Reassessment of effects on lignification and vascular development in the irx4 Arabidopsis mutant

Patten, Ann M.; Cardenas, Claudia L.; Cochrane, Fiona C.; Laskar, Dhrubojyoti D.; Bedgar, Diana L.; Davin, Laurence B.; Lewis, Norman G.

doi:10.1016/j.phytochem.2004.12.016

Cited by 57 publications

(106 citation statements)

References 47 publications

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“…A higher ratio was observed on antisense repression of CCR in tobacco (15,31), no change was recorded in poplar (28), and a decreased ratio was found in irx4 Arabidopsis mutants (19). Developmental stage and growth conditions affect the S/G ratio in Arabidopsis ccr1 mutants (19,26,30), and the decreased S/G ratio in Medicago ccr1 mutants also might be caused by their delayed development. The increased S/G ratio in Medicago ccr2 mutants resulted primarily from decreased G unit levels, perhaps because CCR2 is expressed mainly in xylem vessels, which have little S lignin.…”

Section: Discussionmentioning

confidence: 93%

“…To address further the functions of CCR1 and CCR2 in lignin biosynthesis, we tried to complement the Arabidopsis irregular xylem gene 4 (irx4) ccr1 mutant with each of the two Medicago genes under control of the constitutive 35S promoter. The irx4 mutation in ecotype Landsberg erecta (Ler) is a point mutation in the splice site sequence in the second intron of AtCCR1, a gene known to be involved in lignin biosynthesis (19,25,26). More than 20 independent transformants were obtained for each transgene, and the expression of Medicago CCR1 or CCR2 was confirmed by RT-PCR with the primers listed in Table S2 (Fig.…”

Section: Complementation Of Arabidopsis Ccr1 Mutants With Medicago Ccr1mentioning

confidence: 99%

“…The Arabidopsis genome possesses 11 annotated CCR homologs (16), two of which, CCR1 and CCR2, encode true CCR enzymes (17). CCRs from poplar (18), Arabidopsis (19), and tomato prefer feruloyl CoA as substrate, with caffeoyl CoA a poor substrate. Here we report the characterization of a CCR from Medicago truncatula with strong preference for caffeoyl CoA and provide evidence for its role in a route to monolignol biosynthesis that by-passes the methylation/reduction steps catalyzed by CCoAOMT and CCR1.…”

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confidence: 99%

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Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula

Zhou

Jackson

Shadle³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

103

124

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Cinnamoyl CoA reductases (CCR) convert hydroxycinnamoyl CoA esters to their corresponding cinnamyl aldehydes in monolignol biosynthesis. We identified two CCR genes in the model legume Medicago truncatula. CCR1 exhibits preference for feruloyl CoA, but CCR2 prefers caffeoyl and 4-coumaroyl CoAs, exhibits sigmoidal kinetics with these substrates, and is substrate-inhibited by feruloyl and sinapoyl CoAs. M. truncatula lines harboring transposon insertions in CCR1 exhibit drastically reduced growth and lignin content, whereas CCR2 knockouts grow normally with moderate reduction in lignin levels. CCR1 fully and CCR2 partially complement the irregular xylem gene 4 CCR mutation of Arabidopsis. The expression of caffeoyl CoA 3-O-methyltransferase (CCoAOMT) is up-regulated in CCR2 knockout lines; conversely, knockout of CCoAOMT up-regulates CCR2. These observations suggest that CCR2 is involved in a route to monolignols in Medicago whereby coniferaldehyde is formed via caffeyl aldehyde which then is 3-Omethylated by caffeic acid O-methyltransferase.

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Section: Discussionmentioning

confidence: 93%

Section: Complementation Of Arabidopsis Ccr1 Mutants With Medicago Ccr1mentioning

confidence: 99%

mentioning

confidence: 99%

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Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula

Zhou

Jackson

Shadle³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

103

124

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“…It is noteworthy that, in addition to HCT itself, genes directly downstream of HCT, namely C3H, CCR, and CCoAOMT, are those whose repression has been shown to have the strongest impact on plant growth (Piquemal et al, 1998;Jones et al, 2001;Pinç on et al, 2001aPinç on et al, , 2001bFranke et al, 2002;Goujon et al, 2003;Abdulrazzak et al, 2005;Patten et al, 2005). HCT repression had a particularly strong impact on growth, likely due to its double role in lignin biosynthesis upstream and downstream of the C3H step (see Figure 1).…”

Section: Discussionmentioning

confidence: 99%

Flavonoid Accumulation in Arabidopsis Repressed in Lignin Synthesis Affects Auxin Transport and Plant Growth

et al. 2007

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In Arabidopsis thaliana, silencing of hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT), a lignin biosynthetic gene, results in a strong reduction of plant growth. We show that, in HCT-silenced plants, lignin synthesis repression leads to the redirection of the metabolic flux into flavonoids through chalcone synthase activity. Several flavonol glycosides and acylated anthocyanin were shown to accumulate in higher amounts in silenced plants. By contrast, sinapoylmalate levels were barely affected, suggesting that the synthesis of that phenylpropanoid compound might be HCTindependent. The growth phenotype of HCT-silenced plants was shown to be controlled by light and to depend on chalcone synthase expression. Histochemical analysis of silenced stem tissues demonstrated altered tracheary elements. The level of plant growth reduction of HCT-deficient plants was correlated with the inhibition of auxin transport. Suppression of flavonoid accumulation by chalcone synthase repression in HCT-deficient plants restored normal auxin transport and wildtype plant growth. By contrast, the lignin structure of the plants simultaneously repressed for HCT and chalcone synthase remained as severely altered as in HCT-silenced plants, with a large predominance of nonmethoxylated H units. These data demonstrate that the reduced size phenotype of HCT-silenced plants is not due to the alteration of lignin synthesis but to flavonoid accumulation.

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“…Similarly, as again revealed by thioacidolysis and NMR, in COMT-deficient angiosperms, the novel monomer 5-hydroxyconiferyl alcohol (partially) substitutes for the sinapyl alcohol whose production is thwarted, producing novel benzodioxane structures in the lignins (Jouanin et al, 2000;Marita et al, 2001Marita et al, , 2003Morreel et al, 2004;Ralph et al, 2001). Contrary to claims that incorporation of non-monolignol monomers has been 'unequivocally disproven' (Anterola and Lewis, 2002;Lewis, 1999;Patten et al, 2005), monomer substitution is well authenticated in lignification, and evidence continues to mount that natural and mutant/transgenic lignins may derive from quite an array of phenolic precursors Boudet, 1998;Lu et al, 2004;Ralph, 2006;Ralph et al, 2004bRalph et al, , 2007Ralph et al, , 2008Sederoff et al, 1999). The evidence presented here suggests that ferulic acid itself is a previously unrecognized monomer in lignification, being incorporated at low levels in various types of 'normal' plants, and at elevated levels in various CCR-deficient transgenics.…”

Section: Implications Of Ferulic Acid In Ligninmentioning

confidence: 96%

Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency)

Ralph¹,

Kim²,

Lu³

et al. 2007

The Plant Journal

116

133

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SummaryA molecular marker compound, derived from lignin by the thioacidolysis degradative method, for structures produced when ferulic acid is incorporated into lignin in angiosperms (poplar, Arabidopsis, tobacco), has been structurally identified as 1,2,2-trithioethyl ethylguaiacol [1-(4-hydroxy-3-methoxyphenyl)-1,2,2-tris(ethylthio)ethane]. Its truncated side chain and distinctive oxidation state suggest that it derives from ferulic acid that has undergone bis-8-O-4 (cross) coupling during lignification, as validated by model studies. A diagnostic contour for such structures is found in two-dimensional 13 C-1 H correlated (HSQC) NMR spectra of lignins isolated from cinnamoyl CoA reductase (CCR)-deficient poplar. As low levels of the marker are also released from normal (i.e. non-transgenic) plants in which ferulic acid may be present during lignification, notably in grasses, the marker is only an indicator for CCR deficiency in general, but is a reliable marker in woody angiosperms such as poplar. Its derivation, together with evidence for 4-O-etherified ferulic acid, strongly implies that ferulic acid is incorporated into angiosperm lignins. Its endwise radical coupling reactions suggest that ferulic acid should be considered an authentic lignin precursor. Moreover, ferulic acid incorporation provides a new mechanism for producing branch points in the polymer. The findings sharply contradict those reported in a recent study on CCR-deficient Arabidopsis.

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Reassessment of effects on lignification and vascular development in the irx4 Arabidopsis mutant

Cited by 57 publications

References 47 publications

Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula

Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula

Flavonoid Accumulation in Arabidopsis Repressed in Lignin Synthesis Affects Auxin Transport and Plant Growth

Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency)

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