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Title: Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity

Abstract

Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]
  1. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
  2. Department of Plant Biology, Michigan State University, East Lansing, United States
  3. Department of Plant Biology, Michigan State University, East Lansing, United States, University of Wisconsin, Madison, United States
  4. Division of Biological Sciences, University of Missouri, Columbus, United States
  5. Department of Plant Biology, Michigan State University, East Lansing, United States, MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United States
  6. Department of Plant Biology, Michigan State University, East Lansing, United States, Department of Computational Mathematics, Science, and Engineering, Michigan State University, East Lansing, United States
  7. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States, Department of Plant Biology, Michigan State University, East Lansing, United States
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1635731
Alternate Identifier(s):
OSTI ID: 1635732; OSTI ID: 1803407
Grant/Contract Number:  
SC0018409
Resource Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 9; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biochemistry and chemical biology; plant biology; Solanum lycopersicum; Solanum quitoense; Solanum pennellii

Citation Formats

Fan, Pengxiang, Wang, Peipei, Lou, Yann-Ru, Leong, Bryan J., Moore, Bethany M., Schenck, Craig A., Combs, Rachel, Cao, Pengfei, Brandizzi, Federica, Shiu, Shin-Han, and Last, Robert L. Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity. United States: N. p., 2020. Web. doi:10.7554/eLife.56717.
Fan, Pengxiang, Wang, Peipei, Lou, Yann-Ru, Leong, Bryan J., Moore, Bethany M., Schenck, Craig A., Combs, Rachel, Cao, Pengfei, Brandizzi, Federica, Shiu, Shin-Han, & Last, Robert L. Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity. United States. https://doi.org/10.7554/eLife.56717
Fan, Pengxiang, Wang, Peipei, Lou, Yann-Ru, Leong, Bryan J., Moore, Bethany M., Schenck, Craig A., Combs, Rachel, Cao, Pengfei, Brandizzi, Federica, Shiu, Shin-Han, and Last, Robert L. Thu . "Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity". United States. https://doi.org/10.7554/eLife.56717.
@article{osti_1635731,
title = {Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity},
author = {Fan, Pengxiang and Wang, Peipei and Lou, Yann-Ru and Leong, Bryan J. and Moore, Bethany M. and Schenck, Craig A. and Combs, Rachel and Cao, Pengfei and Brandizzi, Federica and Shiu, Shin-Han and Last, Robert L.},
abstractNote = {Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity.},
doi = {10.7554/eLife.56717},
journal = {eLife},
number = ,
volume = 9,
place = {United States},
year = {Thu Jul 02 00:00:00 EDT 2020},
month = {Thu Jul 02 00:00:00 EDT 2020}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.7554/eLife.56717

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Cited by: 37 works
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Works referenced in this record:

Candidate Gene Networks for Acylsugar Metabolism and Plant Defense in Wild Tomato Solanum pennellii
journal, October 2019

  • Mandal, Sabyasachi; Ji, Wangming; McKnight, Thomas D.
  • The Plant Cell, Vol. 32, Issue 1
  • DOI: 10.1105/tpc.19.00552

Gene clustering in plant specialized metabolism
journal, April 2014


Acyltransferases in plants: a good time to be BAHD
journal, June 2006


A Papaver somniferum 10-Gene Cluster for Synthesis of the Anticancer Alkaloid Noscapine
journal, May 2012


The Cer-cqu gene cluster determines three key players in a β-diketone synthase polyketide pathway synthesizing aliphatics in epicuticular waxes
journal, March 2016

  • Schneider, Lizette M.; Adamski, Nikolai M.; Christensen, Caspar Elo
  • Journal of Experimental Botany, Vol. 67, Issue 9
  • DOI: 10.1093/jxb/erw105

The genome of the stress-tolerant wild tomato species Solanum pennellii
journal, September 2014

  • Bolger, Anthony; Scossa, Federico; Bolger, Marie E.
  • Nature Genetics, Vol. 46, Issue 9
  • DOI: 10.1038/ng.3046

Doing the gene shuffle to close synteny: dynamic assembly of biosynthetic gene clusters
journal, May 2020


Solanum pennellii backcross inbred lines (BILs) link small genomic bins with tomato traits
journal, July 2016

  • Ofner, Itai; Lashbrooke, Justin; Pleban, Tzili
  • The Plant Journal, Vol. 87, Issue 2
  • DOI: 10.1111/tpj.13194

Investigation of terpene diversification across multiple sequenced plant genomes
journal, December 2014

  • Boutanaev, Alexander M.; Moses, Tessa; Zi, Jiachen
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419547112

Achieving Diversity in the Face of Constraints: Lessons from Metabolism
journal, June 2012


A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants
journal, April 2017

  • Wisecaver, Jennifer H.; Borowsky, Alexander T.; Tzin, Vered
  • The Plant Cell, Vol. 29, Issue 5
  • DOI: 10.1105/tpc.17.00009

Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010

  • Trapnell, Cole; Williams, Brian A.; Pertea, Geo
  • Nature Biotechnology, Vol. 28, Issue 5
  • DOI: 10.1038/nbt.1621

Evolution of metabolic novelty: A trichome-expressed invertase creates specialized metabolic diversity in wild tomato
journal, April 2019

  • Leong, Bryan J.; Lybrand, Daniel B.; Lou, Yann-Ru
  • Science Advances, Vol. 5, Issue 4
  • DOI: 10.1126/sciadv.aaw3754

Promiscuity, impersonation and accommodation: evolution of plant specialized metabolism
journal, December 2017


Genomic Signatures of Specialized Metabolism in Plants
journal, May 2014


Analysis of a Chemical Plant Defense Mechanism in Grasses
journal, August 1997


Rice Contains Two Disparate ent -Copalyl Diphosphate Synthases with Distinct Metabolic Functions
journal, November 2004

  • Prisic, Sladjana; Xu, Meimei; Wilderman, P. Ross
  • Plant Physiology, Vol. 136, Issue 4
  • DOI: 10.1104/pp.104.050567

Specialized Metabolism in a Nonmodel Nightshade: Trichome Acylinositol Biosynthesis
journal, April 2020

  • Leong, Bryan J.; Hurney, Steven M.; Fiesel, Paul D.
  • Plant Physiology, Vol. 183, Issue 3
  • DOI: 10.1104/pp.20.00276

TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


A Pathogen-Responsive Gene Cluster for Highly Modified Fatty Acids in Tomato
journal, January 2020


An Effective Strategy for Exploring Unknown Metabolic Pathways by Genome Mining
journal, April 2013

  • Castillo, Dorianne A.; Kolesnikova, Mariya D.; Matsuda, Seiichi P. T.
  • Journal of the American Chemical Society, Vol. 135, Issue 15
  • DOI: 10.1021/ja401535g

Biosynthesis of Antinutritional Alkaloids in Solanaceous Crops Is Mediated by Clustered Genes
journal, June 2013


<em>Arabidopsis thaliana</em> Polar Glycerolipid Profiling by Thin Layer Chromatography (TLC) Coupled with Gas-Liquid Chromatography (GLC)
journal, January 2011

  • Wang, Zhen; Benning, Christoph
  • Journal of Visualized Experiments, Issue 49
  • DOI: 10.3791/2518

Convergent Evolution in Plant Specialized Metabolism
journal, June 2011


In vitro reconstruction and analysis of evolutionary variation of the tomato acylsucrose metabolic network
journal, December 2015

  • Fan, Pengxiang; Miller, Abigail M.; Schilmiller, Anthony L.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 2
  • DOI: 10.1073/pnas.1517930113

Genome-Wide Prediction of Metabolic Enzymes, Pathways, and Gene Clusters in Plants
journal, February 2017

  • Schläpfer, Pascal; Zhang, Peifen; Wang, Chuan
  • Plant Physiology, Vol. 173, Issue 4
  • DOI: 10.1104/pp.16.01942

Factors Influencing Gene Family Size Variation Among Related Species in a Plant Family, Solanaceae
journal, September 2018

  • Wang, Peipei; Moore, Bethany M.; Panchy, Nicholas L.
  • Genome Biology and Evolution, Vol. 10, Issue 10
  • DOI: 10.1093/gbe/evy193

Plant Defense Against Herbivores: Chemical Aspects
journal, June 2012


MAKER-P: A Tool Kit for the Rapid Creation, Management, and Quality Control of Plant Genome Annotations
journal, December 2013

  • Campbell, Michael S.; Law, MeiYee; Holt, Carson
  • Plant Physiology, Vol. 164, Issue 2
  • DOI: 10.1104/pp.113.230144

V ARIATIONS IN THE B IOSYNTHESIS OF S EED -S TORAGE L IPIDS
journal, June 2001


The evolutionary paths towards complexity: a metabolic perspective
journal, July 2013


Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes
journal, September 2012

  • Schilmiller, A. L.; Charbonneau, A. L.; Last, R. L.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
  • DOI: 10.1073/pnas.1207906109

Functionally Divergent Alleles and Duplicated Loci Encoding an Acyltransferase Contribute to Acylsugar Metabolite Diversity in Solanum Trichomes
journal, April 2015

  • Schilmiller, Anthony L.; Moghe, Gaurav D.; Fan, Pengxiang
  • The Plant Cell, Vol. 27, Issue 4
  • DOI: 10.1105/tpc.15.00087

pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants
journal, September 2009


Location, location! cellular relocalization primes specialized metabolic diversification
journal, November 2019


Peroxisome targeting signal 1: Is it really a simple tripeptide?
journal, December 2006

  • Brocard, Cécile; Hartig, Andreas
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 12
  • DOI: 10.1016/j.bbamcr.2006.08.022

Metabolite–Enzyme Coevolution: From Single Enzymes to Metabolic Pathways and Networks
journal, June 2018


Profiling, isolation and structure elucidation of specialized acylsucrose metabolites accumulating in trichomes of Petunia species
journal, June 2017


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


A feedback insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato
journal, May 2015


Recent Segmental Duplications in the Human Genome
journal, August 2002


Evolution of gene duplication in plants
journal, June 2016

  • Panchy, Nicholas; Lehti-Shiu, Melissa D.; Shiu, Shin-Han
  • Plant Physiology
  • DOI: 10.1104/pp.16.00523

Evolutionary and Expression Signatures of Pseudogenes in Arabidopsis and Rice
journal, July 2009

  • Zou, Cheng; Lehti-Shiu, Melissa D.; Thibaud-Nissen, Françoise
  • Plant Physiology, Vol. 151, Issue 1
  • DOI: 10.1104/pp.109.140632

All fatty acids are not equal: discrimination in plant membrane lipids
journal, March 2000


Characterization of Trichome-Expressed BAHD Acyltransferases in Petunia axillaris Reveals Distinct Acylsugar Assembly Mechanisms within the Solanaceae
journal, July 2017

  • Nadakuduti, Satya Swathi; Uebler, Joseph B.; Liu, Xiaoxiao
  • Plant Physiology, Vol. 175, Issue 1
  • DOI: 10.1104/pp.17.00538

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
  • DOI: 10.1111/nph.16338

HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014


Production of high levels of 8:0 and 10:0 fatty acids in transgenic canola by overexpression of Ch FatB2, a thioesterase cDNA from Cuphea hookeriana
journal, February 1996


Plant metabolic clusters – from genetics to genomics
journal, April 2016

  • Nützmann, Hans‐Wilhelm; Huang, Ancheng; Osbourn, Anne
  • New Phytologist, Vol. 211, Issue 3
  • DOI: 10.1111/nph.13981

Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation
journal, January 2012

  • McCarthy, Davis J.; Chen, Yunshun; Smyth, Gordon K.
  • Nucleic Acids Research, Vol. 40, Issue 10
  • DOI: 10.1093/nar/gks042

A Specialized Diacylglycerol Acyltransferase Contributes to the Extreme Medium-Chain Fatty Acid Content of Cuphea Seed Oil
journal, March 2017

  • Iskandarov, Umidjon; Silva, Jillian E.; Kim, Hae Jin
  • Plant Physiology, Vol. 174, Issue 1
  • DOI: 10.1104/pp.16.01894

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores
journal, April 2016


A different function for a member of an ancient and highly conserved cytochrome P450 family: From essential sterols to plant defense
journal, November 2006

  • Qi, X.; Bakht, S.; Qin, B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 49
  • DOI: 10.1073/pnas.0607849103

MCScanX-transposed: detecting transposed gene duplications based on multiple colinearity scans
journal, March 2013


Glandular trichomes: micro‐organs with model status?
journal, December 2019

  • Schuurink, Robert; Tissier, Alain
  • New Phytologist, Vol. 225, Issue 6
  • DOI: 10.1111/nph.16283

Within- and cross-species predictions of plant specialized metabolism genes using transfer learning
journal, January 2020


Prototype of an intertwined secondary-metabolite supercluster
journal, September 2013

  • Wiemann, P.; Guo, C. -J.; Palmer, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 42
  • DOI: 10.1073/pnas.1313258110

KAS IV: a 3‐ketoacyl‐ACP synthase from Cuphea sp . is a medium chain specific condensing enzyme
journal, August 1998


The Rise of Chemodiversity in Plants
journal, June 2012


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants
journal, November 2000


Tip of the trichome: evolution of acylsugar metabolic diversity in Solanaceae
journal, June 2019


A gene cluster for secondary metabolism in oat: Implications for the evolution of metabolic diversity in plants
journal, May 2004

  • Qi, X.; Bakht, S.; Leggett, M.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 21
  • DOI: 10.1073/pnas.0401301101

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
  • DOI: 10.1038/s41579-018-0075-3

To Gibberellins and Beyond! Surveying the Evolution of (Di)Terpenoid Metabolism
journal, April 2014


PlantFAdb: a resource for exploring hundreds of plant fatty acid structures synthesized by thousands of plants and their phylogenetic relationships
journal, November 2018

  • Ohlrogge, John; Thrower, Nick; Mhaske, Vandana
  • The Plant Journal, Vol. 96, Issue 6
  • DOI: 10.1111/tpj.14102

A New Type of Peroxisomal Acyl-Coenzyme A Synthetase from Arabidopsis thaliana Has the Catalytic Capacity to Activate Biosynthetic Precursors of Jasmonic Acid
journal, January 2005

  • Schneider, Katja; Kienow, Lucie; Schmelzer, Elmon
  • Journal of Biological Chemistry, Vol. 280, Issue 14
  • DOI: 10.1074/jbc.M413578200

Evolutionary Diversification of Primary Metabolism and Its Contribution to Plant Chemical Diversity
journal, July 2019


Enzyme Promiscuity: A Mechanistic and Evolutionary Perspective
journal, June 2010


Myo -inositol-Derived Glycolipids with Anti-inflammatory Activity from Solanum l anceolatum
journal, July 2005

  • Herrera-Salgado, Yesenia; Garduño-Ramírez, María Luisa; Vázquez, Lorena
  • Journal of Natural Products, Vol. 68, Issue 7
  • DOI: 10.1021/np050054s

A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree
journal, January 2013

  • Särkinen, Tiina; Bohs, Lynn; Olmstead, Richard G.
  • BMC Evolutionary Biology, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2148-13-214