Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants

Li, Dan-Dan; Ni, Rong; Wang, Ping-Ping; Zhang, Xiao-Shuang; Wang, Piao-Yi; Zhu, Ting-Ting; Sun, Chun-Jing; Liu, Chang-Jun; Lou, Hong-Xiang; Cheng, Ai-Xia

doi:10.1104/pp.20.01185

Title: Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants

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Abstract

During the course of evolution of land plants, different classes of flavonoids, including flavonols and anthocyanins, sequentially emerged, facilitating adaptation to the harsh terrestrial environment. Flavanone 3β-hydroxylase (F3H), an enzyme functioning in flavonol and anthocyanin biosynthesis and a member of the 2-oxoglutarate dependent dioxygenase (2-ODD) family, catalyzes the hydroxylation of (2S)-flavanones to dihydroflavonols, but its origin and evolution remains elusive. In this work, we demonstrate that functional flavone synthase Is (FNS Is) are widely distributed in the primitive land plants liverworts and evolutionarily connected to seed plant F3Hs. We identified and characterized a set of 2-ODD enzymes from several liverwort species and plants in various evolutionary clades of the plant kingdom. The bifunctional enzyme FNS I/F2H emerged in liverworts, and FNS I/F3H evolved in Physcomitrium (Physcomitrella) patens and Selaginella moellendorffii, suggesting they represent the functional transition forms between canonical FNS Is and F3Hs. The functional transition from FNS Is to F3Hs provides a molecular basis for the chemical evolution of flavones to flavonols and anthocyanins, which contributes to the acquisition of a broader spectrum of flavonoids in seed plants and facilitates their adaptation to the terrestrial ecosystem.

Authors:

Li, Dan-Dan ^[1]; Ni, Rong ^[1]; Wang, Ping-Ping ^[1]; Zhang, Xiao-Shuang ^[1]; Wang, Piao-Yi ^[1]; Zhu, Ting-Ting ^[1]; Sun, Chun-Jing ^[1];

^[2]; Lou, Hong-Xiang ^[1];

^[1]

Key Laboratory of Chemical Biology of Natural Products, Ministry of Education, School of Pharmaceutical Sciences, Shandong University, Jinan 250012, China
Biology Department, Brookhaven National Laboratory, Upton, New York 11973

Publication Date:: Tue Oct 06 00:00:00 EDT 2020

Research Org.:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)

OSTI Identifier:: 1670506

Alternate Identifier(s):: OSTI ID: 1763339

Report Number(s):: BNL-220930-2021-JAAM
Journal ID: ISSN 0032-0889; /plantphysiol/184/4/1731.atom

Grant/Contract Number:: SC0012704; 31770330; 81630093

Resource Type:: Published Article

Journal Name:: Plant Physiology (Bethesda)

Additional Journal Information:: Journal Name: Plant Physiology (Bethesda) Journal Volume: 184 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; evolution; flavanone 3-beta-hydroxylase; flavone synthase I; liverworts; 2-oxoglutarate/Fe(II)-dependent dioxygenase

Citation Formats


                    Li, Dan-Dan, Ni, Rong, Wang, Ping-Ping, Zhang, Xiao-Shuang, Wang, Piao-Yi, Zhu, Ting-Ting, Sun, Chun-Jing, Liu, Chang-Jun, Lou, Hong-Xiang, and Cheng, Ai-Xia. Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants.  United States: N. p., 2020. 
Web.  doi:10.1104/pp.20.01185.

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                    Li, Dan-Dan, Ni, Rong, Wang, Ping-Ping, Zhang, Xiao-Shuang, Wang, Piao-Yi, Zhu, Ting-Ting, Sun, Chun-Jing, Liu, Chang-Jun, Lou, Hong-Xiang, & Cheng, Ai-Xia. Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants.  United States.  https://doi.org/10.1104/pp.20.01185

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                    Li, Dan-Dan, Ni, Rong, Wang, Ping-Ping, Zhang, Xiao-Shuang, Wang, Piao-Yi, Zhu, Ting-Ting, Sun, Chun-Jing, Liu, Chang-Jun, Lou, Hong-Xiang, and Cheng, Ai-Xia. Tue .  
"Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants".  United States.  https://doi.org/10.1104/pp.20.01185.

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@article{osti_1670506,

  title        = {Molecular Basis for Chemical Evolution of Flavones to Flavonols and Anthocyanins in Land Plants},

  author       = {Li, Dan-Dan and Ni, Rong and Wang, Ping-Ping and Zhang, Xiao-Shuang and Wang, Piao-Yi and Zhu, Ting-Ting and Sun, Chun-Jing and Liu, Chang-Jun and Lou, Hong-Xiang and Cheng, Ai-Xia},

  abstractNote = {During the course of evolution of land plants, different classes of flavonoids, including flavonols and anthocyanins, sequentially emerged, facilitating adaptation to the harsh terrestrial environment. Flavanone 3β-hydroxylase (F3H), an enzyme functioning in flavonol and anthocyanin biosynthesis and a member of the 2-oxoglutarate dependent dioxygenase (2-ODD) family, catalyzes the hydroxylation of (2S)-flavanones to dihydroflavonols, but its origin and evolution remains elusive. In this work, we demonstrate that functional flavone synthase Is (FNS Is) are widely distributed in the primitive land plants liverworts and evolutionarily connected to seed plant F3Hs. We identified and characterized a set of 2-ODD enzymes from several liverwort species and plants in various evolutionary clades of the plant kingdom. The bifunctional enzyme FNS I/F2H emerged in liverworts, and FNS I/F3H evolved in Physcomitrium (Physcomitrella) patens and Selaginella moellendorffii, suggesting they represent the functional transition forms between canonical FNS Is and F3Hs. The functional transition from FNS Is to F3Hs provides a molecular basis for the chemical evolution of flavones to flavonols and anthocyanins, which contributes to the acquisition of a broader spectrum of flavonoids in seed plants and facilitates their adaptation to the terrestrial ecosystem.},

  doi          = {10.1104/pp.20.01185},

  journal      = {Plant Physiology (Bethesda)},

  number       = 4,

  volume       = 184,

  place        = {United States},

  year         = {Tue Oct 06 00:00:00 EDT 2020},

  month        = {Tue Oct 06 00:00:00 EDT 2020}

}

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