Neighboring parenchyma cells contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous

Plant Cell

Volumn 25, Issue 10, 2013, Pages 3988-3999

  Smith, Rebecca A ^a,b   Schuetz, Mathias ^a,b   Roach, Melissa ^a   Mansfield, Shawn D ^a   Ellis, Brian ^b   Samuels, Lacey ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

ALDEHYDE DEHYDROGENASE; CINNAMOYL COA REDUCTASE; LIGNIN;

APOPTOSIS; ARABIDOPSIS; BIOSYNTHESIS; CELL WALL; CYTOLOGY; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT ROOT; PLANT STEM; TRANSGENIC PLANT; XYLEM;

ALDEHYDE OXIDOREDUCTASES; APOPTOSIS; ARABIDOPSIS; CELL WALL; GENE SILENCING; LIGNIN; PLANT ROOTS; PLANT STEMS; PLANTS, GENETICALLY MODIFIED; XYLEM;

EID: 84888426033     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.117176     Document Type: Article

References (61)

1. Alejandro, S., Lee, Y., Tohge, T., Sudre, D., Osorio, S., Park, J., Bovet, L., Lee, Y., Geldner, N., Fernie, A.R., and Martinoia, E. (2012). AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr. Biol. 22: 1207-1212.
2. Baghdady, A., Blervacq, A.S., Jouanin, L., Grima-Pettenati, J., Sivadon, P., and Hawkins, S. (2006). Eucalyptus gunnii CCR and CAD2 promoters are active in lignifying cells during primary and secondary xylem formation in Arabidopsis thaliana. Plant Physiol. Biochem. 44: 674-683.
3. Bednarek, P., Schneider, B., Svatos, A., Oldham, N.J., and Hahlbrock, K. (2005). Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiol. 138: 1058-1070.
4. Berthet, S., Demont-Caulet, N., Pollet, B., Bidzinski, P., Cézard, L., Le Bris, P., Borrega, N., Hervé, J., Blondet, E., Balzergue, S., Lapierre, C., and Jouanin, L. (2011). Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23: 1124-1137.
5. Bevan, M., Shufflebottom, D., Edwards, K., Jefferson, R., and Schuch, W. (1989). Tissue-and cell-specific activity of a phenylalanine ammonia-lyase promoter in transgenic plants. EMBO J. 8: 1899-1906.
6. Chapelle, A., Morreel, K., Vanholme, R., Le-Bris, P., Morin, H., Lapierre, C., Boerjan, W., Jouanin, L., and Demont-Caulet, N. (2012). Impact of the absence of stem-specific β-glucosidases on lignin and monolignols. Plant Physiol. 160: 1204-1217.
7. Chen, C., Meyermans, H., Burggraeve, B., De Rycke, R.M., Inoue, K., De Vleesschauwer, V., Steenackers, M., Van Montagu, M.C., Engler, G.J., and Boerjan, W.A. (2000). Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant Physiol. 123: 853-867.
8. Chong, J., Pierrel, M.A., Atanassova, R., Werck-Reichhart, D., Fritig, B., and Saindrenan, P. (2001). Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol. 125: 318-328.
9. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
10. Coleman, H.D., Park, J.Y., Nair, R., Chapple, C., and Mansfield, S.D. (2008). RNAi-mediated suppression of p-coumaroyl-CoA 39-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc. Natl. Acad. Sci. USA 105: 4501-4506.
11. Courtois-Moreau, C.L., Pesquet, E., Sjödin, A., Muñiz, L., Bollhöner, B., Kaneda, M., Samuels, L., Jansson, S., and Tuominen, H. (2009). A unique program for cell death in xylem fibers of Populus stem. Plant J. 58: 260-274.
12. Curtis, M.D., and Grossniklaus, U. (2003). A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469.
13. Feuillet, C., Lauvergeat, V., Deswarte, C., Pilate, G., Boudet, A., and Grima-Pettenati, J. (1995). Tissue-and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol. Biol. 27: 651-667.
14. Franke, R., Hemm, M.R., Denault, J.W., Ruegger, M.O., Humphreys, J.M., and Chapple, C. (2002a). Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 30: 47-59.
15. Franke, R., Humphreys, J.M., Hemm, M.R., Denault, J.W., Ruegger, M.O., Cusumano, J.C., and Chapple, C. (2002b). The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J. 30: 33-45.
16. Gorzsás, A., Stenlund, H., Persson, P., Trygg, J., and Sundberg, B. (2011). Cell-specific chemotyping and multivariate imaging by combined FT-IR microspectroscopy and orthogonal projections to latent structures (OPLS) analysis reveals the chemical landscape of secondary xylem. Plant J. 66: 903-914.
17. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M.R. (2010). A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64: 355-365.
18. Hauffe, K.D., Paszkowski, U., Schulze-Lefert, P., Hahlbrock, K., Dangl, J.L., and Douglas, C.J. (1991). A parsley 4CL-1 promoter fragment specifies complex expression patterns in transgenic tobacco. Plant Cell 3: 435-443.
19. Hemm, M.R., Rider, S.D., Ogas, J., Murry, D.J., and Chapple, C. (2004). Light induces phenylpropanoid metabolism in Arabidopsis roots. Plant J. 38: 765-778.
20. Hosokawa, M., Suzuki, S., Umezawa, T., and Sato, Y. (2001). Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol. 42: 959-968.
21. Humphreys, J.M., and Chapple, C. (2002). Rewriting the lignin roadmap. Curr. Opin. Plant Biol. 5: 224-229.
22. Jones, L., Ennos, A.R., and Turner, S.R. (2001). Cloning and characterization of irregular xylem4 (irx4): A severely lignin-deficient mutant of Arabidopsis. Plant J. 26: 205-216.
23. Kaneda, M., Rensing, K.H., Wong, J.C.T., Banno, B., Mansfield, S.D., and Samuels, A.L. (2008). Tracking monolignols during wood development in lodgepole pine. Plant Physiol. 147: 1750-1760.
24. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
25. Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and Demura, T. (2005). Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19: 1855-1860.
26. Lanot, A., Hodge, D., Jackson, R.G., George, G.L., Elias, L., Lim, E.K., Vaistij, F.E., and Bowles, D.J. (2006). The glucosyltransferase UGT72E2 is responsible for monolignol 4-O-glucoside production in Arabidopsis thaliana. Plant J. 48: 286-295.
27. Lee, Y., Rubio, M.C., Alassimone, J., and Geldner, N. (2013). A mechanism for localized lignin deposition in the endodermis. Cell 153: 402-412.
28. Leinhos, V., and Savidge, R.A. (1993). Isolation of protoplasts from developing xylem of Pinus banksiana and Pinus strobus. Can. J. For. Res. 23: 343-348.
29. Liu, C.J., Miao, Y.C., and Zhang, K.W. (2011). Sequestration and transport of lignin monomeric precursors. Molecules 16: 710-727.
30. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25: 402-408.
31. McDonnell, L.M. (2010). Investigating the Role of Cellulose Synthases in the Biosynthesis and Properties of Cellulose in Secondary Cell Walls. PhD dissertation (Vancouver, Canada: University of British Columbia).
32. Miao, Y.C., and Liu, C.J. (2010). ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc. Natl. Acad. Sci. USA 107: 22728-22733.
33. Mir Derikvand, M., Sierra, J.B., Ruel, K., Pollet, B., Do, C.T., Thévenin, J., Buffard, D., Jouanin, L., and Lapierre, C. (2008). Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227: 943-956.
34. Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19: 270-280.
35. Naseer, S., Lee, Y., Lapierre, C., Franke, R., Nawrath, C., and Geldner, N. (2012). Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc. Natl. Acad. Sci. USA 109: 10101-10106.
36. Ossowski, S., Schwab, R., and Weigel, D. (2008). Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53: 674-690.
37. Pesquet, E., Korolev, A.V., Calder, G., and Lloyd, C.W. (2010). The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr. Biol. 20: 744-749.
38. Pesquet, E., et al. (2013). Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25: 1314-1328.
39. Pickett-Heaps, J.D. (1968). Radiographic investigations using lignin precursors. Protoplasma 65: 181-205.
40. Roberts, A.W., Frost, A.O., Roberts, E.M., and Haigler, C.H. (2004). Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements. Protoplasma 224: 217-229.
41. Robinson, A.R., and Mansfield, S.D. (2009). Rapid analysis of poplar lignin monomer composition by a streamlined thioacidolysis procedure and near-infrared reflectance-based prediction modeling. Plant J. 58: 706-714.
42. Schilmiller, A.L., Stout, J., Weng, J.K., Humphreys, J., Ruegger, M.O., and Chapple, C. (2009). Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J. 60: 771-782.
43. Schoch, G., Goepfert, S., Morant, M., Hehn, A., Meyer, D., Ullmann, P., and Werck-Reichhart, D. (2001). CYP98A3 from Arabidopsis thaliana is a 39-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 276: 36566-36574.
44. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D. (2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133.
45. Sibout, R., and Höfte, H. (2012). Plant cell biology: The ABC of monolignol transport. Curr. Biol. 22: R533-R535.
46. Takabe, K., Fujita, M., Harada, H., and Saiki, H. (1985). Autoradiographic investigation of lignification in the cell walls of Cryptomeria (Cryptomeria Japonica D Don). Mokuzai Gakkaishi 31: 613-619.
47. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., and Turner, S.R. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. USA 100: 1450-1455.
48. Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R., and Turner, S.R. (1999). The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11: 769-780.
49. Terashima, N., Fukushima, K., He, L., and Takabe, K. (1993). Comprehensive model of the lignified plant cell wall. In Forage Cell Wall Structure and Digestibility, H.G. Jung, D.R. Buxton, R.D. Hatfield, and J. Ralph, eds (Madison, WI: ASA, CSSA, and SSSA), pp. 247-270.
50. Terashima, N., Fukushima, K., and Takabe, K. (1986). Heterogeneity in formation of lignin. VIII. An autoradiographic study on the formation of guaiacyl and syringyl lignin in Magnolia Kobus DC. Wood Sci. Technol. 40: 101-105.
51. Terashima, N., and Fukushima, K. (1988). Heterogeneity in formation of lignin. XI. An autoradiographic study of the heterogeneous formation and structure of pine lignin. Wood Sci. Technol. 22: 259-270.
52. Thévenin, J., Pollet, B., Letarnec, B., Saulnier, L., Gissot, L., Maia-Grondard, A., Lapierre, C., and Jouanin, L. (2011). The simultaneous repression of CCR and CAD, two enzymes of the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Mol. Plant 4: 70-82.
53. Tokunaga, N., Sakakibara, N., Umezawa, T., Ito, Y., Fukuda, H., and Sato, Y. (2005). Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol. 46: 224-232.
54. Turner, S.R., and Somerville, C.R. (1997). Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9: 689-701.
55. Vanholme, R., Demedts, B., Morreel, K., Ralph, J., and Boerjan, W. (2010). Lignin biosynthesis and structure. Plant Physiol. 153: 895-905.
56. Yamaguchi, M., Goué, N., Igarashi, H., Ohtani, M., Nakano, Y., Mortimer, J.C., Nishikubo, N., Kubo, M., Katayama, Y., Kakegawa, K., Dupree, P., and Demura, T. (2010a). VASCULARRELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol. 153: 906-914.
57. Yamaguchi, M., Ohtani, M., Mitsuda, N., Kubo, M., Ohme-Takagi, M., Fukuda, H., and Demura, T. (2010b). VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22: 1249-1263.
58. Yang, F., Mitra, P., Zhang, L., Prak, L., Verhertbruggen, Y., Kim, J.S., Sun, L., Zheng, K., Tang, K., Auer, M., Scheller, H.V., and Loqué, D. (2013). Engineering secondary cell wall deposition in plants. Plant Biotechnol. J. 11: 325-335.
59. Young, R.E., McFarlane, H.E., Hahn, M.G., Western, T.L., Haughn, G.W., and Samuels, A.L. (2008). Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 20: 1623-1638.
60. Zhong, R., Lee, C., and Ye, Z.H. (2010). Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. Trends Plant Sci. 15: 625-632.
61. Zhong, R., Richardson, E.A., and Ye, Z.H. (2007). Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225: 1603-1611.