Genome and transcriptome of Papaver somniferum Chinese landrace CHM indicates that massive genome expansion contributes to high benzylisoquinoline alkaloid biosynthesis

Li Pei , Baishi Wang , Jian Ye , Xiaodi Hu , Lihong Fu , Kui Li , Zhiyu Ni , Zhenlong Wang , Yujie Wei , Luye Shi , Ying Zhang , Xue Bai , Mengwan Jiang , Shuhui Wang , Chunling Ma , Shujin Li , Kaihui Liu , Wanshui Li , Bin Cong

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 5

PDF (3766KB)
Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :5 DOI: 10.1038/s41438-020-00435-5
Article
research-article
Genome and transcriptome of Papaver somniferum Chinese landrace CHM indicates that massive genome expansion contributes to high benzylisoquinoline alkaloid biosynthesis
Author information +
History +
PDF (3766KB)

Abstract

Opium poppy (Papaver somniferum) is a source of morphine, codeine, and semisynthetic derivatives, including oxycodone and naltrexone. Here, we report the de novo assembly and genomic analysis of P. somniferum traditional landrace ‘Chinese Herbal Medicine’. Variations between the 2.62 Gb CHM genome and that of the previously sequenced high noscapine 1 (HN1) variety were also explored. Among 79,668 protein-coding genes, we functionally annotated 88.9%, compared to 68.8% reported in the HN1 genome. Gene family and 4DTv comparative analyses with three other Papaveraceae species revealed that opium poppy underwent two whole-genome duplication (WGD) events. The first of these, in ancestral Ranunculales, expanded gene families related to characteristic secondary metabolite production and disease resistance. The more recent species-specific WGD mediated by transposable elements resulted in massive genome expansion. Genes carrying structural variations and large-effect variants associated with agronomically different phenotypes between CHM and HN1 that were identified through our transcriptomic comparison of multiple organs and developmental stages can enable the development of new varieties. These genomic and transcriptomic analyses will provide a valuable resource that informs future basic and agricultural studies of the opium poppy.

Cite this article

Download citation ▾
Li Pei, Baishi Wang, Jian Ye, Xiaodi Hu, Lihong Fu, Kui Li, Zhiyu Ni, Zhenlong Wang, Yujie Wei, Luye Shi, Ying Zhang, Xue Bai, Mengwan Jiang, Shuhui Wang, Chunling Ma, Shujin Li, Kaihui Liu, Wanshui Li, Bin Cong. Genome and transcriptome of Papaver somniferum Chinese landrace CHM indicates that massive genome expansion contributes to high benzylisoquinoline alkaloid biosynthesis. Horticulture Research, 2021, 8 (1) : 5 DOI:10.1038/s41438-020-00435-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Jacomet, S. Plant economy and village life in Neolithic lake dwellings at the time of the Alpine Iceman. Veg. Hist. Archaeobot. 18, 47-59 (2009).

[2]

Chaturvedi, N., Singh, M., Shukla, A. K. et al. Comparative analysis of Papaver somniferum genotypes having contrasting latex and alkaloid profiles. Protoplasma 251, 857-867 (2014).

[3]

Facchini, P. J. & De Luca, V. Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant J. 54, 763-784 (2008).

[4]

Knaul, F. M. et al. Alleviating the access abyss in palliative care and pain relief-an imperative of universal health coverage: the Lancet Commission report. Lancet 391, 1391-1454 (2017).

[5]

Beaudoin, G. A. W. & Facchini, P. J. Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240, 19-32 (2014).

[6]

Nakagawa, A. et al. Total biosynthesis of opiates by stepwise fermentation using engineered Escherichia coli. Nat. Commun. 7, 10390 (2016).

[7]

Celik, I. et al. Molecular genetic diversity and association mapping of morphine content and agronomic traits in Turkish opium poppy (Papaver somniferum) germplasm. Mol. Breed. 36, 1-13 (2016).

[8]

Verma, N., Jena, S. N., Shukla, S. & Yadav, K. Genetic diversity, population structure and marker trait associations for alkaloid content and licit opium yield in India-wide collection of poppy (Papaver somniferum L.). Plant Gene 7, 26-41 (2016).

[9]

Liu, X. et al. The genome of medicinal plant Macleaya cordata provides new insights into benzylisoquinoline alkaloids metabolism. Mol. Plant 10, 975-989 (2017).

[10]

Hori, K. et al. Mining of the uncharacterized cytochrome P450 genes involved in alkaloid biosynthesis in California poppy using a draft genome sequence. Plant Cell Physiol. 59, 222-233 (2018).

[11]

Guo, L. et al. The opium poppy genome and morphinan production. Science 362, 343-347 (2018).

[12]

Li, Y. et al. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat. Biotechnol. 32, 1045-1052 (2014).

[13]

Kajitani, R. et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 24, 1384-1395 (2014).

[14]

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

[15]

Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061-1067 (2007).

[16]

Sanmiguel, P. & Bennetzen, J. L. Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann. Bot. 82, 37-44 (1998).

[17]

Devos, K. M., Brown, J. K. M. & Bennetzen, J. L. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12, 1075-1079 (2002).

[18]

Ma, J. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14, 860-869 (2004).

[19]

Xu, Y. X. Young but not relatively old retrotransposons are preferentially located in gene-rich euchromatic regions in tomato (Solanum lycopersicum) plants. Plant J. 80, 582-591 (2014).

[20]

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

[21]

Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. Cabios 13, 555 (1997).

[22]

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

[23]

Martin, J. et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat. Genet. 43, 228-235 (2011).

[24]

Denoeud, F. et al. The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345, 1181-1184 (2014).

[25]

Luca, V. D. & Pierre, B. S. The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci. 5, 168-173 (2000).

[26]

Facchini, P. J. & Luca, V. D. Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant J. 54, 763-784 (2010).

[27]

Paterson, A. H. et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423-427 (2012).

[28]

Morris, J. S. et al. Plug-and-play benzylisoquinoline alkaloid biosynthetic gene discovery in engineered yeast. Methods Enzymol. 575, 143-178 (2016).

[29]

Ma, C. & Wang, X . Application of the Gini correlation coefficient to infer regulatory relationships in transcriptome analysis. Plant Physiol. 160, 192-203 (2012).

[30]

Facchini, P. J. et al. Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol. 112, 1669-1677 (1996).

[31]

Mortazavi, A. et al. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).

[32]

Facchini, P. J., Loukanina, N. & Blanche, V. Genetic transformation via somatic embryogenesis to establish herbicide-resistant opium poppy. Plant Cell Rep. 27, 719-727 (2008).

[33]

Bennetzen, J. L. Patterns in grass genome evolution. Curr. Opin. Plant Biol. 10, 176-181 (2007).

[34]

Kim, S. et al. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46, 270-278 (2014).

[35]

Bennett, M. D. Perspectives on polyploidy in plants - ancient and neo. Biol. J. Linn. Soc. 82, 411-423 (2004).

[36]

Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (2007).

[37]

Onoyovwe, A. et al. Morphine biosynthesis in opium poppy involves two cell types: sieve elements and laticifers. Plant Cell 25, 4110-4122 (2013).

[38]

Porebski, S., Bailey, L. G. & Baum, B. R. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol. Biol. Rep. 15, 8-15 (1997).

[39]

Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265-W268 (2007).

[40]

Altschul, S. F. et al. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).

[41]

Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).

[42]

Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).

[43]

Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 9, 1-22 (2008).

[44]

Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).

[45]

Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).

[46]

De Bie, T. et al. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269-1271 (2006).

[47]

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

[48]

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).

[49]

Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).

[50]

Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).

PDF (3766KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/