Ectopic expression of a loblolly pine Class II 4-Coumarate:CoA ligase alters soluble phenylpropanoid metabolism but not lignin biosynthesis in Populus

Plant and Cell Physiology

Volumn 55, Issue 9, 2014, Pages 1669-1678

  Chen, Han Yi ^a,b   Babst, Benjamin A ^a,b,e   Nyamdari, Batbayar ^b,c   Hu, Hao ^b,c   Sykes, Robert ^d   Davis, Mark F ^d   Harding, Scott A ^a,b,c   Tsai, Chung Jui ^a,b,c  

^a MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c National Renewable Energy Laboratory ^*  (United States)

^d NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^e BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Cinnamic acid; Defense; Phenylpropanoid; Pinus; Populus

Indexed keywords

1-PHENYLPROPANOL; 4-COUMARATE-COA LIGASE; 4-COUMARIC ACID; COUMARIC ACID; ISOENZYME; LIGNIN; LONG CHAIN FATTY ACID COENZYME A LIGASE; PROPANOL; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PINE; PLANT LEAF; PLANT ROOT; POPULUS; XYLEM;

AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; COENZYME A LIGASES; COUMARIC ACIDS; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; LIGNIN; MOLECULAR SEQUENCE DATA; PHYLOGENY; PINUS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; POPULUS; PROPANOLS; SEQUENCE ANALYSIS, DNA; XYLEM;

EID: 84925482823     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu098     Document Type: Article

References (69)

1. Achnine, L., Blancaflor, E. B., Rasmussen, S. and Dixon, R. A. (2004) Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16:3098-3109.
2. Allina, S. M., Pri-Hadash, A., Theilmann, D. A., Ellis, B. E. and Douglas, C. J. (1998) 4-Coumarate: coenzyme A ligase in hybrid poplar: properties of native enzymes, cDNA cloning, and analysis of recombinant enzymes. Plant Physiol. 116:743-754.
3. Bassard, J.-E., Richert, L., Geerinck, J., Renault, H., Duval, F., Ullmann, P. et al. (2012) Protein-protein and protein-membrane associations in the lignin pathway. Plant Cell 24:4465-4482.
4. Becker-André, M., Schulze-Lefert, P. and Hahlbrock, K. (1991) Structural comparison, modes of expression, and putative cis-acting elements of the two 4-coumarate: CoA ligase genes in potato. J. Biol. Chem. 266:8551-8559.
5. Benfey, P. N., Ren, L. and Chua, N. H. (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J. 9:1677-1684.
6. Boerjan, W., Ralph, J. and Baucher, M. (2003) Lignin biosynthesis. Annu. Rev. Plant Biol. 54:519-546.
7. Bonello, P., Heller, W. and Sandermann, H. (1993) Ozone effects on rootdisease susceptibility and defence responses in mycorrhizal and nonmycorrhizal seedlings of Scots pine (Pinus sylvestris L.). New Phytol. 124:653-663.
8. Broun, P. (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr. Opin. Plant Biol. 8:272-279.
9. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.
10. Chen, H.-C., Li, Q., Shuford, C. M., Liu, J., Muddiman, D. C., Sederoff, R. R. et al. (2011) Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis. Proc. Natl Acad. Sci. USA 108:21253-21258.
11. Chen, H.-C., Song, J., Williams, C. M., Shuford, C. M., Liu, J., Wang, J. P. et al. (2013) Monolignol pathway 4-coumaric acid: coenzyme A ligases in Populus trichocarpa: Novel specificity, metabolic regulation, and simulation of coenzyme A ligation fluxes. Plant Physiol. 161:1501-1516.
12. Chiron, H., Drouet, A., Lieutier, F., Payer, H.-D., Ernst, D. and Sandermann, H. (2000) Gene induction of stilbene biosynthesis in Scots pine in response to ozone treatment, wounding, and fungal infection. Plant Physiol. 124:865-872.
13. Costa, M. A., Bedgar, D. L., Moinuddin, S. G. A., Kim, K.-W., Cardenas, C. L., Cochrane, F. C. et al. (2005) Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation. Phytochemistry 66:2072-2091.
14. Cukovic, D., Ehlting, J., Van Ziffle, J. A. and Douglas, C. J. (2001) Structure and evolution of 4-coumarate: coenzyme A ligase (4CL) gene families. Biol. Chem. 382:645-654.
15. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F. et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469.
16. Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., Reddy, M. S. S. and Wang, L. J. (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol. Plant Pathol. 3:371-390.
17. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
18. Ehlting, J., Büttner, D., Wang, Q., Douglas, C. J., Somssich, I. E. and Kombrink, E. (1999) Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 19:9-20.
19. Friedmann, M., Ralph, S. G., Aeschliman, D., Zhuang, J., Ritland, K., Ellis, B. E. et al. (2007) Microarray gene expression profiling of developmental transitions in Sitka spruce (Picea sitchensis) apical shoots. J. Exp. Bot. 58:593-614.
20. Gehlert, R., Schoppner, A. and Kindl, H. (1990) Stilbene synthase from seedlings of Pinus sylvestris: purification and induction in response to fungal infection. Mol. Plant Microbe Interact. 3:444-449.
21. Gui, J., Shen, J. and Li, L. (2011) Functional characterization of evolutionarily divergent 4-coumarate: coenzyme A ligases in rice. Plant Physiol. 157:574-586.
22. Hahlbrock, K. and Grisebach, H. (1979) Enzymic controls in the biosynthesis of lignin and flavonoids. Annu. Rev. Plant Physiol. 30:105-130.
23. Hamberger, B., Ellis, M., Friedmann, M., De Azevedo Souza, C., Barbazuk, B. and Douglas, C. J. (2007) Genome-wide analyses of phenylpropanoidrelated genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can. J. Bot. 85:1182-1201.
24. Hamberger, B. and Hahlbrock, K. (2004) The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc. Natl Acad. Sci. USA 101:2209-2214.
25. Harding, S. A., Jarvie, M. M., Lindroth, R. L. and Tsai, C.-J. (2009) A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones. J. Exp. Bot. 60:3443-3452.
26. Harding, S. A., Leshkevich, J., Chiang, V. L. and Tsai, C. J. (2002) Differential substrate inhibition couples kinetically distinct 4-coumarate: coenzyme A ligases with spatially distinct metabolic roles in quaking aspen. Plant Physiol. 128:428-438.
27. Harding, S. A., Xue, L.-J., Du, L., Nyamdari, B., Lindroth, R. L., Sykes, R. et al. (2014) Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense and growth in Populus. Tree Physiol. (in press).
28. Hoffmann, L., Maury, S., Martz, F., Geoffroy, P. and Legrand, M. (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J. Biol. Chem. 278:95-103.
29. Holsters, M., Dewaele, D., Depicker, A., Messens, E., Vanmontagu, M. and Schell, J. (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol. Gen. Genet. 163:181-187.
30. Hu, W.-J., Kawaoka, A., Tsai, C.-J., Lung, J., Osakabe, K., Ebinuma, H. et al. (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proc. Natl Acad. Sci. USA 95:5407-5412.
31. Hu, W. J., Harding, S. A., Lung, J., Popko, J. L., Ralph, J., Stokke, D. D. et al. (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat. Biotechnol. 17:808-812.
32. Huang, X. and Madan, A. (1999) CAP3: a DNA sequence assembly program. Genome Res. 9:868-877.
33. Hudgins, J. W. and Franceschi, V. R. (2004) Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiol. 135:2134-2149.
34. Jørgensen, K., Rasmussen, A. V., Morant, M., Nielsen, A. H., Bjarnholt, N., Zagrobelny, M. et al. (2005) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8:280-291.
35. Kajita, S., Hishiyama, S., Tomimura, Y., Katayama, Y. and Omori, S. (1997) Structural characterization of modified lignin in transgenic tobacco plants in which the activity of 4-coumarate: coenzyme A ligase is depressed. Plant Physiol. 114:871-879.
36. Kao, Y. Y., Harding, S. A. and Tsai, C. J. (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol. 130:796-807.
37. Kind, T., Wohlgemuth, G., Lee, D. Y., Lu, Y., Palazoglu, M., Shahbaz, S. et al. (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal. Chem. 81:10038-10048.
38. Kodan, A., Kuroda, H. and Sakai, F. (2002) A stilbene synthase from Japanese red pine (Pinus densiflora): implications for phytoalexin accumulation and down-regulation of flavonoid biosynthesis. Proc. Natl Acad. Sci. USA 99:3335-3339.
39. Koutaniemi, S., Warinowski, T., Kärkönen, A., Alatalo, E., Fossdal, C., Saranpää, P. et al. (2007) Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Mol. Biol. 65:311-328.
40. Lee, D. and Douglas, C. J. (1996) Two divergent members of a tobacco 4-coumarate: coenzyme A ligase (4CL) gene family-cDNA structure, gene inheritance and expression, and properties of recombinant proteins. Plant Physiol. 112:193-205.
41. 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.
42. Lindermayr, C., Mollers, B., Fliegmann, J., Uhlmann, A., Lottspeich, F., Meimberg, H. et al. (2002) Divergent members of a soybean (Glycine max L.) 4-coumarate: coenzyme A ligase gene family-primary structures, catalytic properties, and differential expression. Eur. J. Biochem. 269:1304-1315.
43. Meilan, R. and Ma, C. (2006) Poplar (Populus spp.). Methods Mol. Biol. 344, 143-151.
44. Meng, H. B. and Campbell, W. H. (1997) Facile enzymic synthesis of caffeoyl-CoA. Phytochemistry 44:605-608.
45. Miller, M. A., Pfeiffer, W. and Schwartz, T. (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE). pp. 1-8, New Orleans, LA.
46. Mochamad Afendi, F., Okada, T., Yamazaki, M., Hirai-Morita, A., Nakamura, Y., Nakamura, K. et al. (2011) KNApSAcK family databases: integrated metabolite-plant species databases for multifaceted plant researches. Plant Cell Physiol. 53:e1.
47. Nagy, N. E., Franceschi, V. R., Solheim, H., Krekling, T. and Christiansen, E. (2000) Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Amer. J. Bot. 87:302-313.
48. Novaes, E., Osorio, L., Drost, D. R., Miles, B. L., Boaventura-Novaes, C. R. D., Benedict, C. et al. (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol. 182:878-890.
49. Nystedt, B., Street, N. R., Wetterbom, A., Zuccolo, A., Lin, Y. C., Scofield, D. G. et al. (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579-584.
50. Pitre, F. E., Pollet, B., Lafarguette, F., Cooke, J. E. K., MacKay, J. J. and Lapierre, C. (2007) Effects of increased nitrogen supply on the lignification of poplar wood. J. Agric. Food Chem. 55:10306-10314.
51. Preisig-Muller, R., Schwekendiek, A., Brehm, I., Reif, H. J. and Kindl, H. (1999) Characterization of a pine multigene family containing elicitor-responsive stilbene synthase genes. Plant Mol. Biol. 39:221-229.
52. Saballos, A., Sattler, S. E., Sanchez, E., Foster, T. P., Xin, Z., Kang, C. et al. (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). Plant J. 70:818-830.
53. Samac, D., Tesfaye, M., Dornbusch, M., Saruul, P. and Temple, S. (2004) A comparison of constitutive promoters for expression of transgenes in alfalfa (Medicago sativa). Transgenic Res. 13:349-361.
54. Schoch, G., Goepfert, S., Morant, M., Hehn, A., Meyer, D., Ullmann, P. et al. (2001) CYP98A3 from Arabidopsis thaliana is a 3'-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 276:36566-36574.
55. Shi, R., Sun, Y.-H., Li, Q., Heber, S., Sederoff, R. and Chiang, V. L. (2010) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol. 51:144-163.
56. Silber, M. V., Meimberg, H. and Ebel, J. (2008) Identification of a 4-coumarate:CoA ligase gene family in the moss, Physcomitrella patens. Phytochemistry 69:2449-2456.
57. Sluiter, J. B., Ruiz, R. O., Scarlata, C. J., Sluiter, A. D. and Templeton, D. W. (2010) Compositional analysis of lignocellulosic feedstocks. 1. Review and description of methods. J. Agric. Food Chem. 58:9043-9053.
58. Sykes, R., Yung, M., Novaes, E., Kirst, M., Peter, G. and Davis, M. (2009) High-throughput screening of plant cell-wall composition using pyrolysis molecular beam mass spectroscopy. Methods Mol. Biol. 581:169-183.
59. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
60. Tsai, C. J., Harding, S. A., Tschaplinski, T. J., Lindroth, R. L. and Yuan, Y. (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol. 172:47-62.
61. Vanholme, R., Demedts, B., Morreel, K., Ralph, J. and Boerjan, W. (2010) Lignin biosynthesis and structure. Plant Physiol. 153:895-905.
62. Vogt, T. (2010) Phenylpropanoid biosynthesis. Mol. Plant 3:2-20.
63. Voo, K. S., Whetten, R. W., O'Malley, D. M. and Sederoff, R. R. (1995) 4-Coumarate: coenzyme A ligase from loblolly pine xylem. Plant Physiol. 108:85-97.
64. Wagner, A., Donaldson, L., Kim, H., Phillips, L., Flint, H., Steward, D. et al. (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol. 149:370-383.
65. Wang, H.-Q., Tuominen, L. K. and Tsai, C.-J. (2011) SLIM: a sliding linear model for estimating the proportion of true null hypotheses in datasets with dependence structures. Bioinformatics 27:225-231.
66. Winkel, B. S. J. (2004) Metabolic channeling in plants. Annu. Rev. Plant Biol. 55:85-107.
67. Xue, L., Guo, W., Yuan, Y., Anino, E. O., Nyamdari, B., Wilson, M. C. et al. (2013) Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state, but not growth in transgenic Populus. Plant Cell 25:2714-2730.
68. Zhang, X. H. and Chiang, V. L. (1997) Molecular cloning of 4-coumarate: coenzyme A ligase in loblolly pine and the roles of this enzyme in the biosynthesis of lignin in compression wood. Plant Physiol. 113:65-74.
69. Zimin, A., Stevens, K. A., Crepeau, M. W., Holtz-Morris, A., Koriabine, M., Marçais, G. et al. (2014) Sequencing and assembly of the 22-Gb loblolly pine genome. Genetics 196:875-890.