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      Characterization of Arabidopsis thaliana Hydroxyphenylpyruvate Reductases in the Tyrosine Conversion Pathway

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          Abstract

          Tyrosine serves as a precursor to several types of plant natural products of medicinal or nutritional interests. Hydroxyphenylpyruvate reductase (HPPR), which catalyzes the reduction of 4-hydroxyphenylpyruvic acid (pHPP) to 4-hydroxyphenyllactic acid (pHPL), has been shown to be the key enzyme in the biosynthesis of rosmarinic acid (RA) from tyrosine and, so far, HPPR activity has been reported only from the RA-accumulating plants. Here, we show that HPPR homologs are widely distributed in land plants. In Arabidopsis thaliana, which does not accumulate RA at detectable level, two homologs (HPPR2 and HPPR3) are functional in reducing pHPP. Phylogenetic analysis placed HPPR2 and HPPR3 in two separate groups within the HPPR clade, and HPPR2 and HPPR3 are distinct from HPR1, a peroxisomal hydroxypyruvate reductase (HPR). In vitro characterization of the recombinant proteins revealed that HPPR2 has both HPR and HPPR activities, whereas HPPR3 has a strong preference for pHPP, and both enzymes are localized in the cytosol. Arabidopsis mutants defective in either HPPR2 or HPPR3 contained lower amounts of pHPL and were impaired in conversion of tyrosine to pHPL. Furthermore, a loss-of-function mutation in tyrosine aminotransferase (TAT) also reduced the pHPL accumulation in plants. Our data demonstrate that in Arabidopsis HPPR2 and HPPR3, together with TAT1, constitute to a probably conserved biosynthetic pathway from tyrosine to pHPL, from which some specialized metabolites, such as RA, can be generated in specific groups of plants. Our finding may have broad implications for the origins of tyrosine-derived specialized metabolites in general.

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          Most cited references35

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          Physiology and Molecular Biology of Phenylpropanoid Metabolism

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            Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B.

            Sourdough lactic acid bacteria were selected for antifungal activity by a conidial germination assay. The 10-fold-concentrated culture filtrate of Lactobacillus plantarum 21B grown in wheat flour hydrolysate almost completely inhibited Eurotium repens IBT18000, Eurotium rubrum FTDC3228, Penicillium corylophilum IBT6978, Penicillium roqueforti IBT18687, Penicillium expansum IDM/FS2, Endomyces fibuliger IBT605 and IDM3812, Aspergillus niger FTDC3227 and IDM1, Aspergillus flavus FTDC3226, Monilia sitophila IDM/FS5, and Fusarium graminearum IDM623. The nonconcentrated culture filtrate of L. plantarum 21B grown in whole wheat flour hydrolysate had similar inhibitory activity. The activity was fungicidal. Calcium propionate at 3 mg ml(-1) was not effective under the same assay conditions, while sodium benzoate caused inhibition similar to L. plantarum 21B. After extraction with ethyl acetate, preparative silica gel thin-layer chromatography, and chromatographic and spectroscopic analyses, novel antifungal compounds such as phenyllactic and 4-hydroxy-phenyllactic acids were identified in the culture filtrate of L. plantarum 21B. Phenyllactic acid was contained at the highest concentration in the bacterial culture filtrate and had the highest activity. It inhibited all the fungi tested at a concentration of 50 mg ml(-1) except for P. roqueforti IBT18687 and P. corylophilum IBT6978 (inhibitory concentration, 166 mg ml(-1)). L. plantarum 20B, which showed high antimold activity, was also selected. Preliminary studies showed that phenyllactic and 4-hydroxy-phenyllactic acids were also contained in the bacterial culture filtrate of strain 20B. Growth of A. niger FTDC3227 occurred after 2 days in breads started with Saccharomyces cerevisiae 141 alone or with S. cerevisiae and Lactobacillus brevis 1D, an unselected but acidifying lactic acid bacterium, while the onset of fungal growth was delayed for 7 days in bread started with S. cerevisiae and selected L. plantarum 21B.
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              Genome-wide analysis of phenylpropanoid defence pathways.

              Phenylpropanoids can function as preformed and inducible antimicrobial compounds, as well as signal molecules, in plant-microbe interactions. Since we last reviewed the field 8 years ago, there has been a huge increase in our understanding of the genes of phenylpropanoid biosynthesis and their regulation, brought about largely by advances in genome technology, from whole-genome sequencing to massively parallel gene expression profiling. Here, we present an overview of the biosynthesis and roles of phenylpropanoids in plant defence, together with an analysis of confirmed and predicted phenylpropanoid pathway genes in the sequenced genomes of 11 plant species. Examples are provided of phylogenetic and expression clustering analyses, and the large body of underlying genomic data is provided through a website accessible from the article. © 2010 The Authors.Molecular Plant Pathology © 2010 BSPP and Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                05 September 2018
                2018
                : 9
                : 1305
                Affiliations
                [1] 1Shanghai Key Laboratory of Plant Functional Genomics and Resources, Plant Science Research Center, Shanghai Chenshan Botanical Garden , Shanghai, China
                [2] 2National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences , Shanghai, China
                [3] 3John Innes Centre, Norwich Research Park , Norwich, United Kingdom
                Author notes

                Edited by: Wanchai De-Eknamkul, Chulalongkorn University, Thailand

                Reviewed by: André O. Hudson, Rochester Institute of Technology, United States; Yan Lu, Western Michigan University, United States

                *Correspondence: Lei Yang, leiyang@ 123456sibs.ac.cn

                This article was submitted to Plant Metabolism and Chemodiversity, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01305
                6133988
                30233632
                43e4b032-1f3c-49aa-ac7a-2a86224b1a54
                Copyright © 2018 Xu, Fang, Li, Zhao, Martin, Chen and Yang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 July 2018
                : 17 August 2018
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 44, Pages: 13, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                hydroxyphenylpyruvate reductase,4-hydroxyphenyllactic acid,tyrosine,rosmarinic acid,arabidopsis thaliana,secondary metabolism

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