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

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 clusteri...

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Main Authors: Pengxiang Fan, Peipei Wang, Yann-Ru Lou, Bryan J Leong, Bethany M Moore, Craig A Schenck, Rachel Combs, Pengfei Cao, Federica Brandizzi, Shin-Han Shiu, Robert L Last
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/56717
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spelling doaj-a7299643ef7245ae905dcbff91e684092021-05-05T21:16:47ZengeLife Sciences Publications LtdeLife2050-084X2020-07-01910.7554/eLife.56717Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversityPengxiang Fan0https://orcid.org/0000-0002-4560-3783Peipei Wang1https://orcid.org/0000-0002-7580-9627Yann-Ru Lou2https://orcid.org/0000-0002-4716-4323Bryan J Leong3https://orcid.org/0000-0003-4042-1160Bethany M Moore4https://orcid.org/0000-0002-2104-7292Craig A Schenck5https://orcid.org/0000-0002-5711-7213Rachel Combs6https://orcid.org/0000-0001-6626-0903Pengfei Cao7https://orcid.org/0000-0001-6998-9302Federica Brandizzi8https://orcid.org/0000-0003-0580-8888Shin-Han Shiu9https://orcid.org/0000-0001-6470-235XRobert L Last10https://orcid.org/0000-0001-6974-9587Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United StatesDepartment of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United States; University of Wisconsin, Madison, United StatesDepartment of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United StatesDivision of Biological Sciences, University of Missouri, Columbus, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United States; MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United States; MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United States; Department of Computational Mathematics, Science, and Engineering, Michigan State University, East Lansing, United StatesDepartment of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States; Department of Plant Biology, Michigan State University, East Lansing, United StatesPlants 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.https://elifesciences.org/articles/56717Solanum lycopersicumSolanum quitoenseSolanum pennellii
collection DOAJ
language English
format Article
sources DOAJ
author Pengxiang Fan
Peipei Wang
Yann-Ru Lou
Bryan J Leong
Bethany M Moore
Craig A Schenck
Rachel Combs
Pengfei Cao
Federica Brandizzi
Shin-Han Shiu
Robert L Last
spellingShingle Pengxiang Fan
Peipei Wang
Yann-Ru Lou
Bryan J Leong
Bethany M Moore
Craig A Schenck
Rachel Combs
Pengfei Cao
Federica Brandizzi
Shin-Han Shiu
Robert L Last
Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
eLife
Solanum lycopersicum
Solanum quitoense
Solanum pennellii
author_facet Pengxiang Fan
Peipei Wang
Yann-Ru Lou
Bryan J Leong
Bethany M Moore
Craig A Schenck
Rachel Combs
Pengfei Cao
Federica Brandizzi
Shin-Han Shiu
Robert L Last
author_sort Pengxiang Fan
title Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
title_short Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
title_full Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
title_fullStr Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
title_full_unstemmed Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity
title_sort evolution of a plant gene cluster in solanaceae and emergence of metabolic diversity
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-07-01
description 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.
topic Solanum lycopersicum
Solanum quitoense
Solanum pennellii
url https://elifesciences.org/articles/56717
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