Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants
Abstract
Plant metabolism underpins many traits of ecological and agronomic importance. Plants produce numerous compounds to cope with their environments but the biosynthetic pathways for most of these compounds have not yet been elucidated. To engineer and improve metabolic traits, we will need comprehensive and accurate knowledge of the organization and regulation of plant metabolism at the genome scale. Here, we present a computational pipeline to identify metabolic enzymes, pathways, and gene clusters from a sequenced genome. Using this pipeline, we generated metabolic pathway databases for 22 species and identified metabolic gene clusters from 18 species. This unified resource can be used to conduct a wide array of comparative studies of plant metabolism. Using the resource, we discovered a widespread occurrence of metabolic gene clusters in plants: 11,969 clusters from 18 species. The prevalence of metabolic gene clusters offers an intriguing possibility of an untapped source for uncovering new metabolite biosynthesis pathways. For example, more than 1,700 clusters contain enzymes that could generate a specialized metabolite scaffold (signature enzymes) and enzymes that modify the scaffold (tailoring enzymes). In four species with sufficient gene expression data, we identified 43 highly coexpressed clusters that contain signature and tailoring enzymes, of which eight weremore »
- Authors:
-
- Carnegie Inst. of Science, Stanford, CA (United States). Plant Biology Dept.
- Univ. of Lyon, Lyon (France). Lab. of Biometry and Evolutionary biology and French National Center for Scientific Research
- Publication Date:
- Research Org.:
- Donald Danforth Plant Science Center, St. Louis, MO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF); National Institutes of Health (NIH), Bethesda, MD (United States); National Commission for Scientific and Technological Research (CONICYT); Swiss National Science Foundation (SNSF); Alexander Humboldt Foundation
- OSTI Identifier:
- 1423882
- Grant/Contract Number:
- SC0008769; IOS-1026003; DBI-0640769; 1U01GM110699-01A1
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant Physiology (Bethesda)
- Additional Journal Information:
- Journal Name: Plant Physiology (Bethesda); Journal Volume: 173; Journal Issue: 4; Journal ID: ISSN 0032-0889
- Publisher:
- American Society of Plant Biologists
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Schläpfer, Pascal, Zhang, Peifen, Wang, Chuan, Kim, Taehyong, Banf, Michael, Chae, Lee, Dreher, Kate, Chavali, Arvind K., Nilo-Poyanco, Ricardo, Bernard, Thomas, Kahn, Daniel, and Rhee, Seung Y. Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants. United States: N. p., 2017.
Web. doi:10.1104/pp.16.01942.
Schläpfer, Pascal, Zhang, Peifen, Wang, Chuan, Kim, Taehyong, Banf, Michael, Chae, Lee, Dreher, Kate, Chavali, Arvind K., Nilo-Poyanco, Ricardo, Bernard, Thomas, Kahn, Daniel, & Rhee, Seung Y. Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants. United States. https://doi.org/10.1104/pp.16.01942
Schläpfer, Pascal, Zhang, Peifen, Wang, Chuan, Kim, Taehyong, Banf, Michael, Chae, Lee, Dreher, Kate, Chavali, Arvind K., Nilo-Poyanco, Ricardo, Bernard, Thomas, Kahn, Daniel, and Rhee, Seung Y. Sat .
"Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants". United States. https://doi.org/10.1104/pp.16.01942. https://www.osti.gov/servlets/purl/1423882.
@article{osti_1423882,
title = {Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants},
author = {Schläpfer, Pascal and Zhang, Peifen and Wang, Chuan and Kim, Taehyong and Banf, Michael and Chae, Lee and Dreher, Kate and Chavali, Arvind K. and Nilo-Poyanco, Ricardo and Bernard, Thomas and Kahn, Daniel and Rhee, Seung Y.},
abstractNote = {Plant metabolism underpins many traits of ecological and agronomic importance. Plants produce numerous compounds to cope with their environments but the biosynthetic pathways for most of these compounds have not yet been elucidated. To engineer and improve metabolic traits, we will need comprehensive and accurate knowledge of the organization and regulation of plant metabolism at the genome scale. Here, we present a computational pipeline to identify metabolic enzymes, pathways, and gene clusters from a sequenced genome. Using this pipeline, we generated metabolic pathway databases for 22 species and identified metabolic gene clusters from 18 species. This unified resource can be used to conduct a wide array of comparative studies of plant metabolism. Using the resource, we discovered a widespread occurrence of metabolic gene clusters in plants: 11,969 clusters from 18 species. The prevalence of metabolic gene clusters offers an intriguing possibility of an untapped source for uncovering new metabolite biosynthesis pathways. For example, more than 1,700 clusters contain enzymes that could generate a specialized metabolite scaffold (signature enzymes) and enzymes that modify the scaffold (tailoring enzymes). In four species with sufficient gene expression data, we identified 43 highly coexpressed clusters that contain signature and tailoring enzymes, of which eight were characterized previously to be functional pathways. Finally, we identified patterns of genome organization that implicate local gene duplication and, to a lesser extent, single gene transposition as having played roles in the evolution of plant metabolic gene clusters.},
doi = {10.1104/pp.16.01942},
journal = {Plant Physiology (Bethesda)},
number = 4,
volume = 173,
place = {United States},
year = {Sat Apr 01 00:00:00 EDT 2017},
month = {Sat Apr 01 00:00:00 EDT 2017}
}
Web of Science
Works referencing / citing this record:
Scalable Biosynthesis of the Seaweed Neurochemical, Kainic Acid
journal, May 2019
- Chekan, Jonathan R.; McKinnie, Shaun M. K.; Moore, Malia L.
- Angewandte Chemie
Challenges and emergent solutions for LC-MS/MS based untargeted metabolomics in diseases
journal, February 2018
- Cui, Liang; Lu, Haitao; Lee, Yie Hou
- Mass Spectrometry Reviews, Vol. 37, Issue 6
Multi-tissue to whole plant metabolic modelling
journal, November 2019
- Shaw, Rahul; Cheung, C. Y. Maurice
- Cellular and Molecular Life Sciences, Vol. 77, Issue 3
Characterization and evolution of gene clusters for terpenoid phytoalexin biosynthesis in tobacco
journal, August 2019
- Chen, Xi; Liu, Fangjie; Liu, Lu
- Planta, Vol. 250, Issue 5
Benzylisoquinoline alkaloid biosynthesis in opium poppy: an update
journal, November 2019
- Singh, Aparna; Menéndez-Perdomo, Ivette M.; Facchini, Peter J.
- Phytochemistry Reviews, Vol. 18, Issue 6
Computational analysis of the productivity potential of CAM
journal, February 2018
- Shameer, Sanu; Baghalian, Kambiz; Cheung, C. Y. Maurice
- Nature Plants, Vol. 4, Issue 3
The birth, evolution and death of metabolic gene clusters in fungi
journal, September 2018
- Rokas, Antonis; Wisecaver, Jennifer H.; Lind, Abigail L.
- Nature Reviews Microbiology, Vol. 16, Issue 12
The Rosa genome provides new insights into the domestication of modern roses
journal, April 2018
- Raymond, Olivier; Gouzy, Jérôme; Just, Jérémy
- Nature Genetics, Vol. 50, Issue 6
Unlocking conserved and diverged metabolic characteristics in cassava carbon assimilation via comparative genomics approach
journal, November 2018
- Siriwat, Wanatsanan; Kalapanulak, Saowalak; Suksangpanomrung, Malinee
- Scientific Reports, Vol. 8, Issue 1
Multigenome analysis implicates miniature inverted-repeat transposable elements (MITEs) in metabolic diversification in eudicots
journal, June 2018
- Boutanaev, Alexander M.; Osbourn, Anne E.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
Robust predictions of specialized metabolism genes through machine learning
journal, January 2019
- Moore, Bethany M.; Wang, Peipei; Fan, Pengxiang
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 6
Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains
journal, July 2019
- Koprivova, Anna; Schuck, Stefan; Jacoby, Richard P.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 31
Exploring plant metabolic genomics: chemical diversity, metabolic complexity in the biosynthesis and transport of specialized metabolites with the tea plant as a model
journal, April 2020
- Zhao, Jian; Li, Penghui; Xia, Tao
- Critical Reviews in Biotechnology, Vol. 40, Issue 5
eCAMI: simultaneous classification and motif identification for enzyme annotation
journal, December 2019
- Xu, Jing; Zhang, Han; Zheng, Jinfang
- Bioinformatics, Vol. 36, Issue 7
Genome sequence of Malania oleifera , a tree with great value for nervonic acid production
journal, January 2019
- Xu, Chao-Qun; Liu, Hui; Zhou, Shan-Shan
- GigaScience, Vol. 8, Issue 2
The PhytoClust tool for metabolic gene clusters discovery in plant genomes
journal, May 2017
- Töpfer, Nadine; Fuchs, Lisa-Maria; Aharoni, Asaph
- Nucleic Acids Research, Vol. 45, Issue 12
The MetaCyc database of metabolic pathways and enzymes
journal, October 2017
- Caspi, Ron; Billington, Richard; Fulcher, Carol A.
- Nucleic Acids Research, Vol. 46, Issue D1
15 years of GDR: New data and functionality in the Genome Database for Rosaceae
journal, October 2018
- Jung, Sook; Lee, Taein; Cheng, Chun-Huai
- Nucleic Acids Research, Vol. 47, Issue D1
The MetaCyc database of metabolic pathways and enzymes - a 2019 update
journal, October 2019
- Caspi, Ron; Billington, Richard; Keseler, Ingrid M.
- Nucleic Acids Research, Vol. 48, Issue D1
Plant Reactome: a knowledgebase and resource for comparative pathway analysis
journal, November 2019
- Naithani, Sushma; Gupta, Parul; Preece, Justin
- Nucleic Acids Research
Robust predictions of specialized metabolism genes through machine learning
posted_content, October 2018
- Moore, Bethany M.; Wang, Peipei; Fan, Pengxiang
- Proceedings of the National Academy of Sciences
QTG-Finder: a machine-learning based algorithm to prioritize causal genes of quantitative trait loci
posted_content, April 2019
- Lin, Fan; Fan, Jue; Rhee, Seung Y.
- G3: Genes|Genomes|Genetics
Epigenomic Landscape of Arabidopsis thaliana Metabolism Reveals Bivalent Chromatin on Specialized Metabolic Genes
posted_content, March 2019
- Zhao, Kangmei; Rhee, Seung Y.
- BioRxiv
Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change In Arabidopsis thaliana
posted_content, October 2019
- Potter, Barney; Song, Michael J.; Doyle, Jeff J.
- The Plant Cell
Epigenetic mapping of the Arabidopsis metabolome reveals mediators of the epigenotype-phenotype map
journal, November 2018
- Kooke, Rik; Morgado, Lionel; Becker, Frank
- Genome Research, Vol. 29, Issue 1
Drivers of metabolic diversification: how dynamic genomic neighbourhoods generate new biosynthetic pathways in the Brassicaceae
journal, December 2019
- Liu, Zhenhua; Suarez Duran, Hernando G.; Harnvanichvech, Yosapol
- New Phytologist, Vol. 227, Issue 4
A Prunus persica genome‐wide RNA‐seq approach uncovers major differences in the transcriptome among chilling injury sensitive and non‐sensitive varieties
journal, October 2018
- Nilo‐Poyanco, Ricardo; Vizoso, Paula; Sanhueza, Dayan
- Physiologia Plantarum, Vol. 166, Issue 3
Diurnal changes in concerted plant protein phosphorylation and acetylation in Arabidopsis organs and seedlings
journal, May 2019
- Uhrig, R. Glen; Schläpfer, Pascal; Roschitzki, Bernd
- The Plant Journal, Vol. 99, Issue 1
Functional analysis tools for post‐translational modification: a post‐translational modification database for analysis of proteins and metabolic pathways
journal, May 2019
- Cruz, Edward R.; Nguyen, Hung; Nguyen, Tin
- The Plant Journal
Deciphering S ‐methylcysteine biosynthesis in common bean by isotopic tracking with mass spectrometry
journal, July 2019
- Joshi, Jaya; Renaud, Justin B.; Sumarah, Mark W.
- The Plant Journal, Vol. 100, Issue 1
The hybrid protein interactome contributes to rice heterosis as epistatic effects
journal, December 2019
- Li, Hong; Jiang, Shuqin; Li, Chen
- The Plant Journal, Vol. 102, Issue 1
Infrastructures of systems biology that facilitate functional genomic study in rice
journal, March 2019
- Hong, Woo-Jong; Kim, Yu-Jin; Chandran, Anil Kumar Nalini
- Rice, Vol. 12, Issue 1
A mass and charge balanced metabolic model of Setaria viridis revealed mechanisms of proton balancing in C4 plants
journal, June 2019
- Shaw, Rahul; Cheung, C. Y. Maurice
- BMC Bioinformatics, Vol. 20, Issue 1
Trait ontology analysis based on association mapping studies bridges the gap between crop genomics and Phenomics
journal, June 2019
- Pan, Qingchun; Wei, Junfeng; Guo, Feng
- BMC Genomics, Vol. 20, Issue 1
Haplotype-resolved genomes of geminivirus-resistant and geminivirus-susceptible African cassava cultivars
journal, September 2019
- Kuon, Joel-E.; Qi, Weihong; Schläpfer, Pascal
- BMC Biology, Vol. 17, Issue 1
A genetical metabolomics approach for bioprospecting plant biosynthetic gene clusters
journal, April 2019
- Witjes, Lotte; Kooke, Rik; van der Hooft, Justin J. J.
- BMC Research Notes, Vol. 12, Issue 1
APETALA2 control of barley internode elongation
journal, May 2019
- Patil, Vrushali; McDermott, Hannah I.; McAllister, Trisha
- Development, Vol. 146, Issue 11
QTG-Finder2: A Generalized Machine-Learning Algorithm for Prioritizing QTL Causal Genes in Plants
journal, May 2020
- Lin, Fan; Lazarus, Elena Z.; Rhee, Seung Y.
- G3: Genes|Genomes|Genetics, Vol. 10, Issue 7
Developmental Plasticity of the Major Alkyl Cannabinoid Chemotypes in a Diverse Cannabis Genetic Resource Collection
journal, October 2018
- Welling, Matthew T.; Liu, Lei; Raymond, Carolyn A.
- Frontiers in Plant Science, Vol. 9
Fruit Salad in the Lab: Comparing Botanical Species to Help Deciphering Fruit Primary Metabolism
journal, July 2019
- Roch, Léa; Dai, Zhanwu; Gomès, Eric
- Frontiers in Plant Science, Vol. 10
Gene Modules Co-regulated with Biosynthetic Gene Clusters for Allelopathy between Rice and Barnyardgrass
journal, August 2019
- Sultana, Most. Humaira; Liu, Fangjie; Alamin, Md.
- International Journal of Molecular Sciences, Vol. 20, Issue 16
Characterization of Plant Volatiles Reveals Distinct Metabolic Profiles and Pathways among 12 Brassicaceae Vegetables
journal, December 2018
- Liu, Yu; Zhang, Hui; Umashankar, Shivshankar
- Metabolites, Vol. 8, Issue 4
Systems Biology and Multi-Omics Integration: Viewpoints from the Metabolomics Research Community
journal, April 2019
- Pinu, Farhana R.; Beale, David J.; Paten, Amy M.
- Metabolites, Vol. 9, Issue 4
Large Scale Proteomic Data and Network-Based Systems Biology Approaches to Explore the Plant World
journal, June 2018
- Di Silvestre, Dario; Bergamaschi, Andrea; Bellini, Edoardo
- Proteomes, Vol. 6, Issue 2
The PhytoClust Tool for Metabolic Gene Clusters Discovery in Plant Genomes
posted_content, October 2016
- Töpfer, Nadine; Fuchs, Lisa-Maria; Aharoni, Asaph
Scalable Biosynthesis of the Seaweed Neurochemical, Kainic Acid
journal, June 2019
- Chekan, Jonathan R.; McKinnie, Shaun M. K.; Moore, Malia L.
- Angewandte Chemie International Edition, Vol. 58, Issue 25
Haplotype-resolved genomes of geminivirus-resistant and geminivirus-susceptible African cassava cultivars
text, January 2019
- Kuon, Joel‑Elias; Qi, Weihong; Schläpfer, Pascal
- ETH Zurich
Unlocking conserved and diverged metabolic characteristics in cassava carbon assimilation via comparative genomics approach
journal, November 2018
- Siriwat, Wanatsanan; Kalapanulak, Saowalak; Suksangpanomrung, Malinee
- Scientific Reports, Vol. 8, Issue 1
Comparative analysis of nucleus-encoded plastid-targeting proteins in Rafflesia cantleyi against photosynthetic and non-photosynthetic representatives reveals orthologous systems with potentially divergent functions
journal, November 2018
- Ng, Siuk-Mun; Lee, Xin-Wei; Mat-Isa, Mohd-Noor
- Scientific Reports, Vol. 8, Issue 1
Correlation-based network analysis combined with machine learning techniques highlight the role of the GABA shunt in Brachypodium sylvaticum freezing tolerance
journal, March 2020
- Toubiana, David; Sade, Nir; Liu, Lifeng
- Scientific Reports, Vol. 10, Issue 1
Inspecting abundantly expressed genes in male strobili in sugi (Cryptomeria japonica D. Don) via a highly accurate cDNA assembly
journal, April 2020
- Wei, Fu-Jin; Ueno, Saneyoshi; Ujino-Ihara, Tokuko
- BioRxiv
Gene Balance Predicts Transcriptional Responses Immediately Following Ploidy Change In Arabidopsis thaliana
posted_content, October 2019
- Potter, Barney; Song, Michael J.; Doyle, Jeff J.
- The Plant Cell
Trait ontology analysis based on association mapping studies bridges the gap between crop genomics and Phenomics
journal, June 2019
- Pan, Qingchun; Wei, Junfeng; Guo, Feng
- BMC Genomics, Vol. 20, Issue 1
A genetical metabolomics approach for bioprospecting plant biosynthetic gene clusters
journal, April 2019
- Witjes, Lotte; Kooke, Rik; van der Hooft, Justin J. J.
- BMC Research Notes, Vol. 12, Issue 1
Transcriptome analysis during ripening of table grape berry cv. Thompson Seedless
journal, January 2018
- Balic, Iván; Vizoso, Paula; Nilo-Poyanco, Ricardo
- PLOS ONE, Vol. 13, Issue 1
QTG-Finder: A Machine-Learning Based Algorithm To Prioritize Causal Genes of Quantitative Trait Loci in Arabidopsis and Rice
journal, July 2019
- Lin, Fan; Fan, Jue; Rhee, Seung Y.
- G3: Genes|Genomes|Genetics, Vol. 9, Issue 10
Multi-Phenotype Association Decomposition: Unraveling Complex Gene-Phenotype Relationships
journal, May 2019
- Weighill, Deborah; Jones, Piet; Bleker, Carissa
- Frontiers in Genetics, Vol. 10
MorphDB: Prioritizing Genes for Specialized Metabolism Pathways and Gene Ontology Categories in Plants
journal, March 2018
- Zwaenepoel, Arthur; Diels, Tim; Amar, David
- Frontiers in Plant Science, Vol. 9
A Dynamic Multi-Tissue Flux Balance Model Captures Carbon and Nitrogen Metabolism and Optimal Resource Partitioning During Arabidopsis Growth
journal, June 2018
- Shaw, Rahul; Cheung, C. Y. Maurice
- Frontiers in Plant Science, Vol. 9
A Bioinformatics Guide to Plant Microbiome Analysis
journal, October 2019
- Lucaciu, Rares; Pelikan, Claus; Gerner, Samuel M.
- Frontiers in Plant Science, Vol. 10
Gene Modules Co-regulated with Biosynthetic Gene Clusters for Allelopathy between Rice and Barnyardgrass
journal, August 2019
- Sultana, Most. Humaira; Liu, Fangjie; Alamin, Md.
- International Journal of Molecular Sciences, Vol. 20, Issue 16
Characterization of Plant Volatiles Reveals Distinct Metabolic Profiles and Pathways among 12 Brassicaceae Vegetables
journal, December 2018
- Liu, Yu; Zhang, Hui; Umashankar, Shivshankar
- Metabolites, Vol. 8, Issue 4
Systems Biology and Multi-Omics Integration: Viewpoints from the Metabolomics Research Community
journal, April 2019
- Pinu, Farhana R.; Beale, David J.; Paten, Amy M.
- Metabolites, Vol. 9, Issue 4
Large Scale Proteomic Data and Network-Based Systems Biology Approaches to Explore the Plant World
journal, June 2018
- Di Silvestre, Dario; Bergamaschi, Andrea; Bellini, Edoardo
- Proteomes, Vol. 6, Issue 2
Haplotype-resolved genomes of geminivirus-resistant and geminivirus-susceptible African cassava cultivars
text, January 2019
- Kuon, Joel‑Elias; Qi, Weihong; Schläpfer, Pascal
- ETH Zurich