CoChat
Sign Up
Cited by 65Plant Gene Expression AnalysisBiochemical and biochemical processesPlant biochemistry and biosynthesis

The DOI matches its Crossref record.

Rerouting the Plant Phenylpropanoid Pathway by Expression of a Novel Bacterial Enoyl-CoA Hydratase/Lyase Enzyme Function

Open access
Mayer, Melinda J., Narbad, Arjan, Parr, Adrian J., Parker, Mary L., Walton, Nicholas J., Mellon, Fred A., Michael, Anthony J.·2001·The Plant Cell
DOI 10.1105/tpc.010063PMC PMC139547
Open this paper in CoChat — free account

Abstract

The gene for a bacterial enoyl-CoA hydratase (crotonase) homolog (HCHL) previously shown to convert 4-coumaroyl-CoA, caffeoyl-CoA, and feruloyl-CoA to the corresponding hydroxybenzaldehydes in vitro provided an opportunity to subvert the plant phenylpropanoid pathway and channel carbon flux through 4-hydroxybenzaldehyde and the important flavor compound 4-hydroxy-3-methoxybenzaldehyde (vanillin). Expression of the Pseudomonas fluorescens AN103 HCHL gene in two generations of tobacco plants caused the development of phenotypic abnormalities, including stunting, interveinal chlorosis and senescence, curled leaf margins, low pollen production, and male sterility. In second generation progeny, the phenotype segregated with the transgene and transgenic siblings exhibited orange/red coloration of the vascular ring, distorted cells in the xylem and phloem bundles, and lignin modification/reduction. There was depletion of the principal phenolics concomitant with massive accumulation of novel metabolites, including the glucosides and glucose esters of 4-hydroxybenzoic acid and vanillic acid and the glucosides of 4-hydroxybenzyl alcohol and vanillyl alcohol. HCHL plants exhibited increased accumulation of transcripts for phenylalanine ammonia-lyase, cinnamate-4-hydroxylase, and 4-coumarate:CoA ligase, whereas beta-1,3-glucanase was suppressed. This study, exploiting the ability of a bacterial gene to divert plant secondary metabolism, provides insight into how plants modify inappropriately accumulated metabolites and reveals the consequences of depleting the major phenolic pools.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1105/tpc.010063

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Alterations in primary metabolites are observed in various plants with altered secondary metabolism.

    “Furthermore, alterations in primary metabolites are observed in various plants with altered secondary metabolism (Mayer et al., 2001;Narayanan et al., 2011;Huber et al., 2016;Machado et al., 2017;Zhang et al., 2020), and the accumulation of specific secondary metabolites has been associated with storage and growth in microevolutionary studies (Heath et al., 2014).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Mayer et al., 2001

    The Results section reports altered phenolics and novel secondary metabolites in HCHL-expressing tobacco, but does not report changes in primary metabolites. Searches for primary metabolites, sugars, amino acids, and precursor pools found no passage establishing that part of the claim; the paper also studies tobacco rather than various plants. Page numbers were not available in our copy. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 56

  1. Atanassova, R., Favet, N., Martz, F., Chabbert, B., Tollier, M.-T., Monties, B., Fritig, B., and Legrand, M. (1995). Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and antisense orientation. Plant J. 8, 465–477. [Google Scholar]
  2. Bate, N.J., Orr, J., Ni, W., Meromi, A., Nadler-Hassar, T., Doerner, P.W., Dixon, R.A., Lamb, C.J., and Elkind, Y. (1994). Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-limiting step in natural product synthesis. Proc. Natl. Acad. Sci. USA 91, 7608–7612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baucher, M., Chabbert, B., Pilate, G., Van Doorsselaere, J., Tollier, M.-T., Petit-Conil, M., Cornu, D., Monties, B., Van Montagu, M., Inze, D., Jouanin, L., and Boerjan, W. (1996). Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol. 112, 1479–1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bevan, M. (1984). Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711–8721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blount, J.W., Korth, K.L., Masoud, S.A., Rasmussen, S., Lamb, C., and Dixon, R.A. (2000). Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiol. 122, 107–116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boudet, A.-M. (1998). A new view of lignification. Trends Plant Sci. 3, 67–71. [Google Scholar]
  7. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254. [DOI] [PubMed] [Google Scholar]
  8. Campbell, M.M., and Sederoff, R.R. (1996). Variation in lignin content and composition: Mechanisms of control and implications for the genetic improvement of plants. Plant Physiol. 110, 3–13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carter, A.J., Beiche, F., Hove-Jensen, B., Narbad, A., Barker, P.J., Schweizer, L.M., and Schweizer, M. (1997). PRS1 is a key member of the gene family encoding phosphoribosylpyrophosphate synthase in Saccharomyces cerevisiae. Mol. Gen. Genet. 254, 148–156. [DOI] [PubMed] [Google Scholar]
  10. Chapple, C.C.S., Vogt, T., Ellis, B.E., and Somerville, C.R. (1992). An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4, 1413–1424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cooper-Driver, G., Corner-Zamodits, J.J., and Swain, T. (1972). The metabolic fate of hydroxybenzoic acids in plants. Z. Naturforsch. 27, 943. [Google Scholar]
  12. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E., and Ryals, J. (1994). A central role of salicylic acid in plant disease resistance. Science 266, 1247–1250. [DOI] [PubMed] [Google Scholar]
  13. Dixon, R.A., and Paiva, N.L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085–1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dixon, R.A., Lamb, C.J., Masoud, S., Sewalt, V.J.H., and Paiva, N.L. (1996). Metabolic engineering: Prospects for crop improvement through the genetic manipulation of phenylpropanoid biosynthesis and defense responses. A review. Gene 179, 61–71. [DOI] [PubMed] [Google Scholar]
  15. Elkind, Y., Edwards, R., Mavandad, M., Hedrick, S.A., Ribak, O., Dixon R.A., and Lamb, C.J. (1990). Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc. Natl. Acad. Sci. USA 87, 9057–9061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fecker, L.F., Rugenhagen, C., and Berlin, J. (1993). Increased production of cadaverine and anabasine in hairy root cultures of Nicotiana tabacum expressing a bacterial lysine decarboxylase gene. Plant Mol. Biol. 23, 11–21. [DOI] [PubMed] [Google Scholar]
  17. Fischer, R., Budde, I., and Hain, R. (1997). Stilbene synthase gene expression causes changes in flower colour and male sterility in tobacco. Plant J. 11, 489–498. [Google Scholar]
  18. Gasson, M.J., Kitamura, Y., McLauchlan, W.R., Narbad, A., Parr, A.J., Parsons, E.L.H., Payne, J., Rhodes, M.J.C., and Walton, N.J. (1998). Metabolism of ferulic acid to vanillin: A bacterial gene of the enoyl-SCoA hydratase/isomerase superfamily encodes an enzyme for the hydration and cleavage of a hydroxycinnamic acid SCoA thioester. J. Biol. Chem. 273, 4163–4170. [DOI] [PubMed] [Google Scholar]
  19. Guerineau, F., Lucy, A., and Mullineaux, P. (1992). Effect of two consensus sequences preceding the translation initiator codon on gene expression in plant protoplasts. Plant Mol. Biol. 18, 815–818. [DOI] [PubMed] [Google Scholar]
  20. Hain, R., Reif, H.J., Krause, E., Langebartels, R., Kindl, H., Vornam, B., Wiese, W., Schmelzer, E., Schreier, P.H., Stocker, R.H., and Stenzel, K. (1993). Disease resistance results from foreign phytoalexin expression in a novel plant. Nature 361, 153–156. [DOI] [PubMed] [Google Scholar]
  21. Halpin, C., Knight, M.E., Foxon, G.A., Campbell, M.M., Boudet, A.M., Boon, J.J., Chabbert, B., Tollier, M.-T., and Schuch, W. (1994). Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J. 6, 339–350. [Google Scholar]
  22. Hibino, T., Takabe, K., Kawazu, T., Shibata, D., and Higuchi, T. (1995). Increase of cinnamaldehyde groups in lignin of transgenic tobacco plants carrying an antisense gene for cinnamyl alcohol dehydrogenase. Biosci. Biotechnol. Biochem. 59, 929–931. [Google Scholar]
  23. Higuchi, T., Ito, T., Umezawa, T., Hibino, T., and Shibata, D. (1994). Red-brown color of lignified tissues of transgenic plants with antisense CAD gene: Wine-red lignin from coniferyl aldehyde. J. Biotechnol. 37, 151–158. [Google Scholar]
  24. Hoffman, N.E., Ko, K., Milkowski, D., and Pichersky, E. (1991). Isolation and characterization of tomato cDNA and genomic clones encoding the ubiquitin gene ubi3. Plant Mol. Biol. 17, 1189–1201. [DOI] [PubMed] [Google Scholar]
  25. Horsch, R.B., Fry, J.E., Hoffman, N.L., Eichholtz, D., Rogers, S.G., and Fraley, R.T. (1985). A simple and general method for transferring genes into plants. Science 227, 1229–1231. [DOI] [PubMed] [Google Scholar]
  26. Kajita, S., Katayama, Y., and Omori, S. (1996). Alterations in the biosynthesis of lignin in transgenic plants with chimeric genes for 4-coumarate:coenzyme A ligase. Plant Cell Physiol. 37, 957–965. [DOI] [PubMed] [Google Scholar]
  27. Karrer, E.E., Beachy, R.N., and Holt, C.A. (1998). Cloning of tobacco genes that elicit the hypersensitive response. Plant Mol. Biol. 36, 681–690. [DOI] [PubMed] [Google Scholar]
  28. Kozak, M. (1986). Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44, 283–292. [DOI] [PubMed] [Google Scholar]
  29. Lee, D., Meyer, K., Chapple, C., and Douglas, C.J. (1997). Antisense suppression of 4-coumarate:coenzyme A ligase activity in Arabidopsis leads to altered lignin subunit composition. Plant Cell 9, 1985–1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Li, S.-M., Wang, Z.-X., Wemakor, E., and Heide, L. (1997). Metabolization of the artificial secondary metabolite 4-hydroxybenzoate in ubiC-transformed tobacco. Plant Cell Physiol. 38, 844–850. [Google Scholar]
  31. MacKay, J.J., Liu, W., Whetten, R., Sederoff, R.R., and O'Malley, D.M. (1995). Genetic analysis of cinnamyl alcohol dehydrogenase in loblolly pine: Single gene inheritance, molecular characterization and evolution. Mol. Gen. Genet. 247, 537–545. [DOI] [PubMed] [Google Scholar]
  32. Martin, C., Carpenter, R., Sommer, H., Saedler, H., and Coen, E.S. (1985). Molecular analysis of instability in flower pigmentation of Antirrhinum majus following isolation of the pallida locus by transposon tagging. EMBO J. 4, 1625–1630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mitra, A. (1999). 4-Hydroxycinnamoyl-CoA Hydratase/Lyase from Pseudomonas fluorescens AN103: Characterisation and Effects of Expression in Transformed Root Cultures of Datura stramonium. PhD Dissertation (University of East Anglia, Norwich, UK).
  34. Mitra, A., Kitamura, Y., Gasson, M.J., Narbad, A., Parr, A.J., Payne, J., Rhodes, M.J.C., Sewter, C., and Walton, N.J. (1999). 4-Hydroxycinnamoyl-CoA hydratase/lyase (HCHL): An enzyme of phenylpropanoid chain cleavage from Pseudomonas. Arch. Biochem. Biophys. 365, 10–16. [DOI] [PubMed] [Google Scholar]
  35. Mo, Y., Nagel, C., and Taylor, L.P. (1992). Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. USA 89, 7213–7217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497. [Google Scholar]
  37. Narbad, A., and Gasson, M.J. (1998). Metabolism of ferulic acid via vanillin using a novel CoA-dependent pathway in a newly-isolated strain of Pseudomonas fluorescens. Microbiology 144, 1397–1405. [DOI] [PubMed] [Google Scholar]
  38. Piquemal, J., Lapierre, C., Myton, K., O'Connell, A., Schuch, W., Grima-Pettenati, J., and Boudet, A.-M. (1998). Down-regulation of cinnamoyl-CoA reductase induces significant changes in lignin profiles in transgenic tobacco plants. Plant J. 13, 71–83. [Google Scholar]
  39. Rasmussen, S., and Dixon, R.A. (1999). Transgene-mediated and elicitor-induced perturbation of metabolic channelling at the entry point into the phenylpropanoid pathway. Plant Cell 11, 1537–1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
  41. Siebert, M., Sommer, S., Li, S.-m., Wang, Z.-w., Severin, K., and Heide, L. (1996). Genetic engineering of plant secondary metabolism: Accumulation of 4-hydroxybenzoate glucosides as a result of the expression of the bacterial ubiC gene in tobacco. Plant Physiol. 112, 811–819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Snook, M.E., Mason, P.F., and Sisson, V.A. (1986). Polyphenols in the Nicotiana species. Tob. Sci. 30, 43–49. [Google Scholar]
  43. Sommer, S., and Heide, L. (1998). Expression of the bacterial chorismate pyruvate-lyase in tobacco: Evidence for the presence of chorismate in the plant cytosol. Plant Cell Physiol. 39, 1240–1244. [DOI] [PubMed] [Google Scholar]
  44. Sommer, S., Köhle, A., Yazaki, K., Shimomura, K., Bechthold, A., and Heide, L. (1999). Genetic engineering of shikonin biosynthesis hairy root cultures of Lithospermum erythrorhizon transformed with the bacterial ubiC gene. Plant Mol. Biol. 39, 683–693. [DOI] [PubMed] [Google Scholar]
  45. Speer, O.E. (1987). A method of retaining phloroglucinol proof of lignin. Stain Technol. 62, 279–280. [DOI] [PubMed] [Google Scholar]
  46. Tamagnone, L., Merida, A., Parr, A., MacKay, S., Culianez-Macia, F.A., Roberts, K., and Martin, C. (1998). The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10, 135–154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tsai, C.-J., Popko, J.L., Mielke, M.R., Hu, W.-J., Podila, G.K., and Chiang, V.L. (1998). Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol. 117, 101–112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. van der Meer, I.M., Stam, M.E., van Tunen, A.J., Mol, J.N., and Stuitje, A.R. (1992). Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4, 253–262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. van Doorsselaere, J., et al. (1995). A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic O-methyltransferase activity. Plant J. 8, 855–864. [Google Scholar]
  50. Verwoerd, T.C., Dekker, B.M.M., and Hoekema, A. (1989). A small-scale procedure for the rapid isolation of plant RNA. Nucleic Acids Res. 17, 2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Vignols, F., Rigau, J., Torres, M.A., Capellades, M., and Puigdomenech, P. (1995). The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7, 407–416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Ward, E.R., Payne, G.B., Moyer, M.B., Williams, S.C., Dincher, S.S., Sharkey, K.C., Beck, J.J., Taylor, H.T., Ahl-Goy, P., Meins, F., Jr., and Ryals, J.A. (1991). Differential regulation of β-1,3-glucanase messenger RNAs in response to pathogen infection. Plant Physiol. 96, 390–397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Winkel-Shirley, B. (1999). Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol. Plant. 107, 142–149. [Google Scholar]
  54. Yahiaoui, N., Marque, C., Myton, K.E., Negrel, J., and Boudet, A.M. (1998). Impact of different levels of cinnamyl alcohol dehydrogenase down-regulation on lignins of transgenic tobacco plants. Planta 204, 8–15. [DOI] [PubMed] [Google Scholar]
  55. Ylstra, B., Touraev, A., Moreno, R.M.B., Stöger, E., Van Tunen, A.J., Vicente, O., Mol, J.N.M., and Heberle-Bors, E. (1992). Flavonols stimulate development, germination and tube growth of tobacco pollen. Plant Physiol. 100, 902–907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Yun, D.-J., Hashimoto, T., and Yamada, Y. (1992). Metabolic engineering of medicinal plants: Transgenic Atropa belladonna with an improved alkaloid composition. Proc. Natl. Acad. Sci. USA 89, 11799–11803. [DOI] [PMC free article] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Metadata

Authors
Mayer, M. J., Narbad, A., Parr, A. J., Parker, M. L., Walton, N. J., Mellon, F. A., & Michael, A. J.
Affiliations
Norwich Research Park (GB)
ORCID
Venue
The Plant Cell
Publisher
Oxford University Press (OUP)
Published
2001-07
Volume
13
Issue
7
Pages
1669-1682
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
DOI
10.1105/tpc.010063
PMC
PMC139547
OpenAlex
W2141280003
Cited by
65
References
0
Citations by year
2026: 1 · 2024: 6 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 1 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 2 · 2012: 5
FWCI
1.17
Type
journal article
Language
en
Open access
Licence
aspb.org/publications/aspb-journals/open-articles (vor, 365 d)
Locations
  • The Plant Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Biotechnology and Biological Sciences Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Gene Expression Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Biochemical and biochemical processes
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
phenylpropanoid pathway, Pseudomonas fluorescens, transgenic tobacco, vanillin, 4-hydroxybenzaldehyde, lignin reduction, male sterility, chlorosis, phenylalanine ammonia-lyase, cinnamate 4-hydroxylase, 4-coumarate:CoA ligase, β-1,3-glucanase, plant secondary metabolism
MeSH terms
Acyl Coenzyme A, Anthocyanins, Antioxidants, Bacterial Proteins, Benzaldehydes, Enoyl-CoA Hydratase, Hydro-Lyases, Phenols, Phenotype, Plants, Toxic, Pseudomonas fluorescens, RNA, Messenger, Nicotiana, Vanillic Acid, Genes, Plant, Gene Expression Regulation, Plant, Plant Structures, RNA, Plant, Plants, Genetically Modified

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review