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

Journal Article · Tue Oct 06 00:00:00 EDT 2020 · Plant Physiology (Bethesda)

DOI:https://doi.org/10.1104/pp.20.01185· OSTI ID:1670506

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]; Liu, Chang-Jun  ^[2]; Lou, Hong-Xiang ^[1]; Cheng, Ai-Xia  ^[1]

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

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.

• Research Organization: Brookhaven National Laboratory (BNL), Upton, NY (United States)
• Sponsoring Organization: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)
• Grant/Contract Number: SC0012704; 31770330; 81630093
• OSTI ID: 1670506
• Alternate ID(s): OSTI ID: 1763339
• Report Number(s): BNL-220930-2021-JAAM; /plantphysiol/184/4/1731.atom
• Journal Information: Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Vol. 184 Journal Issue: 4; ISSN 0032-0889
• Publisher: American Society of Plant Biologists
• Country of Publication: United States
• Language: English

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
evolution
flavanone 3-beta-hydroxylase
flavone synthase I
liverworts
2-oxoglutarate/Fe(II)-dependent dioxygenase