Abstract
The involvement of the maize ZmMYB42 R2R3-MYB factor in the phenylpropanoid pathway and cell wall structure and composition was investigated by overexpression in Arabidopsis thaliana. ZmMYB42 down-regulates several genes of the lignin pathway and this effect reduces the lignin content in all lignified tissues. In addition, ZmMYB42 plants generate a lignin polymer with a decreased S to G ratio through the enrichment in H and G subunits and depletion in S subunits. This transcription factor also regulates other genes involved in the synthesis of sinapate esters and flavonoids. Furthermore, ZmMYB42 affects the cell wall structure and degradability, and its polysaccharide composition. Together, these results suggest that ZmMYB42 may be part of the regulatory network controlling the phenylpropanoid biosynthetic pathway.
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References
Albersheim P, Nevins DS, English PD (1967) A method for the analysis of sugars in plant cell wall polysaccharides by gas liquid chromatography. Carbohydr Res 5:340–345. doi:10.1016/S0008-6215(00)80510-8
Arnaud D, Déjardin A, Leplé JC, Lesage-Descauses MC, Pilate G (2007) Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res 14:103–116. doi:10.1093/dnares/dsm013
Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162. doi:10.1105/tpc.106.044495
Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489. doi:10.1016/0003-2697(73)90377-1
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. doi:10.1146/annurev.arplant.54.031902.134938
Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JE, Blais S, Tremblay L, Morency MJ, Pavy N, Grima-Pettenati J, Séguin A, Mackay J (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59:3925–3939. doi:10.1093/jxb/ern234
Bonke M, Thitamadee S, Mähönen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426:181–186. doi:10.1038/nature02100
Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535. doi:10.1104/pp.126.2.524
Carlsbecker A, Helariutta Y (2005) Phloem and xylem specification: pieces of the puzzle emerge. Curr Opin Plant Biol 8:512–517. doi:10.1016/j.pbi.2005.07.001
Cliff MA, King MC, Schlosser J (2007) Anthocyanin, phenolic composition, colour measurement and sensory analysis of BC commercial red wines. Food Res Int 40:92–100. doi:10.1016/j.foodres.2006.08.002
Cone KC, Cocciolone SM, Burr FA, Burr B (1993) Maize anthocyanin regulatory gene pI is a duplicate of c1 that functions in the plant. Plant Cell 5:1795–1805
Day A, Ruel K, Neutelings G, Crônier D, David H, Hawkins S, Chabbert B (2005) Lignification in the flax stem: evidence for an unusual lignin in bast fibers. Planta 222:234–245. doi:10.1007/s00425-005-1537-1
Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Mérillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140:499–511. doi:10.1104/pp.105.067231
Dische J (1962) Color reactions of carbohydrates. In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry, vol 1. Academic Press, New York, pp 475–514
Do CT, Pollet B, Thévenin J, Sibout R, Denoue D, Barrière Y, Lapierre C, Jouanin L (2007) Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 226:1117–1129. doi:10.1007/s00425-007-0558-3
Dubois M, Giles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method of determination of sugars and related substances. Anal Chem 28:350–356. doi:10.1021/ac60111a017
Encina A, Sevillano JM, Acebes JL, Alvarez J (2002) Cell wall modifications of bean (Phaseolus vulgaris) cell suspensions during habituation and dehabituation to dichlobenil. Physiol Plant 114:182–191. doi:10.1034/j.1399-3054.2002.1140204.x
Fornalé S, Sonbol FM, Maes T, Capellades M, Puigdomenech P, Rigau J, Caparrós-Ruiz D (2006) Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors. Plant Mol Biol 62:809–823. doi:10.1007/s11103-006-9058-2
Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C (2002) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30:33–45. doi:10.1046/j.1365-313X.2002.01266.x
Franken P, Schrell S, Peterson PA, Saedler H, Wienand U (1989) Molecular analysis of protein domain function encoded by the myb-homologous maize genes C1, Zm 1 and Zm 38. Plant J 6:21–30. doi:10.1046/j.1365-313X.1994.6010021.x
Gális I, Simek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K (2006) A novel R2R3-MYB transcription factor NtMYBJS1 is a methyl Jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. Plant J 46:573–592. doi:10.1111/j.1365-313X.2006.02719.x
Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati G (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567. doi:10.1111/j.1365-313X.2005.02480.x
Goujon T, Sibout R, Pollet B, Maba B, Nussaume L, Bechtold N, Lu F, Ralph J, Mila I, Barrière Y, Lapierre C, Jouanin L (2003) A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapoyl esters. Plant Mol Biol 51:973–989. doi:10.1023/A:1023022825098
Grotewold E, Athma P, Peterson T (1991) Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc Natl Acad Sci USA 88:4587–4591. doi:10.1073/pnas.88.11.4587
Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553. doi:10.1016/0092-8674(94)90117-1
Heddges JI, Mann DC (1979) The characterization of plant tissues by their lignin oxidation products. Geochim Cosmochim Acta 43:1803–1807. doi:10.1016/0016-7037(79)90028-0
Heine GF, Malik V, Dias AP, Grotewold E (2007) Expression and molecular characterization of ZmMYB-IF35 and related R2R3-MYB transcription factors. Mol Biotechnol 37:155–164. doi:10.1007/s12033-007-0061-x
Hemm MR, Herrmann KM, Chapple C (2001) AtMYB4: a transcription factor general in the battle against UV. Trends Plant Sci 6:135–136. doi:10.1016/S1360-1385(01)01915-X
Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241:346–349. doi:10.1126/science.241.4863.346
Jia L, Clegg MT, Jiang T (2004) Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol 134:575–585. doi:10.1104/pp.103.027201
Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 15:6150–6161. doi:10.1093/emboj/19.22.6150
Ju C, Zhang F, Gao Y, Zhang W, Yan J, Dai J, Li J (2006) Cloning, chromosome mapping and expression analysis of an R2R3-MYB gene under-expressed in maize hybrid. Mol Biol Rep 33:103–110. doi:10.1007/s11033-006-0016-5
Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol 56:255–270. doi:10.1007/s11103-004-3354-5
Kawaoka A, Ebinuma H (2001) Transcriptional control of lignin biosynthesis by tobacco LIM protein. Phytochemistry 57:1149–1157. doi:10.1016/S0031-9422(01)00054-1
Kirk TK, Obst JR (1988) Lignin determination. Methods Enzymol 161:87–100. doi:10.1016/0076-6879(88)61014-7
Kögel I, Bochter R (1985) Characterization of lignin in forest humus layers by high-performance liquid chromatography of cupric oxide oxidation products. Soil Biol Biochem 17:637–640. doi:10.1016/0038-0717(85)90040-9
Legay S, Lacombe E, Goicoechea M, Briere C, Seguin A, Mackay J, Grima-Pettenati J (2007) Molecular characterization of EgMYB1, a putative transcriptional repressor of the lignin biosynthetic pathway. Plant Sci 173:542–549. doi:10.1016/j.plantsci.2007.08.007
Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496. doi:10.1146/annurev.pp.41.060190.002323
Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171–179
Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54:569–581. doi:10.1111/j.1365-313X.2008.03457.x
Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206. doi:10.1016/j.cub.2005.06.041
Marita JM, Ralph J, Hatfield RD, Chapple C (1999) NMR characterization of lignins in Arabidopsis altered in the activity of ferulate 5-hydroxylase. Proc Natl Acad Sci USA 96:12328–12332. doi:10.1073/pnas.96.22.12328
Marocco A, Wissenbach M, Becker D, Paz-Ares J, Saedler H, Salamini F, Rohde W (1989) Multiple genes are transcribed in Hordeum vulgare and Zea mays that carry the DNA binding domain of the myb oncoproteins. Mol Gen Genet 216:183–187. doi:10.1007/BF00334354
Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trends Genet 13:67–73. doi:10.1016/S0168-9525(96)10049-4
Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17:2088–2093. doi:10.1101/gad.1120003
Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:239–274. doi:10.1023/A:1010699919325
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Nair RB, Bastress KL, Ruegger MO, Denault JW, Chapple C (2004) The Arabidopsis thaliana REDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell 16:544–554. doi:10.1105/tpc.017509
Newman LJ, Perazza DE, Juda L, Campbell MM (2004) Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. Plant J 37:239–250
Patzlaff A, Newman LJ, Dubos C, Whetten RW, Smith C, McInnis S, Bevan MW, Sederoff RR, Campbell MM (2003a) Characterisation of Pt MYB1, an R2R3-MYB from pine xylem. Plant Mol Biol 53:597–608. doi:10.1023/B:PLAN.0000019066.07933.d6
Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003b) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754. doi:10.1046/j.1365-313X.2003.01916.x
Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6:3553–3558
Pérez-Jiménez J, Saura-Calixto F (2008) Anti-oxidant capacity of dietary polyphenols determined by ABTS assay: a kinetic expression of the results. Int J Food Sci Technol 43:185–191
Pilu R, Piazza P, Petroni K, Ronchi A, Martin C, Tonelli C (2003) pl-bol3, a complex allele of the anthocyanin regulatory pl1 locus that arose in a naturally occurring maize population. Plant J 36:510–521. doi:10.1046/j.1365-313X.2003.01898.x
Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995. doi:10.1111/j.1365-313X.2004.02280.x
Rabinowicz PD, Braun EL, Wolfe AD, Bowen B, Grotewold E (1999) Maize R2R3 Myb genes: sequence analysis reveals amplification in the higher plants. Genetics 153:427–444
Ralph J, Kim H, Lu F, Grabber JH, Leplé JC, Berrio-Sierra J, Derikvand MM, Jouanin L, Boerjan W, Lapierre C (2008) 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). Plant J 53:368–379. doi:10.1111/j.1365-313X.2007.03345.x
Rasband WS (2007) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA. http://rsb.info.nih.gov/ij/, 1997–2004
Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J (1998) More than 80 R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14:273–284. doi:10.1046/j.1365-313X.1998.00113.x
Ruegger M, Meyer K, Cusumano JC, Chapple C (1999) Regulation of ferulate-5-hydroxylase expression in Arabidopsis in the context of sinapate ester biosynthesis. Plant Physiol 119:101–110. doi:10.1104/pp.119.1.101
Ruel K, Comtat J, Barnoud F (1977) Localisation histologique et ultrastructurale des xylanes dans les parois primaires des tissus d’ Arundo donax. C R Acad Sci Gen 284:1421–1424
Ruel K, Chabannes M, Boudet AM, Legrand M, Joseleau JP (2001) Reassessment of qualitative changes in lignification of transgenic tobacco plants and their impact on cell wall assembly. Phytochemistry 57:1–9. doi:10.1016/S0031-9422(01)00118-2
Saeman JF, Moore WE, Millet MA (1963) Sugar units present. In: Whistler RL (ed) Methods in carbohydrate chemistry, vol 3. Academic Press, New York, pp 54–69
Sibout R, Eudes A, Pollet B, Goujon T, Mila I, Granier F, Séguin A, Lapierre C, Jouanin L (2003) Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis. Isolation and characterization of the corresponding mutants. Plant Physiol 132:848–860. doi:10.1104/pp.103.021048
Sticklen MB (2008) Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol. Nat Rev Genet 9:433–443. doi:10.1038/nrg2336
Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456. doi:10.1016/S1369-5266(00)00199-0
Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C (1998a) The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–154
Tamagnone L, Merida A, Stacey N, Plaskitt K, Parr A, Chang CF, Lynn D, Dow JM, Roberts K, Martin C (1998b) Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell 10:1801–1816
Torney F, Moeller L, Scarpa A, Wang K (2007) Genetic engineering approaches to improve bioethanol production from maize. Curr Opin Biotechnol 18:193–199. doi:10.1016/j.copbio.2007.03.006
Updegraff DM (1969) Semi-micro determination of cellulose in biological materials. Anal Biochem 32:420–424. doi:10.1016/S0003-2697(69)80009-6
Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:1–8. doi:10.1016/j.pbi.2008.03.005
Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124. doi:10.1007/s11103-005-2910-y
Zhong R, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572. doi:10.1016/j.pbi.2007.09.001
Acknowledgements
This work received financial support from the CONSOLIDER-INGENIO programme (CSD2007-00036) from the Spanish Ministerio de Ciencia e Innovación. F.M. Sonbol was financed by the European Project INCO-II (ICA4-CT-2000-30017), by the CRAG laboratory, and by the “Instituto de Cooperación con el Mundo Árabe, Agencia Española de Cooperación Internacional”. S. Fornale was financed by a post-doctoral grant from the “Generalitat de Catalunya” (2003PIV-A-00033) and by an I3P contract from the “Consejo Superior de Investigaciones Científicas”. D. Caparrós-Ruiz was financed by the Spanish “Ministerio de Educación y Ciencia” (“Ramón y Cajal” Program). This work was carried out within the framework of the “Xarxa de Referència de Biotecnologia” (XarBa) from the Autonomous Government of Catalonia. We are indebted to Dr. Jean-Paul Joseleau (CERMAV-CNRS Grenoble) and Dr. Cathie R. Martin (John Innes Center) for critical reading of the manuscript. We also thank the sequencing and greenhouse teams of IBMB-CSIC as well as Dr. R.S. Joshi for the English revision of the manuscript.
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Fathi-Mohamed Sonbol and Silvia Fornalé contributed equally to this work.
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Sonbol, FM., Fornalé, S., Capellades, M. et al. The maize ZmMYB42 represses the phenylpropanoid pathway and affects the cell wall structure, composition and degradability in Arabidopsis thaliana . Plant Mol Biol 70, 283–296 (2009). https://doi.org/10.1007/s11103-009-9473-2
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DOI: https://doi.org/10.1007/s11103-009-9473-2