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Plant Physiol. (1 987) 84, 1-2 0032-0889/87/84/000 1/02/$01.00/0 Review The Extensins Received for publication February 19, 1987 MARY L. TIERNEY* AND JOSEPH E. VARNER Plant Biology Program, Washington University, St. Louis, Missouri 63130 ABSTRACIr The plant cell wall includes a matrix which is species specific and which chages in composition during growth and development. Characterization of the protein component of the wall matrix has resulted in the purification of extensin and the genes which encode it. Analysis of the protein sequences for the extensins has provided clues about the types of interactions which may occur as the chemistry and architecture of the cell wall accommodate growth and development. SerHypHypHypHyp is a conserved repetitive sequence within all three sequences. However longer repetitive sequences which are rich in other amino acid residues with chemically reactive side chains between the Ser(Hyp)1 "spacer sequences" such as SerHypHypHypHypValTyrLys and SerHypHypHypHypValLysProTyrHisProThrHypValTyrLys can be used to distinguish carrot extensin from each of the two The cell walls of higher plants are dynamic structures which undergo changes in composition and structure in relation to cell age, tissue type, and environmental stimuli. Individual components of the cell wall respond to physical damage (wounding), hormones, pathogen infection, and treatment with fungal elicitors (for review, see Showalter and Varner [11]). Moreover, endogenous cell wall oligosaccharins have been identified which when released affect the synthesis of defense related plant enzymes as well as serve to initiate a variety of developmental programs (3, 14). Thus, an understanding of cell wall components and their interactions is a prerequisite toward elucidating the roles cell wall chemistry and architecture play in plant growth and development. Analysis of the protein composition of the plant cell wall initially focused on hydroxyproline-rich glycoproteins following the discovery by Lamport that hydroxyproline was a major amino acid constituent in cell wall hydrolysates. HRGPs' have subsequently been shown to fall into three classes: hydroxyproline-rich lectins, arabinogalactans, and extensins. The hydroxyproline-rich lectins are a group of hemagglutinating glycoproteins which appear to be limited to the Solanaceae. These proteins contain both a hydroxyproline/serine-rich and a cysteine-rich domain and have been shown to increase upon wounding (11). Arabinogalactan proteins are acidic glycoproteins which are present in most plant tissues and are loosely associated with the cell wall. These proteins are rich in serine, alanine, and hydroxyproline and many function in cell-cell recognition (1 1). Extensins are HRGPs which become insolubilized within the primary cell wall. Soluble forms ofthis protein have been purified from carrot storage roots, soybean seed coats, and cultured tomato cells (1 1), and in all cases the protein is rich in hydroxyproline, serine, tyrosine, and lysine. A genomic clone encoding the carrot extensin gene has also been cloned and sequenced (1 1). The predicted amino acid sequence for carrot extensin from the extensin genomic clone has been compared with tryptic fragments of two species of tomato extensin. The sequence Abbreviation: HRGP, hydroxyproline-rich glycoprotein. tomato extensin species. Therefore it seems that the extensin protein genes have evolved to allow for a variety of functional sequences which may interact uniquely with the wall matrix to be spaced between a common backbone of Ser(Hyp)l spacer sequences. In any guessing game about how the extensins function we need to keep in mind that recently several plant genes have been isolated which may code for structural cell wall proteins unrelated to the HRGPs. cDNA and genomic clones encoding proline/ hydroxyproline-rich proteins have been isolated from both wounded carrot roots and from soybean cell cultures treated with auxin (7, 11). In the case of carrot, these cDNAs have been shown to code for a protein which accumulates in the cell wall after wounding (13). The cDNAs from both carrot and soybean code for proteins with biased amino acid compositions and contain the sequences XYProPro and ProProValTyrLys throughout the coding region. A genomic clone encoding a glycine-rich protein has been isolated from petunia which consists mainly of alternating GlyX residues in which X is frequently Gly, His, or Phe (2). While the protein encoded by this genomic clone has not yet been identified in petunia, a glycine-rich cell wall protein fraction has been identified in both pumpkin and soybean seed coats (1) indicating that the glycine-rich gene sequence may indeed code for another class of celLwall protein. Questions about the function of these proteins must await the determination oftheir compositions, sequences, and localization. The extensins appear to be encoded by small multi-gene families. This leads to the suggestion that different members of the family are regulated by different environmental or developmental signals. In carrots, different extensin mRNA transcripts have been found to accumulate in response to wounding and ethylene treatment (4). Similar types of differential expression have been observed when extensin mRNA accumulation patterns have been analyzed after fungal infection of Phaseolus vulgaris (10). Also, while extensin mRNA transcripts increase in Downloaded from on June 16, 2017 - Published by www.plantphysiol.org Copyright © 1987 American Society of Plant Biologists. All rights reserved. 2 Plant Physiol. Vol. 84, 1987 TIERNEY AND VARNER response to wounding in carrot storage roots and tomato stems and roots, very little extensin mRNA can be detected in leaves. While these data indicate that the extensin gene family may be differentially regulated in various tissues and in response to several external stimuli, more information is needed to elucidate both the mechanisms involved in mediating extensin gene expression and the function of the various extensin species within the cell wall. Once the architecture of the primary cell wall has been established during cell division, the cell wall must still be able to "loosen" or alter this structural matrix during the process of cell elongation. The effect of auxin on cell elongation has been well studied and models involving both obligate new gene expression and wall acidification have been proposed to explain its action. It is well established that treatment of plant tissue with auxin results in the synthesis of new gene products, one of which may be localized in the cell wall (7). However, the contribution that this induced gene expression makes to the mechanism of auxin regulated cell wall elongation has not yet been determined. The observation that there are two separate elongation responses to auxin in higher plants, one which may ready the wall for the process of elongation and a second which requires the action of newly synthesized gene products, has led to the suggestion that the distinctly different models of gene expression and wall acidification initially proposed are not incompatible (15). How might extensin ( 1-15% of the dry weight of the wall of dicotyledonous plants) interact with the other polymer systems (cellulose, 20-30%; xyloglucan, 20-30%; xylans, approximately 5%; pectins, 25-30%) in the wall? First let us look at how the polysaccharide components of the wall are thought to interact. It seems generally agreed that cellulose microfibrils are the principal load-bearing structures of the wall and that these microfibrils are coated with xyloglucans. These xyloglucans may be the primary substrate for the auxin regulated ,B- 1 ,4-glucanase activity which has been implicated in the control of cell wall elongation (6). Thus, with only these two wall components we can model a functional wall made up of load-bearing members embedded in a gel of adjustable properties. Starting from the facts (a) that pectic substances constitute a major fraction of the gel matrix of the wall, (b) that these can be secreted as methyl esters and deesterified later by wall-localized pectin methyl esterase, (c) that the resulting polyanionic matrix will have a higher concentration of protons than non-polyanionic portion of the wall, and (d) the properties of this matrix change markedly with changes in pH and [Ca2+], Nari et al. (9) have proposed that the change in polyanionic character caused by pectin methyl esterase controls the enzymes-e.g. endo-f3-1,4-glucanases-that allow the wall loosening necessary for cell growth. Critical parameters of this model include the density and distribution of the negative charges and the ability of the cell to control these parameters-for example, by pumping Ca2" and/or protons. The theory and properties of polyelectrolyte (polyacrylamidepolyacrylic acid) gels have been studied in detail (12). In char- acterizing the physical properties of gels Tanaka has shown that the gel properties of a highly polymerized network change markedly with small changes in the composition, pH, and ionic strength of the solvent in which the gel is immersed. It seems to us that the theory described by Tanaka (12) is applicable to the proposals of Nari et al. (9) and deserve examination. The physical nature of the oligosaccharide/protein matrix present in the cell wall may indeed resemble a gel in its response to changes in pH, ion concentration, and oligosaccharide/enzyme interactions which have been characterized as a function of growth and development. What then is the function of extensin in determining cell wall structure? Do its positive charges align with the negative charges of pectin to make an electrovalent zipper with the degree of closure controlled by pH and [Ca2+]? Is it co-localized with pectin or does it form its own discrete polycationic matrix? Is extensin polymerized to form a net (5, 8)? Is extensin covalently crosslinked to carbohydrate components of the wall? If so, what is the chemistry of the cross-links? Are we asking the right questions? LITERATURE CITED 1. CASSAB GI, JE VARNER 1986 A new protein in petunia. Nature 323: 110 2. CONDIT CM, RB MEAGHER 1986 A gene encoding a novel glycine-rich structural protein of petunia. Nature 323: 178-181 3. DAvis KR, AG DARVILL, P ALBERSHEIM, A DELL 1986 Host pathogen interactions. XXIX. Oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexin in soybean. Plant Physiol 80: 568-577 4. ECKER JR, RW DAVIS 1987 Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA. In press 5. FRY SC 1986 Cross-linking of matrix polymers in growing cell walls of angiosperms. Annu Rev Plant Physiol 37: 165-186 6. HAYASHI T, Y-S WONG, G MACLACHLAN 1984 Pea xyloglucan and cellulose. II. Hydrolysis by pea endo-1,4--yglucanases. Plant Physiol 75: 596-604 7. HONG JC, RT NAGAO, JL KEY 1985 Sequence analysis of an auxin-responsive developmentally regulated soybean gene. In GA Galamed, ed, First International Congress of Plant Molecular Biology. University of Georgia Center for Continued Education, Athens, p 91 8. LAMPORT DTA, L EPSTEIN 1983 A new model for the primary cell wall: a concatenated extensin-cellulose network. In DD Randall, DG Blevins, RS Larson, BS Rapp, eds, Current Topics in Plant Biochemistry and Physiology, Vol. II. University of Missouri, Columbia, pp 73-83 9. NARI J, G NOAT, G DIAMANTIDIS, M WOUDSTRA, J RICARD 1986 Electrostatic effects and the dynamics of enzyme reactions at the surface of plant cells. 3. Interplay between limited cell-wall autolysis, pectin methyl esterase activity and electrostatic effects in soybean walls. Eur J Biochem 155: 199-202 10. SHOWALTER AM, JN BELL, CL CRAMER, JA BAILEY, JE VARNER, CJ LAMB 1985 Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82: 6551-6555 11. SHOWALTER AM, JE VARNER 1987 Plant hydroxyproline-rich glycoproteins. In A Marcus, ed, The Biochemistry of Plants: A Comprehensive Treatise; Vol XI. Molecular Biology. Academic Press, New York. In press 12. TANAKA T 1980 Phase transitions in ionic gels. Physiol Rev Lett 45: 1636- 1639 13. TIERNEY ML 1986 Accumulation of a new proline-rich protein in carrot root cell walls after wounding. Plant Physiol 80: S-70 14. TRAN THANH VAN K, P TOUBART, A COUSSON, AG DARVILL, DJ GOLLIN, P CHELF, P ALBERSHEIM 1985 Manipulation of morphogenetic pathways of tobacco explants by oligosaccharins. Nature 314: 615-617 15. VANDERHOEF LN 1980 Auxin regulated cell enlargement: is there action at the level of gene expression? In CJ Leaver, ed, Genome Organization and Expression in Plants. Plenum Press, New York, pp 159-173 Downloaded from on June 16, 2017 - Published by www.plantphysiol.org Copyright © 1987 American Society of Plant Biologists. All rights reserved.