ReviewTrends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity
The comprehensive analysis of the effects of genetic and mutational manipulations of monolignol pathway enzymes revealed fully predictable consequences on lignification and the vascular apparatus. Carbon allocation to the pathway is determined by Phe availability, and relative C4H and C3H activities. While the data obtained put to rest the claims of surrogate monomers being involved in lignin biosynthesis, new tools have been developed which now permit dissection of the lignin assembly process.
Section snippets
Introduction: overall scope of the analysis
In just over a decade, a number of studies have been conducted to manipulate gene expression in the monolignol (1–3) pathway, with important ramifications for control of subsequent lignin assembly(ies) (see Fig. 1). These studies have usually been done with the overall aim of modifying lignin contents and/or their compositions in plants. The anticipated benefits to humanity are potentially economic and environmental, in terms of cheaper and more process-amenable trees for pulp and paper
The functional basis for organized heterogeneous lignin assembly
From an evolutionary perspective, the monolignol-derived lignins are found in the pteridophytes (ferns), gymnosperms and angiosperms. [Fig. 1 summarizes our current understanding of the biosynthetic pathway to the monolignols (1–3) from Phe (4) and/or Tyr (5).] With few exceptions, it has long been known (Lewis and Yamamoto, 1990) that the monolignol pathway affording the corresponding lignins in pteridophytes and gymnosperms only utilizes p-coumaryl (1) and coniferyl (2) alcohols, whereas in
The control of monolignol ratio and lignin composition: metabolic and transcriptional profiling
Why do vascular plants consistently produce various types of cell walls with lignins from either two or three monolignols, and how does this occur in vivo? Furthermore, why are these moieties also differentially deposited into specific regions of developing cell wall types? To begin to answer such questions, two approaches have been taken: one is via metabolic flux and transcriptional profiling studies, and the second involves analysis of transgenic plants and/or mutants, where levels of
Technical limitations in current lignin analysis
Given that lignin deposition and composition can vary with cell wall layer, cell wall type and species, it is necessary to consider the efficacy and limitations of the lignin analytical procedures currently employed. Typically, these include methods of lignin quantification, estimates of lignin monomeric compositions, the isolation of lignin-derived preparations, and their spectroscopic analyses. None of these methods, however, are cell specific. Furthermore, each has serious limitations, most
Does perturbing lignin assembly always occur at the expense of vascular integrity?
To date, many transgenic plants and mutants have only been very preliminarily characterized, and thus the overall effects of genetic alteration are not well understood. This is especially true in terms of determining the effects on lignin assembly proper and the differential regulation of compartmentalized metabolic segments in the phenylpropanoid network. Nevertheless, it is instructive to consider what has been obtained thus far from studies directed towards lignin modification, and to
Concluding remarks
This comprehensive analysis summarizes what is known thus far as regards the preliminary characterization of plant tissues, following either up- or downregulation and/or mutation of various steps in the monolignol-forming pathway. The data obtained reveal a much more complex pattern of lignin assembly in different cell types and cell wall layers than hitherto recognized. No evidence, at any level of inquiry, indicated that the process of lignification, including biopolymer assembly, involved
Acknowledgements
The authors wish to thank the Department of Energy (DE-FG03-97ER20259), the National Aeronatutics and Space Administration (NAG2-1198 and NAG-1513), the US Department of Agriculture (99-35103-8037), McIntire-Stennis and the G. Thomas Hargrove and Lewis and Dorothy B. Cullman for generous support of the studies related to this review. The authors are also indebted to Drs. Richard A. Dixon and Jacquline Grima-Pettenati for PAL and CCR figures, respectively, and to Dr. Clint Chapple for provision
Norman G. Lewis is the Director of the Institute of Biological Chemistry and the Arthur M. and Katie Eisig-Tode Distinguished Professor at Washington State University. He was initially trained in Chemistry (BSc Honors, 1973, University of Strathclyde) before completing a PhD (1977) in organic chemistry (alkaloid biosynthesis) at the University of British Columbia (Vancouver, BC). Postdoctoral training was in alkaloid/Vitamin B12 biosynthesis with Sir Alan R. Battersby. Professor Lewis' current
References (171)
- et al.
Superinduction of phenylalanine ammonia-lyase in gherkin hypocotyls caused by the inhibitor, L-α-aminooxy-β-phenylpropionic acid
Biochimica et Biophysica Acta
(1979) - et al.
α-Aminooxy-β-phenylpropionic acid-a potent inhibitor of l-phenylalanine ammonia-lyase in vitro and in vivo
Plant Science Letters
(1977) - et al.
Transcriptional control of monolignol biosynthesis in Pinus taedafactors affecting monolignol ratios and carbon allocation in phenylpropanoid metabolism
The Journal of Biological Chemistry
(2002) - et al.
Multi-site modulation of flux during monolignol formation in loblolly pine (Pinus taeda)
Biochemical and Biophysical Research Communications
(1999) - et al.
Antisense and sense expression of cDNA coding for CYP73A15, a class II cinnamate 4-hydroxylase, leads to a delayed and reduced production of lignin in tobacco
Phytochemistry
(2001) A new view of lignification
Trends in Plant Sciences
(1998)- et al.
Phenylalanine ammonia lyase
Phytochemistry
(1973) - et al.
Lignification in cell suspension cultures of Pinus taeda. In situ characterization of a gymnosperm lignin
The Journal of Biological Chemistry
(1993) - et al.
Stress responses in alfalfa (Medicago sativa L.) XVIII: molecular cloning and expression of the elicitor-inducible cinnamic acid 4-hydroxylase cytochrome P450
Archives of Biochemistry and Biophysics
(1993) - et al.
Ozone induction and purification of spruce cinnamyl alcohol dehydrogenase
Phytochemistry
(1993)
Ferulic acid 5-hydroxylasea new cytochrome P-450-dependent enzyme from higher plant microsomes involved in lignin synthesis
Federation of European Biochemical Societies Letters
The mechanical properties of xylem tissue from tobacco plants (Nicotiana tabacum ‘Samsun’)
Annals of Botany
The growth response of the stems of genetically modified tobacco plants (Nicotiana tabacum ‘Samsun’) to flexural stimulation
Annals of Botany
Using viscoelastic properties of the woody tissue from tobacco plants (Nicotiana tabacum) to comment on the molecular structure of cell walls
Annals of Botany
Red-brown color of lignified tissues of transgenic plants with antisense CAD genewine-red lignin from coniferyl aldehyde
Journal of Biotechnology
Immunological characterization of transgenic tobacco plants with a chimeric gene for 4-coumarate:CoA ligase that have altered lignin in their xylem tissue
Plant Science
Transcriptional control of lignin biosynthesis by tobacco LIM protein
Phytochemistry
Formation of trans-caffeoyl-coA from trans-4-coumaroyl-CoA by Zn2+-dependent enzymes in cultured plant cells and its activation by an elicitor-induced pH shift
Archives of Biochemistry and Biophysics
The abnormal lignins produced by the brown-midrib mutants of maize. I. The brown-midrib-1 mutant
Archives of Biochemistry and Biophysics
Degradation of abnormal lignins in the brown-midrib mutants and double mutants of maize
Phytochemistry
Chlorogenic acid biosynthesischaracterization of a light-induced microsomal 5-O-(4-coumaroyl)-D-quinate/shikimate 3′-hydroxylase from carrot (Daucus carota L.) cell suspension cultures
Archives of Biochemistry and Biophysics
Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria
Phytochemistry
A 20th century roller coaster ridea short account of lignification
Current Opinion in Plant Biology
Lignansbiosynthesis and function
Turnover of isoflavones in Cicer arietinum L
Naturwissenschaften
Inhibition of lignin formation by L-α-aminooxy-β-phenylpropionic acid, an inhibitor of phenylalanine ammonia-lyase
European Journal of Cell Biology
Inhibition of anthocyanin formation in seedlings and flowers by the enantiomers of α-aminooxy-β-phenylpropionic acid and their N-benzyloxycarbonyl derivatives
Planta
Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and antisense orientation
The Plant Journal
Cloning of three A-type cytochromes P450, CYP71E1, CYP98, and CYP99 from Sorghum bicolor (L.) Moench by a PCR approach and identification by expression in Escherichia coli of CYP71E1 as a multifunctional cytochrome P450 in the biosynthesis of the cyanogenic glucoside dhurrin
Plant Molecular Biology
In vitro dry matter disappearance of brown midrib mutants of maize (Zea mays L.)
Journal of Animal Science
Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis
Proceedings of the National Academy of Sciences of the United States of America
Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility
Plant Molecular Biology
Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar
Plant Physiology
Biosynthesis and genetic engineering of lignin
Critical Reviews in Plant Sciences
Cell wall degradability of transgenic tobacco stems in relation to their chemical extraction and lignin quality
Journal of Agricultural and Food Chemistry
Sulphite-promoted delignification of woodidentification of paucidisperse lignosulphonates
Canadian Journal of Chemistry
Isolation of lignin from finely divided wood with neutral solvents
Nature
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 Physiology
Native lignin. I. Its isolation and methylation
Journal of the American Chemical Society
The Chemistry of Lignin
Molecular characterisation and expression of a wound-inducible cDNA encoding a novel cinnamyl-alcohol dehydrogenase enzyme in lucerne (Medicago sativa L.)
Plant Molecular Biology
Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L.
Plant Physiology
Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants
The Plant Journal
An Arabidopsis mutant defective in the general phenylpropanoid pathway
The Plant Cell
The sapwood-heartwood transition
Australian Forestry
A gene encoding caffeoyl coenzyme A 3-O-methyltransferase (CCoAOMT) from Populus trichocarpa (Accession No. AJ223621)
Plant Physiology
Evidence for a novel biosynthetic pathway that regulates the ratio of syringyl to guaiacyl residues in lignin in the differentiating xylem of Magnolia kobus DC
Planta
Studies on lignin and related compounds. LIX. Aromatic aldehydes from plant materials
Journal of the American Chemical Society
Natural products (secondary metabolites)
Phenylpropanoid metabolismbiosynthesis of monolignols, lignans and neolignans, lignins and suberins
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Norman G. Lewis is the Director of the Institute of Biological Chemistry and the Arthur M. and Katie Eisig-Tode Distinguished Professor at Washington State University. He was initially trained in Chemistry (BSc Honors, 1973, University of Strathclyde) before completing a PhD (1977) in organic chemistry (alkaloid biosynthesis) at the University of British Columbia (Vancouver, BC). Postdoctoral training was in alkaloid/Vitamin B12 biosynthesis with Sir Alan R. Battersby. Professor Lewis' current research interests are mainly associated with biosynthesis of plant phenolics, including how their ordered deposition into various cell wall types is achieved. He is a Regional Editor of Phytochemistry, as well as serving on other editorial boards.
Aldwin M. Anterola holds a PhD (2001) degree in Plant Physiology from Washington State University. He graduated cum laude from the University of the Philippines, with a BS Degree in Agricultural Chemistry (1994). He worked for a year in the same University, as a junior faculty teaching laboratory classes in general chemistry, organic chemistry and biochemistry. As a graduate student, he received the Helen and Loyal H. Davis Fellowship, a Student Award for Best Paper from the Phytochemical Society of North America, and an American Chemical Society (Cellulose and Paper Division) Graduate Student Award for his research. He currently works as a Scientific Editor for Phytochemistry, and as a part-time Postdoctoral Research Associate in the co-author's laboratory.