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Title: Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids

Journal Article · · New Phytologist
DOI: https://doi.org/10.1111/nph.14852 · OSTI ID:1412668
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  1. Shandong Univ., Jinan (China). Key Lab. of Chemical Biology of Natural Products, Ministry of Education, School of Pharmaceutical Sciences
  2. Brookhaven National Lab. (BNL), Upton, NY (United States). Biology Dept.

Summary Flavonoids ubiquitously distribute to the terrestrial plants and chalcone isomerase ( CHI )‐catalyzed intramolecular and stereospecific cyclization of chalcones is a committed step in the production of flavonoids. However, so far the bona fide CHI s are found only in vascular plants, and their origin and evolution remains elusive. We conducted transcriptomic and/or genomic sequence search, subsequent phylogenetic analysis, and detailed biochemical and genetic characterization to explore the potential existence of CHI proteins in the basal bryophyte liverwort species and the lycophyte Selaginella moellendorffii . We found that both liverwort and Selaginella species possess canonical CHI ‐fold proteins that cluster with their corresponding higher plant counterparts. Among them, some members exhibited bona fide CHI activity, which catalyze stereospecific cyclization of both 6′‐hydroxychalcone and 6′‐deoxychalcone, yielding corresponding 5‐hydroxy and 5‐deoxyflavanones, resembling the typical type II CHI s currently known to be ‘specific’ for legume plants. Expressing those primitive bona fide CHI s in the Arabidopsis chi mutant restores the seed coat transparent testa phenotype and the accumulation of flavonoids. These findings, in contrast to our current understanding of the evolution of enzymatic CHI s, suggest that emergence of the bona fide type II CHI s is an ancient evolution event that occurred before the divergence of liverwort lineages.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0012704; DE‐SC0012704; MCB-1051675
OSTI ID:
1412668
Alternate ID(s):
OSTI ID: 1405542
Report Number(s):
BNL-114460-2017-JA
Journal Information:
New Phytologist, Vol. 217, Issue 2; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (54)

Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells journal January 2008
Molecular cloning and function assay of a chalcone isomerase gene (GbCHI) from Ginkgo biloba journal November 2010
Isolation and characterization of a maize gene encoding chalcone flavonone isomerase journal January 1994
The origin and evolution of lignin biosynthesis: Tansley review journal June 2010
Secondary metabolites from Marchantia paleacea calluses and their allelopathic effects on Arabidopsis seed growth journal February 2013
Chalcone isomerase family and fold: No longer unique to plants journal February 2004
The flavonoid biosynthetic pathway in plants: Function and evolution journal February 1994
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling journal November 2005
Lineage-specific loss and divergence of functionally linked genes in eukaryotes journal October 2000
Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors journal October 2008
Hepatoprotective and free radical scavenging activities of phenolic petrosins and flavonoids isolated from Equisetum arvense journal December 2004
Convergent Evolution of Syringyl Lignin Biosynthesis via Distinct Pathways in the Lycophyte Selaginella and Flowering Plants journal April 2010
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 journal April 2007
Cloning of Chalcone–Flavanone Isomerase cDNA fromPueraria lobataand Its Overexpression inEscherichia coli journal September 1996
A Cluster of Genes Encodes the Two Types of Chalcone Isomerase Involved in the Biosynthesis of General Flavonoids and Legume-Specific 5-Deoxy(iso)flavonoids in Lotus japonicus journal January 2003
Significance of flavonoids in plant resistance: a review journal July 2006
Flavonoids: a colorful model for the regulation and evolution of biochemical pathways journal May 2005
Water-Soluble Constituents from the LiverwortMarchantia polymorpha journal November 2007
A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta journal September 2003
A Rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants journal November 2008
Cloning of the two chalcone flavanone isomerase genes from Petunia hybrida: coordinate, light-regulated and differential expression of flavonoid genes. journal May 1988
A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation journal March 2014
Soybean chalcone isomerase: evolution of the fold, and the differential expression and localization of the gene family journal November 2014
Chemodiversity in Selaginella: a reference system for parallel and convergent metabolic evolution in terrestrial plants journal January 2013
Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis journal May 2012
Cloning of a cDNA encoding the Saussurea medusa chalcone isomerase and its expression in transgenic tobacco journal July 2006
Arabidopsis Kelch Repeat F-Box Proteins Regulate Phenylpropanoid Biosynthesis via Controlling the Turnover of Phenylalanine Ammonia-Lyase journal December 2013
Comparative biochemistry of chalcone isomerases journal January 1988
Sequence analysis of a chalcone isomerase cDNA of Phaseolus vulgaris L. journal January 1991
Partial Reconstruction of Flavonoid and Isoflavonoid Biosynthesis in Yeast Using Soybean Type I and Type II Chalcone Isomerases journal March 2005
Nuclear Localization of Flavonoid Enzymes in Arabidopsis journal April 2005
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal December 1998
Liver and colon DNA oxidative damage and gene expression profiles of rats fed Arabidopsis thaliana mutant seeds containing contrasted flavonoids journal April 2008
Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants journal November 2006
The Genetics and Biochemistry of Floral Pigments journal June 2006
Genome-wide analysis of the chalcone synthase superfamily genes of Physcomitrella patens journal October 2009
Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.) journal March 1994
Progress in the Chemistry of Organic Natural Products book January 1995
Characterization of tt15 , a novel transparent testa mutant of Arabidopsis thaliana (L.) Heynh. journal May 1999
Genetic control of chalcone isomerase activity in flowers of Dianthus caryophyllus journal June 1980
Distribution of flavonoids in the lower plants and its evolutionary significance book January 1988
Independent origins of syringyl lignin in vascular plants journal May 2008
Multiple functional roles of flavonoids in photoprotection: Letters journal May 2010
Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis journal October 2002
Transition state stabilization by general acid catalysis, water expulsion, and enzyme reorganization in Medicago savita chalcone isomerase journal February 2004
Flavonoid Biosynthesis. A Colorful Model for Genetics, Biochemistry, Cell Biology, and Biotechnology journal June 2001
Chemical Constituents of the Bryophytes book January 1995
Purification and characterization of chalcone isomerase from soybeans. journal July 1988
Potential application in amoxicillin removal of Alcaligenes sp. MMA and enzymatic studies through molecular docking journal March 2020
Progress in the chemistry of organic natural products journal January 1983
Biological and molecular interplay between two viruses and powdery and downy mildews in two grapevine cultivars journal November 2020
Progress in the Chemistry of Organic Natural Products. journal March 1956
Progress in the Chemistry of Organic Natural Products journal January 1977
Progress in the Chemistry of Organic Natural Products. journal July 1960

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