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Wood Contains a Cell-Wall Structural Protein (Immunocytolocalization/Loblolly Pine/Extensin/Xylem/Xylogenesis) WULI BAO*, DAVID M

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Wood Contains a Cell-Wall Structural Protein (Immunocytolocalization/Loblolly Pine/Extensin/Xylem/Xylogenesis) WULI BAO*, DAVID M Proc. Natl. Acad. Sci. USA Vol. 89, pp. 6604-6608, July 1992 Plant Biology Wood contains a cell-wall structural protein (immunocytolocalization/loblolly pine/extensin/xylem/xylogenesis) WULI BAO*, DAVID M. O'MALLEY, AND RONALD R. SEDEROFF Department of Forestry, Box 8008, North Carolina State University, Raleigh, NC 27695 Communicated by Joseph E. Varner, April 20, 1992 (received for review February 17, 1992) ABSTRACT A pine extensin-like protein (PELP) has been the proteins themselves (7-10) demonstrate tissue-specific localized in metabolically active cells of differentiating xylem expression in several different species of plants. Some struc- and in mature wood of loblolly pine (Pinus taeda L.). This tural proteins are associated with vascular systems (7, 9, 10). proline-rich glycosylated protein was purified from cell walls of For example, proline-rich proteins are found by immunocy- differentiating xylem by differential solubility and gel electro- tochemical localization to be associated with xylem vessel phoresis. Polyclonal rabbit antibodies were raised against the elements in soybean (7). Glycine-rich proteins in bean are deglycosylated purified protein (dPELP) and purified antibody located specifically in the tracheary elements of the protox- was used for immunolocalization. Immunogold and alkaline ylem (9). However, there have been no reports of cell-wall phosphatase secondary antibody staining both show antigen in structural proteins in wood cell walls (1). secondary cell walls ofearlywood and less staining in latewood. Hydroxyproline, the major amino acid of extensin, has Immunoassays of milled dry wood were developed and used to been measured in cell walls of cultured cells from Gingko show increased availability of antigen after hydrogen fluoride biloba, Cupressus sp., and Ephedra sp., suggesting the or cellulase treatment and decreased antigen after chlorite presence of extensin-like proteins in gymnosperms (11). treatment. The specificity ofthe antigen-antibody reaction was Hydroxyproline was also found in low amounts (about 5% of confirmed by competition assays and by preadsorption of the total amino acids) in acid hydrolysates of wood from antibody to the purified protein. We propose that extensin-like Pinus sylvestris (2). In this paper, an extensin-like cell-wall protein is present in xylem cell walls during ligniflication and protein of loblolly pine (Pinus taeda) is identified and puri- that the protein remains as a structural component of cell walls fied. Immunolocalization shows that the protein is present in in wood for many years after xylogenesis. We suggest that such structural proteins play important roles in the differentiation of cell walls of mature wood. xylem and thereby could affect the properties of wood. MATERIALS AND METHODS Wood is a renewable natural resource that forms the basis of Plant Materials. All plant materials were obtained from a large industry serving human needs for fiber and fuel. Wood loblolly pine growing in the North Carolina coastal plain. is secondary xylem, formed by the vascular cambium of woody plants. The chemical composition and physical prop- Differentiating xylem was collected in May or June from erties of wood have been the subject of intense research for rapidly growing trees 11-13 years old. Bark can be peeled the past century. Cellulose, lignin, hemicellulose, and ex- from the stems of trees during this time. The differentiating tractives account for >99% of the mass of wood (1). Proteins xylem remained attached to the wood, while the cambium have not been considered to be important components of and phloem stayed attached to the bark. The differentiating wood. xylem was removed with vegetable peelers and was frozen Small amounts of nitrogen (by Kjeldahl analysis) can be immediately in liquid nitrogen. The stored material was used detected in milled wood (2). Stable heartwood of pines as a source of cell-wall proteins during the rest of the year. contains nitrogen at -0.05% of the total dry weight (3). Fresh wood of 4- to 6-year-old loblolly pine was cut with Amino acids can be recovered from wood by acid hydrolysis a sledge microtome into 20-/Lm sections for immunolocaliza- of extractive free wood (2). Laidlaw and Smith (2) found that tion. Pieces of dried wood from 10-year-old stems (dried for amino acids accounted for at least 70% ofthe nitrogen in pine 2 years at room temperature) were milled into powder for wood. They proposed that protein was the major nitrogenous immunoassays. material in wood but found that the amino acid composition Purification and Analysis of the Cell-Wall Structural Pro- of their material differed from that of Lamport and North- tein. Frozen loblolly pine xylem was ground to a powder in cote, who found a hydroxyproline-rich protein in cell walls of a blender in liquid nitrogen and suspended in extraction cultured cells ofsycamore (Acerpseudoplantanus) (4). Cowl- buffer (0.1% potassium acetate, pH 5.0/4 mM Na2S205). The ing and Merrill (5) also suggested that extensin in the xylem cell-wall fraction was obtained by filtration and washing primary cell walls could account for some of the nitrogen seven times in 2 mM Na2S205. A protein fraction was found in mature wood. extracted from the cell walls with 0.4 M calcium chloride (8) The proteins most likely to be found in wood are cell-wall and was further fractionated by differential solubility in 5% structural proteins. Three kinds of cell-wall proteins, which CC13COOH (12). The resulting cell-wall protein was further differ in amino acid composition, have been found in plants purified by SDS/PAGE (7.5% polyacrylamide) (13) and elec- (6). These are hydroxyproline-rich glycoproteins, glycine- troelution (14). The protein, called pine extensin-like protein rich proteins, and proline-rich proteins (6, 7). These proteins (PELP), was deglycosylated (dPELP) by hydrogen fluoride are generally considered to be important structural compo- (15). Amino acid analysis by phenyl isothiocyanate deriva- nents of the plant cell walls. Localization studies of mRNA tization was done as described (16) after acid hydrolysis (17). coding for cell-wall structural proteins and the localization of The hydrolyzed amino acids were separated by reverse- The publication costs of this article were defrayed in part by page charge Abbreviations: PELP, pine extensin-like protein; dPELP, deglyco- payment. This article must therefore be hereby marked "advertisement" sylated PELP; FPLC, fast-protein liquid chromatography. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 6604 Downloaded by guest on September 29, 2021 Plant Biology: Bao et al. Proc. Natl. Acad. Sci. USA 89 (1992) 6605 phase C18 HPLC (16) and identified by comparison to amino for 1 hr, which dissolves lignin and cross-linked protein in acid standards (Sigma). wood (20, 21). Immunological Assays. Purified dPELP was used as antigen to inject two New Zealand White rabbits. Bands containing the dPELP were cut from gels (SDS/PAGE), dried under RESULTS vacuum (Speedvac), and ground to a fine powder. The Protein Purification. A PELP fraction was isolated from protein (50 .ug) was mixed with complete Freund's adjuvant differentiating xylem of loblolly pine. Cell walls were ob- for the primary injection. A second injection was carried out tained from 200 to 400 g of loblolly pine xylem as described, 45 days later with 30 gg of dPELP mixed with incomplete and the cell-wall fraction was extracted with 0.5 M CaCl2. adjuvant. Serum was collected 2 weeks later for ELISA and The extracted protein was then precipitated with 5% immunoblotting (Western blotting) (18). ELISA was used to CCl3COOH to obtain a CCl3COOH-soluble fraction. This titer the serum and to estimate the relative amounts of fraction showed a single band on SDS/PAGE (Fig. la) with antigen. Preimmune serum was used routinely for controls. low mobility. A band of the same mobility as PELP was Alkaline phosphatase-conjugated goat anti-rabbit serum (Sig- visible with crude cell-wall extracts of differentiating xylem ma) was used as the secondary antibody. Proteins for West- (Fig. la, lane 3). This result suggests that PELP is an ern blots were separated on SDS/PAGE (7.5% polyacryl- abundant component of the total cell-wall protein. When amide) and blotted onto nitrocellulose. Tris-buffered saline using the whole-cell soluble extract or total cell-wall proteins, (TBS) used for immunoassays was 50 mM Tris-HCl, pH a band was visible in the same position on a Western blot 7.6/0.15 M NaCl. prepared with PELP antibodies (Fig. lb, lanes 1 and 3). The Purification of Anti-dPELP IgG. Rabbit anti-dPELP serum final CCl3COOH-soluble fraction was about 1/400th of the was purified by ion-exchange chromatography (Mono Q, total soluble protein and about 1/6th of the cell-wall CaCl2- Pharmacia) on a fast protein liquid chromatography (FPLC) extracted protein. column [0.0-0.3 M NaCl gradient in 20 mM Tris'HCl (pH Properties of the PELP Fraction. Treatment of PELP with 8.0)]. The relative amount of IgG in different fractions was hydrofluoric acid in pyridine increased the SDS/PAGE mo- determined by ELISA with goat anti-rabbit IgG coupled to bility ofthe protein, indicating that the protein is glycosylated alkaline (Fig. la, lane 7) and has an apparent molecular mass of 68 phosphatase. Anti-dPELP activity was also deter- kDa. We hydrolyzed the dPELP fraction with 6 M HCO and mined by ELISA plate assays. Further purification of the determined the relative proportion of amino acids (Table 1). anti-dPELP antibodies was carried out by affinity purifica- The protein is rich in proline (25%) and hydroxyproline tion with dPELP antigen immobilized on nitrocellulose (19). (11%), consistent with a structural role. Briefly, a specific band ofpurified dPELP electrophoresed on Properties of Anti-dPELP Antibody.
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