfactometry. Proc. Fla. State Hort. Soc. 114, 153-157 (2001).

[57]

Defilippi, B. G., Kader, A. A. & Dandekar, A. M. Apple aroma: alcohol acyltransferase, a rate limiting step for ester biosynthesis, is regulated by ethylene. Plant Sci. 168, 1199-1210 (2005).

[58]

Niziol, J., Misiorek, M. & Ruman, T . Mass spectrometry imaging of low molecular weight metabolites in strawberry fruit (Fragaria x ananassa Duch.) cv. Primoris with109Ag nanoparticle enhanced target . Phytochemistry 159, 11-19 (2019).

[59]

Chen, H., Cao, S., Jin, Y., Tang, Y. & Qi, H. The relationship between CmADHs and the diversity of volatile organic compounds of three aroma types of melon (Cucumis melo). Front. Physiol. 7, 254 (2016).

[60]

Tholl, D. Biosynthesis and biological functions of terpenoids in plants. Adv. Biochem. Eng. Biotechnol. 148, 63-106 (2015).

[61]

Muchlinski, A. et al. Diversity and function of terpene synthases in the production of carrot aroma and flavor compounds. Sci. Rep. 10, 9989 (2020).

[62]

Kulheim, C. et al. The Eucalyptus terpene synthase gene family. BMC Genomics 16, 450 (2015).

[63]

Chen, S. et al. E)-Nerolidol is a volatile signal that induces defenses against insects and pathogens in tea plants. Hortic. Res. 7, 52 (2020).

[64]

Song, X. et al. Deciphering the high-quality genome sequence of coriander that causes controversial feelings. Plant Biotechnol. J. 18, 1444-1456 (2020).

[65]

Dudareva, N., Klempien, A., Muhlemann, J. K. & Kaplan, I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. N. Phytol. 198, 16-32 (2013).

[66]

Singh, R. K., Sane, V. A., Misra, A., Ali, S. A. & Nath, P. Differential expression of the mango alcohol dehydrogenase gene family during ripening. Phytochemistry 71, 1485-1494 (2010).

[67]

Singh, R. K., Srivastava, S., Chidley, H. G., Nath, P. & Sane, V. A. Overexpression of mango alcohol dehydrogenase (MiADH1) mimics hypoxia in transgenic tomato and alters fruit flavor components. Agric. Gene 7, 23-33 (2018).

[68]

Qin, G. et al. Identification and expression patterns of alcohol dehydrogenase genes involving in ester volatile biosynthesis in pear fruit. J. Integr. Agric. 16, 1742-1750 (2017).

[69]

Zhu, G. et al. Rewiring of the fruit metabolome in tomato breeding. Cell 172, 249-261 (2018).

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