The gene expression and enzymatic activity of pinoresinol-lariciresinol reductase during wood formation in Taiwania cryptomerioides Hayata

References

Adlercreutz, H. (2007) Lignans and human health. Crit. Rev. Clin. Lab. Sci. 44:483–525.10.1080/10408360701612942Search in Google Scholar

Bayindir, Ü., Alfermann, A.W., Fuss, E. (2008) Hinokinin biosynthesis in Linum corymbulosum Reichenb. Plant J. 55:810–820.10.1055/s-0028-1084838Search in Google Scholar

Bergstrom, B. (2003) Chemical and structural changes during heartwood formation in Pinus sylvestris. Forestry 76:45–53.10.1093/forestry/76.1.45Search in Google Scholar

Bolger, A.M., Lohse, M., Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.10.1093/bioinformatics/btu170Search in Google Scholar

Bugos, R.C., Chiang, V.L., Zhang, X.H., Campbell, E.R., Podila, G.K., Campbell, W.H. (1995) RNA isolation from plant tissues recalcitrant to extraction in guanidine. Biotechniques 19:734–737.Search in Google Scholar

Burlat, V., Kwon, M., Davin, L.B., Lewis, N.G. (2001) Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry 57:883–897.10.1016/S0031-9422(01)00117-0Search in Google Scholar

Celedon, J.M., Chiang, A., Yuen, M.M.S., Diaz-Chavez, M.L., Madilao, L.L., Finnegan, P.M., Barbour, E.L., Bohlmann, J. (2016) Heartwood-specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)-santalol fragrance biosynthesis. Plant J. 86:289–299.10.1111/tpj.13162Search in Google Scholar

Chang, S., Puryear, J., Cairney, J. (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11:113–116.10.1007/BF02670468Search in Google Scholar

Chang, S.T., Wang, S.Y., Su, Y.C., Huang, S.L., Kuo, Y.H. (1999) Chemical constituents and mechanisms of discoloration of Taiwania (Taiwania cryptomerioides Hayata) heartwood – 1. The structure reconfirmation and conversion mechanism of taiwanin A. Holzforschung 53:142–146.10.1515/HF.1999.023Search in Google Scholar

Chang, S.T., Wang, D.S.Y., Wu, C.L., Shiah, S.G., Kuo, Y.H., Chang, C.J. (2000) Cytotoxicity of extractives from Taiwania cryptomerioides heartwood. Phytochemistry 55:227–232.10.1016/S0031-9422(00)00275-2Search in Google Scholar

Chang, S.T., Wang, S.Y., Kuo, Y.H. (2003) Resources and bioactive substances from Taiwania (Taiwania cryptomerioides). J. Wood Sci. 49:1–4.10.1007/s100860300000Search in Google Scholar

Chen, R.B., Li, Q., Tan, H.X., Chen, J., Xiao, Y., Ma, R., Gao, S., Zerbe, P., Chen, W., Zhang, L. (2015) Gene-to-metabolite network for biosynthesis of lignans in MeJA-elicited Isatis indigotica hairy root cultures. Front. Plant Sci. 6:952.10.3389/fpls.2015.00952Search in Google Scholar

Cheng, H., Li, L.L., Xu, F., Wang, Y., Yuan, H.H., Wu, C.H., Wang, S.B., Liao, Z.Q., Hua, J., Wang, Y.P., Cheng, S.Y., Cao, F.L. (2013) Expression patterns of an isoflavone reductase-like gene and its possible roles in secondary metabolism in Ginkgo biloba. Plant Cell Rep. 32:637–650.10.1007/s00299-013-1397-2Search in Google Scholar

Cheng, Q., Li, N., Dong, L., Zhang, D., Fan, S., Jiang, L., Wang, X., Xu, P., Zhang, S. (2015) Overexpression of soybean isoflavone reductase (GmIFR) enhances resistance to Phytophthora sojae in soybean. Front. Plant Sci. 6:1024.10.3389/fpls.2015.01024Search in Google Scholar

Chien, S.C., Kuo, Y.H. (2009) Review of the chemical constitutes of Taiwania cryptomerioides. J. Chin. Chem. Soc. 67:33–44.Search in Google Scholar

Chou, Y.W., Thomas, P.I., Ge, X.J., LePage, B.A., Wang, C.N. (2011) Refugia and phylogeography of Taiwania in East Asia. J. Biogeogr. 38:1992–2005.10.1111/j.1365-2699.2011.02537.xSearch in Google Scholar

Corbin, C., Drouet, S., Mateljak, I., Markulin, L., Decourtil, C., Renouard, S., Lopez, T., Doussot, J., Lamblin, F., Auguin, D., Laine, E., Fuss, E., Hano, C. (2017) Functional characterization of the pinoresinol-lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response. Planta 246:405–420.10.1007/s00425-017-2701-0Search in Google Scholar

Dalisay, D.S., Kim, K.W., Lee, C., Yang, H., Rübel, O., Bowen, B.P., Davin, L.B., Lewis, N.G. (2015) Dirigent protein-mediated lignan and cyanogenic glucoside formation in flax seed: integrated omics and MALDI mass spectrometry imaging. J. Nat. Prod. 78:1231–1242.10.1021/acs.jnatprod.5b00023Search in Google Scholar

Dinkova-Kostova, A.T., Gang, D.R., Davin, L.B., Bedgar, D.L., Chu, A., Lewis, N.G. (1996) (+)-Pinoresinol/(+)-lariciresinol reductase from Forsythia intermedia. Protein purification, cDNA cloning, heterologous expression and comparison to isoflavone reductase. J. Biol. Chem. 271:29473–29482.10.1074/jbc.271.46.29473Search in Google Scholar

Fauré, M., Lissi, E., Torres, R., Videla, L.A. (1990) Antioxidant activities of lignans and flavonoids. Phytochemistry 29:3773–3775.10.1016/0031-9422(90)85329-ESearch in Google Scholar

Fujita, M., Gang, D.R., Davin, L.B., Lewis, N.G. (1999) Recombinant pinoresinol-lariciresinol reductases from western red cedar (Thuja plicata) catalyze opposite enantiospecific conversions. J. Biol. Chem. 274:618–627.10.1074/jbc.274.2.618Search in Google Scholar

Gang, D.R., Costa, M.A., Fujita, M., Dinkova-Kostova, A.T., Wang, H.B., Burlat, V., Martin, W., Sarkanen, S., Davin, L.B., Lewis, N.G. (1999a) Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis. Chem. Biol. 6:143–151.10.1016/S1074-5521(99)89006-1Search in Google Scholar

Gang, D.R., Kasahara, H., Xia, Z.Q., Vander Mijnsbrugge, K., Bauw, G., Boerjan, W., Van Montagu, M., Davin, L.B., Lewis, N.G. (1999b) Evolution of plant defense mechanisms. Relationships of phenylcoumaran benzylic ether reductases to pinoresinol-lariciresinol and isoflavone reductases. J. Biol. Chem. 274:7516–7527.10.1074/jbc.274.11.7516Search in Google Scholar

Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q.D., Chen, Z.H., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., Regev, A. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29:644–652.10.1038/nbt.1883Search in Google Scholar

Harmatha, J., Dinan, L. (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interactions. Phytochem. Rev. 2:321–330.10.1023/B:PHYT.0000045494.98645.a3Search in Google Scholar

Harn, H.J., Chuang, H.M., Chang, L.F., Huang, A., Hsieh, S.T., Lin, S.Z., Chou, C.W., Kuo, Y.H., Chiou, T.W. (2014) Taiwanin A targets non-steroidal anti-inflammatory drug-activated gene-1 in human lung carcinoma. Fitoterapia 99:227–235.10.1016/j.fitote.2014.08.020Search in Google Scholar

Hemmati, S., Schmidt, T.J., Fuss, E. (2007) (+)-Pinoresinol/(−)-lariciresinol reductase from Linum perenne Himmelszelt involved in the biosynthesis of justicidin B. FEBS Lett. 581:603–610.10.1016/j.febslet.2007.01.018Search in Google Scholar

Hemmati, S., von Heimendahl, C.B.I., Klaes, M., Alfermann, A.W., Schmidt, T.J., Fuss, E. (2010) Pinoresinol-lariciresinol reductases with opposite enantiospecificity determine the enantiomeric composition of lignans in the different organs of Linum usitatissimum L. Planta Med. 76:928–934.10.1055/s-0030-1250036Search in Google Scholar

Ho, P.J., Chou, C.K., Kuo, Y.H., Tu, L.C., Yeh, S.F. (2007) Taiwanin A induced cell cycle arrest and p53-dependent apoptosis in human hepatocellular carcinoma HepG2 cells. Life Sci. 80:493–503.10.1016/j.lfs.2006.10.017Search in Google Scholar

Johansson, C.I., Saddler, J.N., Beatson, R.P. (2000) Characterization of the polyphenolics related to the colour of western red cedar (Thuja plicata Donn) heartwood. Holzforschung 54:246–254.10.1515/HF.2000.042Search in Google Scholar

Kemp, M.S., Burden, R.S. (1986) Phytoalexins and stress metabolites in the sapwood of trees. Phytochemistry 25:1261–1269.10.1016/S0031-9422(00)81269-8Search in Google Scholar

Kim, M.K., Jeon, J.H., Fujita, M., Davin, L.B., Lewis, N.G. (2002) The western red cedar (Thuja plicata) 8-8′ DIRIGENT family displays diverse expression patterns and conserved monolignol coupling specificity. Plant Mol. Biol. 49:199–214.10.1023/A:1014940930703Search in Google Scholar

Kim, K.W., Moinuddin, S.G.A., Atwell, K.M., Costa, M.A., Davin, L.B., Lewis, N.G. (2012) Opposite stereoselectivities of dirigent proteins in Arabidopsis and Schizandra species. J. Biol. Chem. 287:33957–33972.10.1074/jbc.M112.387423Search in Google Scholar

Kuo, H.J., Wei, Z.Y., Lu, P.C., Huang, P.L., Lee, K.T. (2014) Bioconversion of pinoresinol into matairesinol by use of recombinant Escherichia coli. Appl. Environ. Microbiol. 80:2687–2692.10.1128/AEM.03397-13Search in Google Scholar

Kwon, M., Davin, L.B., Lewis, N.G. (2001) In situ hybridization and immunolocalization of lignan reductases in woody tissues: implications for heartwood formation and other forms of vascular tissue preservation. Phytochemistry 57:899–914.10.1016/S0031-9422(01)00108-XSearch in Google Scholar

Larson, R.A. (1988) The antioxidants of higher-plants. Phytochemistry 27:969–978.10.1016/0031-9422(88)80254-1Search in Google Scholar

Lau, W., Sattely, E.S. (2015) Six enzymes from mayapple that complete the biosynthetic pathway to the etoposide aglycone. Science 349:1224–1228.10.1126/science.aac7202Search in Google Scholar

Lim, K.J., Paasela, T., Harju, A., Venäläinen, M., Paulin, L., Auvinen, P., Kärkkäinen, K., Teeri, T.H. (2016) Developmental changes in Scots pine transcriptome during heartwood formation. Plant Physiol. 172:1403–1417.10.1104/pp.16.01082Search in Google Scholar

Liu, L.Y., Tseng, H.I., Lin, C.P., Lin, Y.Y., Huang, Y.H., Huang, C.K., Chang, T.H., Lin, S.S. (2014) High-throughput transcriptome analysis of the leafy flower transition of Catharanthus roseus induced by peanut witches’-broom phytoplasma infection. Plant Cell Physiol. 55:942–957.10.1093/pcp/pcu029Search in Google Scholar

Love, M.I., Huber, W., Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550.10.1186/s13059-014-0550-8Search in Google Scholar

MacRae, W.D., Towers, G.H.N. (1984) Biological activities of lignans. Phytochemistry 23:1207–1220.10.1016/S0031-9422(00)80428-8Search in Google Scholar

Magel, E.A. (2000) Biochemistry and physiology of heartwood formation. In: Cell and Molecular Biology of Wood Formation. Eds. Savidge, R., Barnett, J., Napier, R. BIOS Scientific Publishers, Oxford. pp. 363–376.Search in Google Scholar

Min, T.P., Kasahara, H., Bedgar, D.L., Youn, B.Y., Lawrence, P.K., Gang, D.R., Halls, S.C., Park, H.J., Hilsenbeck, J.L., Davin, L.B., Lewis, N.G., Kang, C. (2003) Crystal structures of pinoresinol-lariciresinol and phenylcoumaran benzylic ether reductases and their relationship to isoflavone reductases. J. Biol. Chem. 278:50714–50723.10.1074/jbc.M308493200Search in Google Scholar PubMed

Nakaba, S., Arakawa, I., Morimoto, H., Nakada, R., Bito, N., Imai, T., Funada, R. (2016) Agatharesinol biosynthesis-related changes of ray parenchyma in sapwood sticks of Cryptomeria japonica during cell death. Planta 243:1225–1236.10.1007/s00425-016-2473-ySearch in Google Scholar PubMed

Nakatsubo, T., Mizutani, M., Suzuki, S., Hattori, T., Umezawa, T. (2008) Characterization of Arabidopsis thaliana pinoresinol reductase, a new type of enzyme involved in lignan biosynthesis. J. Biol. Chem. 283:15550–15557.10.1074/jbc.M801131200Search in Google Scholar PubMed PubMed Central

Niculaes, C., Morreel, K., Kim, H., Lu, F.C., Mckee, L.S., Ivens, B., Haustraete, J., Vanholme, B., De Rycke, R., Hertzberg, M., Fromm, J., Bulone, V., Polle, A., Ralph, J., Boerjan, W. (2014) Phenylcoumaran benzylic ether reductase prevents accumulation of compounds formed under oxidative conditions in poplar xylem. Plant Cell. 26:3775–3791.10.1105/tpc.114.125260Search in Google Scholar PubMed PubMed Central

Nuoendagula, Kamimura, N., Mori, T., Nakabayashi, R., Tsuji, Y., Hishiyama, S., Saito, K., Masai, E., Kajita, S. (2016) Expression and functional analyses of a putative phenylcoumaran benzylic ether reductase in Arabidopsis thaliana. Plant Cell Rep. 35:513–526.10.1007/s00299-015-1899-1Search in Google Scholar PubMed

Paiva, N.L., Edwards, R., Sun, Y.J., Hrazdina, G., Dixon, R.A. (1991) Stress responses in alfalfa (Medicago sativa L.) 11. Molecular cloning and expression of alfalfa isoflavone reductase, a key enzyme of isoflavonoid phytoalexin biosynthesis. Plant Mol. Biol. 17:653–667.10.1007/BF00037051Search in Google Scholar PubMed

Paiva, N.L., Sun, Y.J., Dixon, R.A., Vanetten, H.D., Hrazdina, G. (1994) Molecular cloning of isoflavone reductase from pea (Pisum sativum L): evidence for a 3R-isoflavanone intermediate in (+)-pisatin biosynthesis. Arch. Biochem. Biophys. 312:501–510.10.1006/abbi.1994.1338Search in Google Scholar PubMed

Patten, A.M., Davin, L.B., Lewis, N.G. (2008) Relationship of dirigent protein and 18s RNA transcript localization to heartwood formation in western red cedar. Phytochemistry 69:3032–3037.10.1016/j.phytochem.2008.06.020Search in Google Scholar PubMed

Pittermann, J., Stuart, S.A., Dawson, T.E., Moreau, A. (2012) Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers. Proc. Natl. Acad. Sci. USA 109:9647–9652.10.1073/pnas.1114378109Search in Google Scholar PubMed PubMed Central

Roberts, A., Pachter, L. (2013) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat. Methods 10:71–73.10.1038/nmeth.2251Search in Google Scholar PubMed PubMed Central

Saguez, J., Attoumbré, J., Giordanengo, P., Baltora-Rosset, S. (2013) Biological activities of lignans and neolignans on the aphid Myzus persicae (Sulzer). Arthropod Plant Interact. 7:225–233.10.1007/s11829-012-9236-xSearch in Google Scholar

Satake, H., Koyama, T., Bahabadi, S.E., Matsumoto, E., Ono, E., Murata, J. (2015) Essences in metabolic engineering of lignan biosynthesis. Metabolites 5:270–290.10.3390/metabo5020270Search in Google Scholar PubMed PubMed Central

Shyur, L.F., Lee, S.H., Chang, S.T., Lo, C.P., Kuo, Y.H., Wang, S.Y. (2010) Taiwanin A inhibits MCF-7 cancer cell activity through induction of oxidative stress, upregulation of DNA damage checkpoint kinases, and activation of p53 and FasL/Fas signaling pathways. Phytomedicine 18:16–24.10.1016/j.phymed.2010.06.005Search in Google Scholar PubMed

Suzuki, S., Umezawa, T. (2007) Biosynthesis of lignans and norlignans. J. Wood Sci. 53:273–284.10.1007/s10086-007-0892-xSearch in Google Scholar

Suzuki, S., Umezawa, T., Shimada, M. (2002) Stereochemical diversity in lignan biosynthesis of Arctium lappa L. Biosci. Biotechnol. Biochem. 66:1262–1269.10.1271/bbb.66.1262Search in Google Scholar PubMed

Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729.10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central

Tiemann, K., Inzé, D., Vanmontagu, M., Barz, W. (1991) Pterocarpan phytoalexin biosynthesis in elicitor-challenged chickpea (Cicer arietinum L) cell cultures. Purification, characterization and cDNA cloning of NADPH:isoflavone oxidoreductase. Eur. J. Biochem. 200:751–757.10.1111/j.1432-1033.1991.tb16241.xSearch in Google Scholar PubMed

Tsao, N.W., Sun, Y.H., Chien, S.C., Chu, F.H., Chang, S.T., Kuo, Y.H., Wang, S.Y. (2016) Content and distribution of lignans in Taiwania cryptomerioides Hayata. Holzforschung 70:511–518.10.1515/hf-2015-0154Search in Google Scholar

Vanholme, R., Demedts, B., Morreel, K., Ralph, J., Boerjan, W. (2010) Lignin biosynthesis and structure. Plant Physiol. 153:895–905.10.1104/pp.110.155119Search in Google Scholar PubMed PubMed Central

Vargas-Arispuro, I., Reyes-Báez, R., Rivera-Castañeda, G., Martínez-Téllez, M.A., Rivero-Espejel, I. (2005) Antifungal lignans from the creosotebush (Larrea tridentata). Ind. Crop. Prod. 22:101–107.10.1016/j.indcrop.2004.06.003Search in Google Scholar

Vassão, D.G., Kim, K.W., Davin, L.B., Lewis, N.G. (2010) 1.23 – Lignans (neolignans) and allyl/propenyl phenols: biogenesis, structural biology, and biological/human health considerations. In: Comprehensive Natural Products II. Eds. Liu, H.W., Mander, L. Elsevier, Oxford. pp. 815–928.10.1016/B978-008045382-8.00001-0Search in Google Scholar

von Heimendahl, C.B.I., Schäfer, K.M., Eklund, P., Sjöholm, R., Schmidt, T.J., Fuss, E. (2005) Pinoresinol-lariciresinol reductases with different stereospecificity from Linum album and Linum usitatissimum. Phytochemistry 66:1254–1263.10.1016/j.phytochem.2005.04.026Search in Google Scholar PubMed

Xia, Z.Q., Costa, M.A., Pélissier, H.C., Davin, L.B., Lewis, N.G. (2001) Secoisolariciresinol dehydrogenase purification, cloning, and functional expression. Implications for human health protection. J. Biol. Chem. 276:12614–12623.10.1074/jbc.M008622200Search in Google Scholar PubMed

Xiao, Y., Ji, Q., Gao, S.H., Tan, H.X., Chen, R.B., Li, Q., Chen, J.F., Yang, Y.B., Zhang, L., Wang, Z.T., Chen, W.S., Hu, Z.B. (2015) Combined transcriptome and metabolite profiling reveals that IiPLR1 plays an important role in lariciresinol accumulation in Isatis indigotica. J. Exp. Bot. 66:6259–6271.10.1093/jxb/erv333Search in Google Scholar PubMed PubMed Central

Yoshida, K., Nishiguchi, M., Futamura, N., Nanjo, T. (2007) Expressed sequence tags from Cryptomeria japonica sapwood during the drying process. Tree Physiol. 27:1–9.10.1093/treephys/27.1.1Search in Google Scholar PubMed

Zhao, Q., Zeng, Y.N., Yin, Y.B., Pu, Y.Q., Jackson, L.A., Engle, N.L., Martin, M.Z., Tschaplinski, T.J., Ding, S.Y., Ragauskas, A.J., Dixon, R.A. (2015) Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis. Phytochemistry 112:170–178.10.1016/j.phytochem.2014.07.008Search in Google Scholar PubMed

Zheng, P.M., Aoki, D., Yoshida, M., Matsushita, Y., Imai, T., Fukushima, K. (2014) Lignification of ray parenchyma cells in the xylem of Pinus densiflora. Part I: microscopic investigation by POM, UV microscopy, and TOF-SIMS. Holzforschung 68:897–905.10.1515/hf-2013-0231Search in Google Scholar