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Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus

Chenxin Li, Joshua C. Wood, Anh Hai Vu, John P. Hamilton, Carlos Eduardo Rodriguez Lopez, Richard M. E. Payne, Delia Ayled Serna Guerrero, Kotaro Yamamoto, Brieanne Vaillancourt, Lorenzo Caputi, View ORCID ProfileSarah E. O’Connor, C. Robin Buell
doi: https://doi.org/10.1101/2022.07.04.498697
Chenxin Li
1Center for Applied Genetic Technologies, University of Georgia, Athens GA, 30602 USA
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Joshua C. Wood
1Center for Applied Genetic Technologies, University of Georgia, Athens GA, 30602 USA
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Anh Hai Vu
2Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany
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John P. Hamilton
1Center for Applied Genetic Technologies, University of Georgia, Athens GA, 30602 USA
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Carlos Eduardo Rodriguez Lopez
3Escuela de Ingenieria y Ciencias, Tecnologico de Monterrey, Av. Eugenio Garza Sada 2501, 64849, Monterrey, Mexico
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Richard M. E. Payne
4The John Innes Centre, Department of Biological Chemistry, Norwich Research Park, Norwich, NR4 7UH UK
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Delia Ayled Serna Guerrero
2Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany
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Kotaro Yamamoto
5School of Science, Association of International Arts and Science, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan
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Brieanne Vaillancourt
1Center for Applied Genetic Technologies, University of Georgia, Athens GA, 30602 USA
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Lorenzo Caputi
2Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany
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  • For correspondence: robin.buell@uga.edu
Sarah E. O’Connor
2Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745, Jena, Germany
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  • ORCID record for Sarah E. O’Connor
  • For correspondence: robin.buell@uga.edu
C. Robin Buell
1Center for Applied Genetic Technologies, University of Georgia, Athens GA, 30602 USA
6Department of Crop & Soil Sciences, University of Georgia, Athens GA, 30602 USA
7Institute of Plant Breeding, Genetics & Genomics, University of Georgia, Athens GA, 30602 USA
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  • For correspondence: robin.buell@uga.edu
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ABSTRACT

Advances in omics technologies now permit generation of highly contiguous genome assemblies, detection of transcripts and metabolites at the level of single cells, and high-resolution determination of gene regulatory features including 3-dimensional chromatin interactions. Using a complementary, multi-omics approach, we interrogated the monoterpene indole alkaloid (MIA) biosynthetic pathway in Catharanthus roseus, a source of leading anti-cancer drugs. We identified not only new clusters of genes involved in MIA biosynthesis on the eight C. roseus chromosomes but also rampant gene duplication including paralogs of MIA pathway genes. Clustering was not limited to the linear genome and through chromatin interaction data, MIA pathway genes were shown to be present within the same topologically associated domain, permitting identification of a secologanin transporter. Single cell RNA-sequencing revealed exquisite and sequential cell-type specific partitioning of the leaf MIA biosynthetic pathway that, when coupled with a newly developed single cell metabolomics approach, permitted identification of a reductase that yields the bis-indole alkaloid anhydrovinblastine. Last, we revealed cell-type specific expression in the root MIA pathway that is conferred in part by neo- and sub-functionalization of paralogous MIA pathway genes. This study highlights how a suite of omic approaches, including single cell gene expression and metabolomics, can efficiently link sequence with function in complex, specialized metabolic pathways of plants.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 04, 2022.
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Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus
Chenxin Li, Joshua C. Wood, Anh Hai Vu, John P. Hamilton, Carlos Eduardo Rodriguez Lopez, Richard M. E. Payne, Delia Ayled Serna Guerrero, Kotaro Yamamoto, Brieanne Vaillancourt, Lorenzo Caputi, Sarah E. O’Connor, C. Robin Buell
bioRxiv 2022.07.04.498697; doi: https://doi.org/10.1101/2022.07.04.498697
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Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus
Chenxin Li, Joshua C. Wood, Anh Hai Vu, John P. Hamilton, Carlos Eduardo Rodriguez Lopez, Richard M. E. Payne, Delia Ayled Serna Guerrero, Kotaro Yamamoto, Brieanne Vaillancourt, Lorenzo Caputi, Sarah E. O’Connor, C. Robin Buell
bioRxiv 2022.07.04.498697; doi: https://doi.org/10.1101/2022.07.04.498697

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