In situ detection of laccase activity and immunolocalisation of a compression-wood-specific laccase (CoLac1) in differentiating xylem of Chamaecyparis obtusa
Hideto Hiraide A B , Masato Yoshida A , Saori Sato A and Hiroyuki Yamamoto A
+ Author Affiliations
- Author Affiliations
A Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan.
B Corresponding author. Email: hiraide.hideto@e.mbox.nagoya-u.ac.jp
Functional Plant Biology 43(6) 542-552 https://doi.org/10.1071/FP16044
Submitted: 12 February 2016 Accepted: 13 April 2016 Published: 12 May 2016
Abstract
The secondary cell wall of compression wood tracheids has a highly lignified region (S2 L) in its outermost portion. To better understand the mechanism of S2 L formation, we focussed on the activity of laccase (a monolignol oxidase) and performed in situ studies of this enzyme in differentiating compression wood. Staining of differentiating compression wood demonstrated that laccase activity began in all cell wall layers before the onset of lignification. We detected no activity of peroxidase (another monolignol oxidase) in any cell wall layer. Thus, laccase likely plays the major role in monolignol oxidisation during compression wood differentiation. Laccase activity was higher in the S2 L region than in other secondary wall regions, suggesting that this enzyme was responsible for the high lignin concentration in this region of the cell wall. Immunolabelling demonstrated the expression of a compression-wood-specific laccase (CoLac1) immediately following the onset of secondary wall thickening, this enzyme was localised to the S2 L region, whereas much less abundant in the S1 layer or inner S2 layer. Thus, the CoLac1 protein is most likely localised to the outer part of S2 and responsible for the high lignin concentration in the S2 L region.
Additional keywords: growth stress, immunolocalization, in-gel laccase activity staining, laccase activity staining, peroxidase activity staining, reaction wood, wood formation.
References
Allona I, Quinn M, Shoop E, Swope K, St Cyr S, Carlis J, Riedl J, Retzel E, Campbell MM, Sederoff R, Whetten RW (1998) Analysis of xylem formation in pine by cDNA sequencing. Proceedings of the National Academy of Sciences of the United States of America 95, 9693–9698.| Analysis of xylem formation in pine by cDNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltlClt70%3D&md5=25017f7439e93072cc94f4a7c31a10b5CAS | 9689143PubMed |
Altaner CM, Tokareva EN, Jarvis MC, Harris PJ (2010) Distribution of (1→4)-beta-galactans, arabinogalactan proteins, xylans and (1→3)-beta-glucans in tracheid cell walls of softwoods. Tree Physiology 30, 782–793.
| Distribution of (1→4)-beta-galactans, arabinogalactan proteins, xylans and (1→3)-beta-glucans in tracheid cell walls of softwoods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXoslyktrw%3D&md5=a7528bc26c7562851ab645f851f4f3c8CAS | 20382964PubMed |
Bao W, O’malley DM, Whetten R, Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260, 672–674.
| A laccase associated with lignification in loblolly pine xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXisFWmsr0%3D&md5=e8eb6efc0c97319b56cbe4cce05b488bCAS | 17812228PubMed |
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Annals of Botany 115, 1053–1074.
| The cell biology of lignification in higher plants.Crossref | GoogleScholarGoogle Scholar | 25878140PubMed |
Berthet S, Demont-Caulet N, Pollet B, Bidzinski P, Ce’zard L, Le Bris P, Borrega N, Herve’ J, Blondet E, Balzergue S, Lapierre C, Jouanin L (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. The Plant Cell 23, 1124–1137.
| Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1yjsLc%3D&md5=f7d2eab66d8e2bfc67a979e7c02ce899CAS | 21447792PubMed |
Boyd JD (1972) Tree growth stresses. V. Evidence of an origin in differentiation and lignification. Wood Science and Technology 6, 251–262.
| Tree growth stresses. V. Evidence of an origin in differentiation and lignification.Crossref | GoogleScholarGoogle Scholar |
Brown CL (1971) ‘Trees. Structure and function.’ In ‘Secondary growth’. (Eds Brown CL, Zimmermann MH) pp. 98–99. (Springer-Verlag: Berlin)
Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. Journal of Experimental Botany 60, 391–408.
| Specific functions of individual class III peroxidase genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSmt74%3D&md5=02268e91f72e7346b638c8d1b9ff5b2aCAS | 19088338PubMed |
Donaldson LA (2001) Lignification and lignin topochemistry – an ultrastructural view. Phytochemistry 57, 859–873.
| Lignification and lignin topochemistry – an ultrastructural view.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVygsLg%3D&md5=4ee964b6b09b41677f1571b98c8bdf7aCAS | 11423137PubMed |
Donaldson LA, Knox JP (2012) Localisation of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignifications and microfibril orientation. Plant Physiology 158, 642–653.
| Localisation of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignifications and microfibril orientation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOkt7k%3D&md5=83b23c9cd5d173eb53a49f642a8ff5fbCAS | 22147521PubMed |
Fagerstedt KV, Kukkola EM, Koistinen VVT, Takahashi J, Marjamaa K (2010) Cell all lignin is polymerised by class III secretable plant peroxidases in Norway spruce. Journal of Integrative Plant Biology 52, 186–194.
| Cell all lignin is polymerised by class III secretable plant peroxidases in Norway spruce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVCntrw%3D&md5=c3b257b9167fbc0bebb371e401f03cb9CAS | 20377680PubMed |
Fergus BJ, Procter AR, Scott JAN, Goring DAI (1969) The distribution of lignin in spruce wood as determined by ultraviolet microscopy. Wood Science and Technology 3, 117–138.
| The distribution of lignin in spruce wood as determined by ultraviolet microscopy.Crossref | GoogleScholarGoogle Scholar |
Fujita M, Saiki H, Harada H (1978) The secondary wall formation of compression wood tracheids. II. Cell wall thickening and lignification. Mokuzai Gakkai Shi 24, 158–163.
Hiraide H, Yoshida M, Ihara K, Sato S, Yamamoto H (2014) High lignin deposition on the outer region of the secondary wall middle layer in compression wood matches the expression of a laccase gene in Chamaecyparis obtusa. Journal of Plant Biology Research 3, 87–100.
Kim JS, Awano T, Yoshinaga A, Takabe K (2010) Immunolocalization of beta-1→4-galactan and its relationship with lignin distribution in developing compression wood of Cryptomeria japonica. Planta 232, 109–119.
| Immunolocalization of beta-1→4-galactan and its relationship with lignin distribution in developing compression wood of Cryptomeria japonica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFKlt7k%3D&md5=88ec049680dfb2d8e800beccb3c0eddbCAS | 20376677PubMed |
Koutaniemi S, Warinowski T, Kärkönen A, Alatalo E, Fossdal CG, Saranpää P, Laakso T, Fagerstedt KV, Simola LK, Paulin L, Rudd S, Teeri TH (2007) Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR. Plant Molecular Biology 65, 311–328.
| Expression profiling of the lignin biosynthetic pathway in Norway spruce using EST sequencing and real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeisL3O&md5=ac598e9fd0457b74f7fdfa2b2dba755bCAS | 17764001PubMed |
McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221, 619–636.
| Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVymsbk%3D&md5=be0a5b353a8b5f0ab237f04309e9a8fbCAS | 15940465PubMed |
McDougall GJ (2000) A comparison of proteins from the developing xylem of compression and non-compression wood of branches of Sitka spruce (Picea sitchensis) reveals a differentially expressed laccase. Journal of Experimental Botany 51, 1395–1401.
| A comparison of proteins from the developing xylem of compression and non-compression wood of branches of Sitka spruce (Picea sitchensis) reveals a differentially expressed laccase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVWnsrk%3D&md5=3497736cc0d8de03cff4d71eabecba36CAS | 10944153PubMed |
Okuyama T, Takeda H, Yamamoto H, Yoshida M (1998) Relation between growth stress and lignin concentration in the cell wall. Journal of Wood Science 44, 83–89.
| Relation between growth stress and lignin concentration in the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1SnsLw%3D&md5=59845aa36a484a7061dcb9b07a7cc06aCAS |
Onaka F (1949) Studies on compression- and tension-wood. Mokuzai Kenkyu 1, 1–88. [in Japanese].
Ranocha P, McDougall G, Hawkins S, Sterjiades R, Borderies G, Stewart D, Cabanes-Macheteau M, Boudet AM, Goffner D (1999) Biochemical characterization, molecular cloning and expression of laccases – a divergent gene family – in poplar. European Journal of Biochemistry 259, 485–495.
| Biochemical characterization, molecular cloning and expression of laccases – a divergent gene family – in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1KrsQ%3D%3D&md5=23514b587657078790f0545860f2b0b0CAS | 9914531PubMed |
Sato Y, Whetten RW (2006) Characterization of two laccases of loblolly pine (Pinus taeda) expressed in tobacco BY-2 cells. Journal of Plant Research 119, 581–588.
| Characterization of two laccases of loblolly pine (Pinus taeda) expressed in tobacco BY-2 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1elsLfN&md5=85a2cd0f8f7a96382bff75d5814ca8c9CAS | 16952031PubMed |
Scurfield G (1973) Reaction wood: its structure and function. Science 179, 647–655.
| Reaction wood: its structure and function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvgsFyhsQ%3D%3D&md5=fdfe952454cef31b2930531328227959CAS | 17774092PubMed |
Shigeto J, Itoh Y, Tsutsumi Y, Kondo R (2012) Identification of Tyr74 and Tyr177 as substrate oxidation sites in cationic cell wall-bound peroxidase from Populus alba L. The FEBS Journal 279, 348–357.
| Identification of Tyr74 and Tyr177 as substrate oxidation sites in cationic cell wall-bound peroxidase from Populus alba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlSrsbc%3D&md5=ecedded75272d06f233f68a335e13ab5CAS | 22099451PubMed |
Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y (2013) Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. Journal of Agricultural and Food Chemistry 61, 3781–3788.
| Putative cationic cell-wall-bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1WisL0%3D&md5=d138eb21b4146faf842dcc94d1432371CAS | 23551275PubMed |
Shigeto J, Nagano M, Fujita K, Tsutsumi Y (2014) Catalytic profile of Arabidopsis peroxidases, AtPrx-2, 25 and 71, contributing to stem lignification. PLoS One 9, e105332
| Catalytic profile of Arabidopsis peroxidases, AtPrx-2, 25 and 71, contributing to stem lignification.Crossref | GoogleScholarGoogle Scholar | 25137070PubMed |
Shigeto J, Itoh Y, Hirao S, Ohira K, Fujita K, Tsutsumi Y (2015) Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. Journal of Integrative Plant Biology 57, 349–356.
| Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvV2gs7s%3D&md5=7641342e4dac47436ebafaf9c3aea31cCAS | 25644691PubMed |
Sinnott EW (1952) Reaction wood and the regulation of tree form. American Journal of Botany 39, 69–78.
| Reaction wood and the regulation of tree form.Crossref | GoogleScholarGoogle Scholar |
Sterjiades R, Dean JFD, Eriksson KEL (1992) Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiology 99, 1162–1168.
| Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVOhtbo%3D&md5=09de38fa6969d9c21f5fa51065e9b57fCAS | 16668984PubMed |
Takabe K, Fujita M, Harada H, Saiki H (1981) Lignification process of Japanese black pine (Pinus thunbergii Parl.) tracheids. Mokuzai Gakkai Shi 27, 813–820.
Terashima N (1989) An improved radiotracer method for studying formation and structure of lignin. In ‘Plant cell wall polymers, biogenesis and biodegradation. ACS Symposium Series. Vol. 399’. (Eds NG Lewis, MG Paice) pp. 148–159. (American Chemical Society: Washington DC, NY, USA)
Terashima N, Fukushima K, He LF, Takabe K (1993) Comprehensive model of the lignified plant cell wall. In ‘Forage cell wall structure and digestibility’. (Eds HG Jung, DR Buxton, RD Hatfield, J Ralph) pp. 247–270. (American Society of Agronomy: Madison, WI, USA)
Timell TE (1986) ‘Compression wood in gymnosperms. Vol. 1.’ (Springer: Berlin)
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiology 153, 895–905.
| Lignin biosynthesis and structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFejs7o%3D&md5=b413fa8ce3ce83e5a993147111aa7ad2CAS | 20472751PubMed |
Villalobos DP, Díaz-Moreno SM, Said E-SS, Cañas RA, Osuna D, Van Kerckhoven SHE, Bautista R, Claros MG, Cánovas FM, Cantón FR (2012) Reprogramming of gene expression during compression wood formation in pine: coordinated modulation of S-adenosylmethionine, lignin and lignan related genes. BMC Plant Biology 12, 100–116.
| Reprogramming of gene expression during compression wood formation in pine: coordinated modulation of S-adenosylmethionine, lignin and lignan related genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCgu7bJ&md5=e0436ac3dba6527735176a2382e2cb2bCAS | 22747794PubMed |
Whetten R, Sun YH, Zhang Y, Sederoff R (2001) Functional genomics and cell wall synthesis in loblolly pine. Plant Molecular Biology 47, 275–291.
| Functional genomics and cell wall synthesis in loblolly pine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslGmtr4%3D&md5=c51b98edaa29924eba5f7a358c944307CAS | 11554476PubMed |
Wilson BF, Archer RR (1977) Reaction wood: induction and mechanical action. Annual Review of Plant Physiology 28, 23–43.
| Reaction wood: induction and mechanical action.Crossref | GoogleScholarGoogle Scholar |
Wilson BF, Archer RR (1979) Tree design: some biological solutions to mechanical problems. Bioscience 29, 293–298.
| Tree design: some biological solutions to mechanical problems.Crossref | GoogleScholarGoogle Scholar |
Yamamoto H, Okuyama T, Yoshida M, Sugiyama K (1991) Generation process of growth stresses in cell walls. III. Growth stress in compression wood. Mokuzai Gakkai Shi 37, 94–100.
Yamamoto H, Yoshida M, Okuyama T (2002) Growth stress controls negative gravitropism in woody plant stems. Planta 216, 280–292.
| Growth stress controls negative gravitropism in woody plant stems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFOiug%3D%3D&md5=35696c2ef3fdbdf6b4ebaf6dd2fa1fc9CAS | 12447542PubMed |
Yamashita S, Yoshida M, Takayama S, Okuyama T (2007) Stem-righting mechanism in gymnosperm trees deduced from limitations in compression wood development. Annals of Botany 99, 487–493.
| Stem-righting mechanism in gymnosperm trees deduced from limitations in compression wood development.Crossref | GoogleScholarGoogle Scholar | 17218339PubMed |
Yamashita S, Yoshida M, Yamamoto H, Okuyama T (2008) Screening genes that change expression during compression wood formation in Chamaecyparis obtusa. Tree Physiology 28, 1331–1340.
| Screening genes that change expression during compression wood formation in Chamaecyparis obtusa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFegurvJ&md5=50bb54ad60382223b2a7e7863392675fCAS | 18595845PubMed |
Yamashita S, Yoshida M, Yamamoto H (2009) Relationship between development of compression wood and gene expression. Plant Science 176, 729–735.
| Relationship between development of compression wood and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVWis7g%3D&md5=fcd58288739d8fe880efdab1d8051dabCAS |
Yoshida M, Ohta H, Yamamoto H, Okuyama T (2002) Tensile growth stress and lignin distribution in the cell walls of yellow poplar, Liriodendron tulipifera Linn. Trees 16, 457–464.
| Tensile growth stress and lignin distribution in the cell walls of yellow poplar, Liriodendron tulipifera Linn.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosFWltro%3D&md5=2ddef1df72c767217f0a6f3dcfda701aCAS |
Yoshinaga A, Kusumoto H, Laurans F, Pilate G, Takabe K (2012) Lignification in poplar tension wood lignified cell wall layers. Tree Physiology 32, 1129–1136.
| Lignification in poplar tension wood lignified cell wall layers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlymsL%2FM&md5=3bcf7f41ea5ed8fcf60515113a3d91b7CAS | 22933655PubMed |
Zhao Q, Nakashima J, Chen F, Yin YB, Fu CX, Yun JF, Shao H, Wang XQ, Wang ZY, Dixon RA (2013) LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis. The Plant Cell 25, 3976–3987.
| LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOrtrrJ&md5=920cf34dc6eadbbcc2cc607311090bdcCAS | 24143805PubMed |
