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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

Abstract

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 eventmore » that occurred before the divergence of liverwort lineages.« less

Authors:
 [1];  [2];  [1];  [1];  [1]; ORCiD logo [2];  [1]
  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.
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1412668
Alternate Identifier(s):
OSTI ID: 1405542
Report Number(s):
BNL-114460-2017-JA
Journal ID: ISSN 0028-646X
Grant/Contract Number:  
SC0012704; DE‐SC0012704; MCB-1051675
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 217; Journal Issue: 2; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Flavonoids; Chalcone isomerase; Evolution; Liverwort; Selaginella moellendorffii (Spikemoss)

Citation Formats

Cheng, Ai-Xia, Zhang, Xuebin, Han, Xiao-Juan, Zhang, Yu-Ying, Gao, Shuai, Liu, Chang-Jun, and Lou, Hong-Xiang. Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids. United States: N. p., 2017. Web. doi:10.1111/nph.14852.
Cheng, Ai-Xia, Zhang, Xuebin, Han, Xiao-Juan, Zhang, Yu-Ying, Gao, Shuai, Liu, Chang-Jun, & Lou, Hong-Xiang. Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids. United States. https://doi.org/10.1111/nph.14852
Cheng, Ai-Xia, Zhang, Xuebin, Han, Xiao-Juan, Zhang, Yu-Ying, Gao, Shuai, Liu, Chang-Jun, and Lou, Hong-Xiang. Mon . "Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids". United States. https://doi.org/10.1111/nph.14852. https://www.osti.gov/servlets/purl/1412668.
@article{osti_1412668,
title = {Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids},
author = {Cheng, Ai-Xia and Zhang, Xuebin and Han, Xiao-Juan and Zhang, Yu-Ying and Gao, Shuai and Liu, Chang-Jun and Lou, Hong-Xiang},
abstractNote = {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.},
doi = {10.1111/nph.14852},
journal = {New Phytologist},
number = 2,
volume = 217,
place = {United States},
year = {2017},
month = {10}
}

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Works referenced in this record:

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

  • Grotewold, Erich; Peterson, Thomas
  • Molecular and General Genetics MGG, Vol. 242, Issue 1
  • DOI: 10.1007/BF00277341

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

  • Koes, Ronald E.; Quattrocchio, Francesca; Mol, Joseph N. M.
  • BioEssays, Vol. 16, Issue 2
  • DOI: 10.1002/bies.950160209

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

  • Aravind, L.; Watanabe, H.; Lipman, D. J.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 21
  • DOI: 10.1073/pnas.200346997

Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors
journal, October 2008

  • Butelli, Eugenio; Titta, Lucilla; Giorgio, Marco
  • Nature Biotechnology, Vol. 26, Issue 11
  • DOI: 10.1038/nbt.1506

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

  • Weng, Jing-Ke; Akiyama, Takuya; Bonawitz, Nicholas D.
  • The Plant Cell, Vol. 22, Issue 4
  • DOI: 10.1105/tpc.109.073528

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

Cloning of Chalcone–Flavanone Isomerase cDNA fromPueraria lobataand Its Overexpression inEscherichia coli
journal, September 1996

  • Terai, Yoshiya; Fujii, Isao; Byun, Soon-He
  • Protein Expression and Purification, Vol. 8, Issue 2
  • DOI: 10.1006/prep.1996.0091

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

  • Curtis, Mark D.; Grossniklaus, Ueli
  • Plant Physiology, Vol. 133, Issue 2, p. 462-469
  • DOI: 10.1104/pp.103.027979

A Rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants
journal, November 2008

  • Gambino, Giorgio; Perrone, Irene; Gribaudo, Ivana
  • Phytochemical Analysis, Vol. 19, Issue 6
  • DOI: 10.1002/pca.1078

A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation
journal, March 2014

  • Morita, Yasumasa; Takagi, Kyoko; Fukuchi-Mizutani, Masako
  • The Plant Journal, Vol. 78, Issue 2
  • DOI: 10.1111/tpj.12469

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

  • Ngaki, Micheline N.; Louie, Gordon V.; Philippe, Ryan N.
  • Nature, Vol. 485, Issue 7399
  • DOI: 10.1038/nature11009

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

  • Blyden, E. R.; Doerner, P. W.; Lamb, C. L.
  • Plant Molecular Biology, Vol. 16, Issue 1
  • DOI: 10.1007/BF00017927

Partial Reconstruction of Flavonoid and Isoflavonoid Biosynthesis in Yeast Using Soybean Type I and Type II Chalcone Isomerases
journal, March 2005

  • Ralston, Lyle; Subramanian, Senthil; Matsuno, Michiyo
  • Plant Physiology, Vol. 137, Issue 4
  • DOI: 10.1104/pp.104.054502

Nuclear Localization of Flavonoid Enzymes in Arabidopsis
journal, April 2005

  • Saslowsky, David E.; Warek, Ujwala; Winkel, Brenda S. J.
  • Journal of Biological Chemistry, Vol. 280, Issue 25
  • DOI: 10.1074/jbc.M413506200

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

  • Luceri, Cristina; Giovannelli, Lisa; Pitozzi, Vanessa
  • Food and Chemical Toxicology, Vol. 46, Issue 4
  • DOI: 10.1016/j.fct.2007.10.007

Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants
journal, November 2006

  • Sparkes, Imogen A.; Runions, John; Kearns, Anne
  • Nature Protocols, Vol. 1, Issue 4
  • DOI: 10.1038/nprot.2006.286

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

  • Koduri, P. K. Harshavardhan; Gordon, Graeme S.; Barker, Elizabeth I.
  • Plant Molecular Biology, Vol. 72, Issue 3
  • DOI: 10.1007/s11103-009-9565-z

Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.)
journal, March 1994

  • Sparvoli, Francesca; Martin, Cathie; Scienza, Attilio
  • Plant Molecular Biology, Vol. 24, Issue 5
  • DOI: 10.1007/BF00029856

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

  • Forkmann, G.; Dangelmayr, B.
  • Biochemical Genetics, Vol. 18, Issue 5-6
  • DOI: 10.1007/BF00484399

Independent origins of syringyl lignin in vascular plants
journal, May 2008

  • Weng, J. -K.; Li, X.; Stout, J.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 22
  • DOI: 10.1073/pnas.0801696105

Multiple functional roles of flavonoids in photoprotection: Letters
journal, May 2010


Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis
journal, October 2002

  • Liu, C. -J.; Blount, J. W.; Steele, C. L.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 22
  • DOI: 10.1073/pnas.212522099

Transition state stabilization by general acid catalysis, water expulsion, and enzyme reorganization in Medicago savita chalcone isomerase
journal, February 2004

  • Hur, S.; Newby, Z. E. R.; Bruice, T. C.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
  • DOI: 10.1073/pnas.0308264100

Flavonoid Biosynthesis. A Colorful Model for Genetics, Biochemistry, Cell Biology, and Biotechnology
journal, June 2001


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

  • Sodhi, Kushneet Kaur; Kumar, Mohit; Singh, Dileep Kumar
  • Archives of Microbiology, Vol. 202, Issue 6
  • DOI: 10.1007/s00203-020-01868-1

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

  • van Tamelen, Eugene E.
  • Journal of the American Chemical Society, Vol. 78, Issue 6
  • DOI: 10.1021/ja01587a062

Progress in the Chemistry of Organic Natural Products
journal, January 1977


Progress in the Chemistry of Organic Natural Products.
journal, July 1960

  • van Tamelen, E. E.
  • Journal of the American Chemical Society, Vol. 82, Issue 14
  • DOI: 10.1021/ja01499a099

Works referencing / citing this record:

UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants
journal, August 2018

  • Clayton, William A.; Albert, Nick W.; Thrimawithana, Amali H.
  • The Plant Journal, Vol. 96, Issue 3
  • DOI: 10.1111/tpj.14044

Auronidins are a previously unreported class of flavonoid pigments that challenges when anthocyanin biosynthesis evolved in plants
journal, September 2019

  • Berland, Helge; Albert, Nick W.; Stavland, Anne
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 40
  • DOI: 10.1073/pnas.1912741116

Noncatalytic chalcone isomerase-fold proteins in Humulus lupulus are auxiliary components in prenylated flavonoid biosynthesis
journal, May 2018

  • Ban, Zhaonan; Qin, Hao; Mitchell, Andrew J.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 22
  • DOI: 10.1073/pnas.1802223115

The Origin and Evolution of Plant Flavonoid Metabolism
journal, August 2019

  • Yonekura-Sakakibara, Keiko; Higashi, Yasuhiro; Nakabayashi, Ryo
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00943

Identification and evolutionary analysis of chalcone isomerase-fold proteins in ferns
journal, September 2019

  • Ni, Rong; Zhu, Ting-Ting; Zhang, Xiao-Shuang
  • Journal of Experimental Botany, Vol. 71, Issue 1
  • DOI: 10.1093/jxb/erz425

Identification and evolutionary analysis of chalcone isomerase-fold proteins in ferns
journal, September 2019

  • Ni, Rong; Zhu, Ting-Ting; Zhang, Xiao-Shuang
  • Journal of Experimental Botany, Vol. 71, Issue 1
  • DOI: 10.1093/jxb/erz425

The Origin and Evolution of Plant Flavonoid Metabolism
journal, August 2019

  • Yonekura-Sakakibara, Keiko; Higashi, Yasuhiro; Nakabayashi, Ryo
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00943

The Evolution of Flavonoid Biosynthesis: A Bryophyte Perspective
journal, February 2020