A phased Vanilla planifolia genome enables genetic improvement of flavour and production.


Journal

Nature food
ISSN: 2662-1355
Titre abrégé: Nat Food
Pays: England
ID NLM: 101761102

Informations de publication

Date de publication:
Dec 2020
Historique:
received: 19 05 2020
accepted: 09 11 2020
medline: 1 12 2020
pubmed: 1 12 2020
entrez: 2 5 2023
Statut: ppublish

Résumé

The global supply of vanilla extract is primarily sourced from the cured beans of the tropical orchid species Vanilla planifolia. Vanilla plants were collected from Mesoamerica, clonally propagated and globally distributed as part of the early spice trade. Today, the global food and beverage industry depends on descendants of these original plants that have not generally benefited from genetic improvement. As a result, vanilla growers and processors struggle to meet global demand for vanilla extract and are challenged by inefficient and unsustainable production practices. Here, we report a chromosome-scale, phased V. planifolia genome, which reveals sequence variants for genes that may impact the vanillin pathway and therefore influence bean quality. Resequencing of related vanilla species, including the minor commercial species Vanilla × tahitensis, identified genes that could impact productivity and post-harvest losses through pod dehiscence, flower anatomy and disease resistance. The vanilla genome reported in this study may enable accelerated breeding of vanilla to improve high-value traits.

Identifiants

pubmed: 37128067
doi: 10.1038/s43016-020-00197-2
pii: 10.1038/s43016-020-00197-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

811-819

Informations de copyright

© 2020. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Childers, N. F. Vanilla Culture in Puerto Rico (US Department of Agriculture, 1948).
Medina, J. D. L. C., Jiménes, G. C. R. & García, H. S. Vanilla: Post-Harvest Operations (Food and Agriculture Organization of the United Nations, 2009).
Vanilla Beans and Extract Market Worth US$ 4.3 Bn by 2025 (Acumen Research and Consulting, 2019).
Correll, D. S. Vanilla—its botany, history, cultivation and economic import. Econ. Bot. 7, 291–358 (1953).
doi: 10.1007/BF02930810
Ecott, T. Vanilla: Travels in Search of the Luscious Substance (Penguin UK, 2005).
Chambers, A. H. Advances in Plant Breeding Strategies: Industrial and Food Crops Ch. 18 (Springer, 2019).
Chambers, A. H., Moon, P., Edmond, V. & Bassil, E. Vanilla Cultivation in Southern Florida (EDIS, 2019).
Sasikumar, B. Vanilla breeding—a review. Agric. Rev. 31, 139–144 (2010).
Lepers-Andrzejewski, S., Causse, S., Caromel, B., Wong, M. & Dron, M. Genetic linkage map and diversity analysis of Tahitian vanilla (Vanilla × tahitensis, Orchidaceae). Crop Sci. 52, 795–806 (2012).
doi: 10.2135/cropsci2010.11.0634
Yang, H. L. et al. A re-evaluation of the final step of vanillin biosynthesis in the orchid Vanilla planifolia. Phytochemistry 139, 33–46 (2017).
pubmed: 28411481 doi: 10.1016/j.phytochem.2017.04.003
Dong, Y. & Wang, Y. Z. Seed shattering: from models to crops. Front. Plant Sci. 6, 476 (2015).
pubmed: 26157453 pmcid: 4478375
Lapeyre-Montes, F., Conejero, G., Verdeil, J.-L. & Odoux, E. in Vanilla (Medicinal and Aromatic Plants—Industrial Profiles) (eds Odoux, E. & Grisoni, M.) Ch. 10 (CRC Press, 2010).
Soto-Arenas, M. & Cameron, K. in Genera Orchidacearum Vol. 3 (eds Pridgeon, A. M. et al.) 321–334 (Oxford Univ. Press, 2003).
Gigant, R. L. et al. in Microsatellite Markers Ch. 4, 73–93 (IntechOpen, 2016).
National Academies of Sciences, Engineering, and Medicine A Review of the Citrus Greening Research and Development Efforts Supported by the Citrus Research and Development Foundation: Fighting a Ravaging Disease (National Academies Press, 2018).
Ploetz, R. C. Fusarium wilt of banana. Phytopathology 105, 1512–1521 (2015).
pubmed: 26057187 doi: 10.1094/PHYTO-04-15-0101-RVW
Delassus, M. La lutte contre la fusariose du vanillier par les méthodes génétiques. Agron. Trop. 18, 245–246 (1963).
Hu, Y. et al. Genomics-based diversity analysis of vanilla species using a Vanilla planifolia draft genome and genotyping-by-sequencing. Sci. Rep. 9, 3416 (2019).
pubmed: 30833623 pmcid: 6399343 doi: 10.1038/s41598-019-40144-1
Brown, S. C. et al. DNA remodeling by strict partial endoreplication in orchids, an original process in the plant kingdom. Genome Biol. Evol. 9, 1051–1071 (2017).
pubmed: 28419219 pmcid: 5546068 doi: 10.1093/gbe/evx063
Bory, S. et al. Natural polyploidy in Vanilla planifolia (Orchidaceae). Genome 51, 816–826 (2008).
pubmed: 18923533 doi: 10.1139/G08-068
Lepers-Andrzejewski, S., Siljak-Yakovlev, S., Brown, S. C., Wong, M. & Dron, M. Diversity and dynamics of plant genome size: an example of polysomaty from a cytogenetic study of Tahitian vanilla (Vanilla × tahitensis, Orchidaceae). Am. J. Bot. 98, 986–997 (2011).
pubmed: 21613071 doi: 10.3732/ajb.1000415
Cai, J. et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47, 65–72 (2015).
pubmed: 25420146 doi: 10.1038/ng.3149
Zhang, G. Q. et al. The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci. Rep. 6, 19029 (2016).
pubmed: 26754549 pmcid: 4709516 doi: 10.1038/srep19029
Zhang, G. Q. et al. The Apostasia genome and the evolution of orchids. Nature 549, 379–383 (2017).
pubmed: 28902843 pmcid: 7416622 doi: 10.1038/nature23897
Wang, W. et al. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nat. Commun. 5, 3311 (2014).
pubmed: 24548928 doi: 10.1038/ncomms4311
Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435–1442 (2015).
pubmed: 26523774 pmcid: 4867222 doi: 10.1038/ng.3435
Lubinsky, P. et al. Neotropical roots of a Polynesian spice: the hybrid origin of Tahitian vanilla, Vanilla tahitensis (Orchidaceae). Am. J. Bot. 95, 1040–1047 (2008).
pubmed: 21632424 doi: 10.3732/ajb.0800067
Gallage, N. J. et al. The intracellular localization of the vanillin biosynthetic machinery in pods of Vanilla planifolia. Plant Cell Physiol. 59, 304–318 (2018).
pubmed: 29186560 doi: 10.1093/pcp/pcx185
Rao, X. et al. A deep transcriptomic analysis of pod development in the vanilla orchid (Vanilla planifolia). BMC Genomics 15, 964 (2014).
pubmed: 25380694 pmcid: 4233054 doi: 10.1186/1471-2164-15-964
Gallage, N. J. & Møller, B. L. in Biotechnology of Natural Products Ch. 1, 3–24 (Springer, 2018).
Widiez, T. et al. Functional characterization of two new members of the caffeoyl CoA O-methyltransferase-like gene family from Vanilla planifolia reveals a new class of plastid-localized O-methyltransferases. Plant Mol. Biol. 76, 475–488 (2011).
pubmed: 21629984 doi: 10.1007/s11103-011-9772-2
Fock-Bastide, I. et al. Expression profiles of key phenylpropanoid genes during Vanilla planifolia pod development reveal a positive correlation between PAL gene expression and vanillin biosynthesis. Plant Physiol. Biochem. 74, 304–314 (2014).
pubmed: 24342082 doi: 10.1016/j.plaphy.2013.11.026
Gallage, N. J. et al. Vanillin formation from ferulic acid in Vanilla planifolia is catalysed by a single enzyme. Nat. Commun. 5, 4037 (2014).
pubmed: 24941968 doi: 10.1038/ncomms5037
Odoux, E. & Brillouet, J.-M. Anatomy, histochemistry and biochemistry of glucovanillin, oleoresin and mucilage accumulation sites in green mature vanilla pod (Vanilla planifolia; Orchidaceae): a comprehensive and critical reexamination. Fruits 64, 221–241 (2009).
doi: 10.1051/fruits/2009017
Zhang, M. P. et al. Preparation of megabase-sized DNA from a variety of organisms using the nuclei method for advanced genomics research. Nat. Protoc. 7, 467–478 (2012).
pubmed: 22343429 doi: 10.1038/nprot.2011.455
Datema, E. et al. The megabase-sized fungal genome of Rhizoctonia solani assembled from nanopore reads only. Preprint at bioRxiv https://doi.org/10.1101/084772 (2016).
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Li, H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics 32, 2103–2110 (2016).
pubmed: 27153593 pmcid: 4937194 doi: 10.1093/bioinformatics/btw152
Vaser, R., Sovic, I., Nagarajan, N. & Sikic, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27, 737–746 (2017).
pubmed: 28100585 pmcid: 5411768 doi: 10.1101/gr.214270.116
Lee, Y. G. et al. Constructing a reference genome in a single lab: the possibility to use Oxford nanopore technology. Plants 8, 270 (2019).
pmcid: 6724115 doi: 10.3390/plants8080270
Michael, T. P. et al. High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat. Commun. 9, 541 (2018).
pubmed: 29416032 pmcid: 5803254 doi: 10.1038/s41467-018-03016-2
Giordano, F. et al. De novo yeast genome assemblies from MinION, PacBio and MiSeq platforms. Sci. Rep. 7, 3935 (2017).
pubmed: 28638050 pmcid: 5479803 doi: 10.1038/s41598-017-03996-z
Liao, Y. C. et al. Completing circular bacterial genomes with assembly complexity by using a sampling strategy from a single MinION run with barcoding. Front. Microbiol. 10, 2068 (2019).
pubmed: 31551994 pmcid: 6737777 doi: 10.3389/fmicb.2019.02068
Roach, M. J., Schmidt, S. A. & Borneman, A. R. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics 19, 460 (2018).
pubmed: 30497373 pmcid: 6267036 doi: 10.1186/s12859-018-2485-7
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at http://arxiv.org/abs/1303.3997 (2013).
Faust, G. G. & Hall, I. M. SAMBLASTER: fast duplicate marking and structural variant read extraction. Bioinformatics 30, 2503–2505 (2014).
pubmed: 24812344 pmcid: 4147885 doi: 10.1093/bioinformatics/btu314
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Kronenberg, Z. N. et al. FALCON-Phase: integrating PacBio and Hi-C data for phased diploid genomes. Preprint at BioRxiv https://doi.org/10.1101/327064 (2018).
Ghurye, J., Pop, M., Koren, S., Bickhart, D. & Chin, C. S. Scaffolding of long read assemblies using long range contact information. BMC Genomics 18, 527 (2017).
pubmed: 28701198 pmcid: 5508778 doi: 10.1186/s12864-017-3879-z
Burton, J. N. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119–1125 (2013).
pubmed: 24185095 pmcid: 4117202 doi: 10.1038/nbt.2727
Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3, 99–101 (2016).
pubmed: 27467250 pmcid: 5596920 doi: 10.1016/j.cels.2015.07.012
Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplots: reference-free profiling of polyploid genomes. Preprint at BioRxiv https://doi.org/10.1101/747568 (2019).
Price, A. L., Jones, N. C. & Pevzner, P. A. De novo identification of repeat families in large genomes. Bioinformatics 21, I351–I358 (2005).
pubmed: 15961478 doi: 10.1093/bioinformatics/bti1018
Tarailo-Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics 25, 4.10.1–4.10.14 (2009).
Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19, ii215–ii225 (2003).
pubmed: 14534192 doi: 10.1093/bioinformatics/btg1080
Guigo, R., Knudsen, S., Drake, N. & Smith, T. Prediction of gene structure. J. Mol. Biol. 226, 141–157 (1992).
pubmed: 1619647 doi: 10.1016/0022-2836(92)90130-C
Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
pubmed: 15144565 pmcid: 421630
Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).
pubmed: 15145805 doi: 10.1093/bioinformatics/bth315
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11, 1650–1667 (2016).
pubmed: 27560171 pmcid: 5032908 doi: 10.1038/nprot.2016.095
Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).
pubmed: 31375807 pmcid: 7605509 doi: 10.1038/s41587-019-0201-4
Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666 (2003).
pubmed: 14500829 pmcid: 206470 doi: 10.1093/nar/gkg770
Sato, S. et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635–641 (2012).
doi: 10.1038/nature11119
Osuna-Cruz, C. M. et al. PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Res. 46, D1197–D1201 (2018).
pubmed: 29156057 doi: 10.1093/nar/gkx1119
Frazee, A. C. et al. Ballgown bridges the gap between transcriptome assembly and expression analysis. Nat. Biotechnol. 33, 243–246 (2015).
pubmed: 25748911 pmcid: 4792117 doi: 10.1038/nbt.3172
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
pubmed: 29722887 pmcid: 5967553 doi: 10.1093/molbev/msy096
Whelan, S. & Goldman, N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691–699 (2001).
pubmed: 11319253 doi: 10.1093/oxfordjournals.molbev.a003851
Aronesty, E. ea-utils (fastqmcf) (2011); https://expressionanalysis.github.io/ea-utils/
Kim, D., Landmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142 pmcid: 4655817 doi: 10.1038/nmeth.3317
Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at http://arxiv.org/abs/1207.3907 (2012).
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w
pubmed: 22728672 pmcid: 3679285 doi: 10.4161/fly.19695
Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186 (2012).
pubmed: 22110026 doi: 10.1093/nar/gkr944
Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006).
pubmed: 16845082 pmcid: 1538804 doi: 10.1093/nar/gkl315
Yang, Z. H. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
pubmed: 17483113 doi: 10.1093/molbev/msm088
Dixon, R. A. in Handbook of Vanilla Science and Technology Ch. 24 (Wiley, 2018).

Auteurs

Tomas Hasing (T)

Elo Life Systems, Durham, NC, USA.

Haibao Tang (H)

Center for Genomics and Biotechnology, Fujian Agricultural and Forestry University, Fuzhou, China.

Maria Brym (M)

Tropical Research and Education Center, Horticultural Sciences Department, University of Florida, Homestead, FL, USA.

Fayaz Khazi (F)

Elo Life Systems, Durham, NC, USA.

Tengfang Huang (T)

Elo Life Systems, Durham, NC, USA. thuang@elolife.ag.

Alan H Chambers (AH)

Tropical Research and Education Center, Horticultural Sciences Department, University of Florida, Homestead, FL, USA. ac@ufl.edu.

Classifications MeSH