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• W1985333595 abstract "The extracellular matrix (ECM) ofVolvox is modified during development or in response to external stimuli, like the sex-inducing pheromone. It has recently been demonstrated that a number of genes triggered by the sex-inducing pheromone are also inducible by wounding. By differential screening of a cDNA library, a novel gene was identified that is transcribed in response to the pheromone. Its gene product was characterized as an ECM glycoprotein with a striking feature: it exhibits a hydroxyproline content of 68% and therefore is an extreme member of the family of hydroxyproline-rich glycoproteins (HRGPs). HRGPs are known as constituents of higher plant ECMs and seem to function as structural barriers in defense responses. The Volvox HRGP is also found to be inducible by wounding. This indicates that the wound response scenarios of higher plants and multicellular green algae may be evolutionary related. The extracellular matrix (ECM) ofVolvox is modified during development or in response to external stimuli, like the sex-inducing pheromone. It has recently been demonstrated that a number of genes triggered by the sex-inducing pheromone are also inducible by wounding. By differential screening of a cDNA library, a novel gene was identified that is transcribed in response to the pheromone. Its gene product was characterized as an ECM glycoprotein with a striking feature: it exhibits a hydroxyproline content of 68% and therefore is an extreme member of the family of hydroxyproline-rich glycoproteins (HRGPs). HRGPs are known as constituents of higher plant ECMs and seem to function as structural barriers in defense responses. The Volvox HRGP is also found to be inducible by wounding. This indicates that the wound response scenarios of higher plants and multicellular green algae may be evolutionary related. extracellular matrix hydroxyproline-rich glycoprotein deep zone polymerase chain reaction rapid amplification of cDNA ends kilobase(s) high pressure liquid chromatography polyacrylamide gel electrophoresis hydrogen fluoride hydroxyproline-rich The evolution of a complex extracellular matrix (ECM)1 from a simple cell wall was one of the prerequisites to promote the transition from unicellularity to multicellularity. The volvocine algae provide the unique opportunity for exploring the pathways that led from a simple cell wall to a complex ECM that stabilizes the shape of an organism and mediates many developmental responses of cells to internal as well as external stimuli. The volvocine algae range in complexity from unicellular Chlamydomonas to multicellular organisms, with differentiated cells and complete division of labor, in the genusVolvox. The asexually growing organism of Volvox carteri is composed of only two cell types: 2000–4000 biflagellate Chlamydomonas-like somatic cells are arranged in a monolayer at the surface of a hollow sphere (1Starr R.C. Arch. Protistenk. 1969; 111: 204-222Google Scholar, 2Starr R.C. Dev. Biol. Suppl. 1970; 4: 59-100Google Scholar) and 16 much larger reproductive cells (“gonidia”) lie just below the somatic cell sheet. Volvox cells are surrounded and held together by a glycoprotein-rich ECM (reviewed in Refs. 3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar and 4Sumper M. Hallmann A. Int. Rev. Cytol. 1998; 180: 51-85Crossref PubMed Google Scholar). Cell walls and ECMs of the volvocine algae are assembled entirely from glycoproteins (5Miller D.H. Mellman I.S. Lamport D.T.A. Miller M. J. Cell Biol. 1974; 63: 420-429Crossref PubMed Scopus (74) Google Scholar) and a high content of hydroxyproline has been detected. Hydroxyproline-rich glycoproteins (HRGPs) represent a constituent of higher plant ECMs, and much work has been done to analyze the structures of these proteins (6Cooper J.B. Chen J.A. Varner J.E. Dugger W.M. Bartnicki-Garcia S. Structure, Function, and Biosynthesis of Plant Cell Walls. Waverly Press, Baltimore, MD1984: 75-88Google Scholar, 7Showalter A.M. Varner J.E. Stumpf P.K. Conn E.E. The Biochemistry of Plants. 15. Academic Press, New York1989: 485-520Google Scholar, 8Varner J.E. Lin L. Cell. 1989; 56: 231-239Abstract Full Text PDF PubMed Scopus (271) Google Scholar, 9Kieliszewski M.J. Lamport D.T.A. Plant J. 1994; 5: 157-172Crossref PubMed Scopus (439) Google Scholar, 10Knox J.P. FASEB J. 1995; 9: 1004-1012Crossref PubMed Scopus (119) Google Scholar, 11Knox J.P. Int. Rev. Cytol. 1997; 171: 79-120Crossref PubMed Google Scholar). However, there are few examples in the literature where multiple ECM proteins have been examined in molecular detail from a single species or from closely related species. This approach has been initiated with volvocine algae to allow a more integrated approach to elucidate the structure, assembly, and function of ECM proteins.A remarkably rapid remodelling of the ECM is observed under the influence of the sex-inducing pheromone (a glycoprotein) that triggers initiation of the sexual life cycle of Volvox carteri(12Wenzl S. Sumper M. FEBS Lett. 1982; 143: 311-315Crossref Scopus (27) Google Scholar, 13Wenzl S. Sumper M. Dev. Biol. 1986; 115: 119-128Crossref Scopus (24) Google Scholar, 14Gilles R. Gilles C. Jaenicke L. Naturwissenschaften. 1983; 70: 571-572Crossref Scopus (20) Google Scholar). In particular, synthesis of some members of the pherophorin family of ECM proteins (15Sumper M. Berg E. Wenzl S. Godl K. EMBO J. 1993; 12: 831-836Crossref PubMed Scopus (39) Google Scholar, 16Godl K. Hallmann A. Rappel A. Sumper M. Planta. 1995; 196: 781-787Crossref PubMed Google Scholar, 17Godl K. Hallmann A. Wenzl S. Sumper M. EMBO J. 1997; 16: 25-34Crossref PubMed Scopus (28) Google Scholar) is strongly induced by the pheromone. Pherophorins are ECM glycoproteins that contain a C-terminal domain with homology to the sex-inducing pheromone.By differential screening of a cDNA library, additional genes were recently identified that are transcribed under the control of the sex-inducing pheromone (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar). Unexpectedly, genes were found, in addition to those encoding the pherophorins, that encode extracellular chitinases and proteinases. In higher plants, similar protein families are known to play an important role in defense against fungi. Indeed, it could be demonstrated that the same set of genes triggered by the sex-inducing pheromone is also inducible by wounding ofVolvox spheroids.Pheromone-induced changes in the composition of the ECM have been characterized in detail within the cellular zone of the ECM (12Wenzl S. Sumper M. FEBS Lett. 1982; 143: 311-315Crossref Scopus (27) Google Scholar, 13Wenzl S. Sumper M. Dev. Biol. 1986; 115: 119-128Crossref Scopus (24) Google Scholar,15Sumper M. Berg E. Wenzl S. Godl K. EMBO J. 1993; 12: 831-836Crossref PubMed Scopus (39) Google Scholar, 16Godl K. Hallmann A. Rappel A. Sumper M. Planta. 1995; 196: 781-787Crossref PubMed Google Scholar, 19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar) and to a lesser extent within the deep zone (DZ) (17Godl K. Hallmann A. Wenzl S. Sumper M. EMBO J. 1997; 16: 25-34Crossref PubMed Scopus (28) Google Scholar), which contains all ECM components internal to the cellular zone (for nomenclature see Ref. 3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar). The DZ appears as a relatively amorphous component that fills the deepest regions of the spheroid and that may constitute more than 90% of the total volume of the organism. In this paper, we characterize a HRGP exhibiting an extreme composition that is expressed in response to the sex-inducing pheromone and to wounding and that is part of the DZ compartment of the ECM.DISCUSSIONThis paper describes the structure and properties of a novel component of the Volvox ECM with the striking feature of being composed of 68% hydroxyproline. Some of these hydroxyprolines are arranged in Ser-(Pro)3 and Ser-(Pro)4elements that are typical of higher plant extensins (9Kieliszewski M.J. Lamport D.T.A. Plant J. 1994; 5: 157-172Crossref PubMed Scopus (439) Google Scholar). Bradleyet al. (43Bradley D.J. Kjellbom P. Lamb C.J. Cell. 1992; 70: 21-30Abstract Full Text PDF PubMed Scopus (1004) Google Scholar) noted that tissue wounding in higher plants selectively stimulates the expression of tyrosine-rich extensins. In this respect, the algal DZ-HRPG is different because it contains only a single tyrosine residue. Similarly, it does not perfectly fit into the general class of higher plant extensins because the predominant basic amino acid lysine is replaced by arginine in the algal polypeptide. To our knowledge, there is no other protein described with a (hydroxy)-proline content as high as 68%. For example, the higher plant extensins with the highest (hydroxy)-proline contents are those of Vigna unguiculata (44Arsenijevic-Maksimovic I. Broughton W.J. Krause A. Mol. Plant Microbe Interact. 1997; 10: 95-101Crossref PubMed Scopus (26) Google Scholar), Nicotiana tabacum (45Keller B. Lamb C.J. Genes Dev. 1989; 3: 1639-1646Crossref PubMed Scopus (143) Google Scholar), and Gossypium barbadense (46John M.E. Keller G. Plant Physiol. 1995; 108: 669-676Crossref PubMed Scopus (60) Google Scholar), exhibiting 53, 44, and 40%, respectively. In the animal kingdom the mini-collagen of Hydra attenuata (47Kurz E.M. Holstein T.W. Petri B.M. Engel J. David C.N. J. Cell Biol. 1991; 115: 1159-1169Crossref PubMed Scopus (99) Google Scholar) exhibits 44%.A typical feature of algal ECM proteins characterized so far is a strictly modular composition, where hydroxyproline-rich (HR) sequences seem to serve as rod-shaped spacers separating modules that are completely devoid of hydroxyproline residues. It has been suggested that these hydroxyproline-rich stretches define a HR module family combining more specialized modules to yield chimeric and multifunctional ECM proteins (4Sumper M. Hallmann A. Int. Rev. Cytol. 1998; 180: 51-85Crossref PubMed Google Scholar). In this sense, DZ-HRGP represents the first volvocacean ECM glycoprotein being only composed of one (or more?) HR module(s). Electronmicroscopic studies have shown that main parts of the volvocacean ECM consist of a network of fibrous structures (48Goodenough U.W. Heuser J.E. J. Cell Biol. 1985; 101: 1550-1568Crossref PubMed Scopus (110) Google Scholar, 49Adair W.S. Steinmetz S.A. Mattson D.M. Goodenough U.W. Heuser J.E. J. Cell Biol. 1987; 105: 2373-2382Crossref PubMed Scopus (55) Google Scholar). Most probably, the rod-shaped HR modules mainly have a structural function and serve as building blocks to create these defined framework of the ECM. Where analyzed in more detail, these modules were found to be targets for extensive posttranslational modifications. Among the modifications identified in Volvoxare O-glycosylations with oligoarabinosides, attachment of saccharides containing phosphodiester bridges between arabinose residues, and in a single case, the additional attachment of a highly sulfated arabinomannan (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). As analyzed in more detail for the ECM protein SSG 185, the HR module is also involved in covalent cross-linking of the monomeric units (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). If DZ-HRPG serves a similar function, this rod-shaped molecule could be involved in the creation of the fibrous networks observed in the deep zone compartment (3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar). The fact that overexpression of DZ-HRPG did not create an aberrant ECM morphology could indicate the participation of a second ECM molecule in the cross-linking reaction. In this case, only the concomitant overexpression of both ECM partners interacting in a stoichiometric relation would be expected to cause a visible phenotype.The natural resistance of higher plants to diseases involves an array of inducible defense responses, including synthesis of extracellular hydrolytic enzymes such as proteases and chitinases and the accumulation of HRGPs within the ECM. The latter glycoproteins are hypothesized to function in defense as structural barriers (50Showalter A.M. Rumeau D. Adair W.S. Mecham R.P. Organization and Assembly of Plant and Animal Extracellular Matrix. Academic Press, New York1990: 247-281Crossref Google Scholar) or as specific microbial agglutinins (51Leach J.E. Cantrell M.A. Sequeira L. Plant Physiol. 1982; 70: 1353-1358Crossref PubMed Google Scholar, 52Mellon J.E. Helgeson J.P. Plant Physiol. 1982; 70: 401-405Crossref PubMed Google Scholar) against pathogen attack. Surprisingly, the simple multicellular green alga Volvoxresponds to wounding in much the same way as observed in higher plants. As was demonstrated recently (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar), Volvox responds to wounding with the synthesis of a chitinase as well as a protease that is combined with chitin-binding modules. With the additional demonstration of a typical HRGP that is produced in response to wounding, it now appears that much of the response scenario found in higher plants already exists in multicellular green algae. Even more surprising is the fact that these algal pathways are also triggered by the sex-inducing pheromone. However, Kirk and Kirk (53Kirk D.L. Kirk M.M. Science. 1986; 231: 51-54Crossref PubMed Scopus (58) Google Scholar) were able to demonstrate that synthesis of the sex-inducing pheromone can be triggered in somatic cells by a short heat shock applied to asexually growing organisms. This response induces the production of dormant zygotes that survive unfavorable conditions like drought. Although wounding is unable to induce pheromone production, similar biochemical responses are observed after wounding and pheromone application (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar). As induction of sexuality and subsequent production of zygotes obviously is part of the strategy of the organism to escape from environmental stress, it appears to make sense that apparently completely different stimuli (wounding and pheromone treatment) cause up-regulation of the same set of genes. Further studies on this algal system should confirm or deny an evolutionary relation of both the pheromone and the wound response systems. In addition, the possible relation of this algal system and the wound healing reactions in higher plants deserves further investigation. The evolution of a complex extracellular matrix (ECM)1 from a simple cell wall was one of the prerequisites to promote the transition from unicellularity to multicellularity. The volvocine algae provide the unique opportunity for exploring the pathways that led from a simple cell wall to a complex ECM that stabilizes the shape of an organism and mediates many developmental responses of cells to internal as well as external stimuli. The volvocine algae range in complexity from unicellular Chlamydomonas to multicellular organisms, with differentiated cells and complete division of labor, in the genusVolvox. The asexually growing organism of Volvox carteri is composed of only two cell types: 2000–4000 biflagellate Chlamydomonas-like somatic cells are arranged in a monolayer at the surface of a hollow sphere (1Starr R.C. Arch. Protistenk. 1969; 111: 204-222Google Scholar, 2Starr R.C. Dev. Biol. Suppl. 1970; 4: 59-100Google Scholar) and 16 much larger reproductive cells (“gonidia”) lie just below the somatic cell sheet. Volvox cells are surrounded and held together by a glycoprotein-rich ECM (reviewed in Refs. 3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar and 4Sumper M. Hallmann A. Int. Rev. Cytol. 1998; 180: 51-85Crossref PubMed Google Scholar). Cell walls and ECMs of the volvocine algae are assembled entirely from glycoproteins (5Miller D.H. Mellman I.S. Lamport D.T.A. Miller M. J. Cell Biol. 1974; 63: 420-429Crossref PubMed Scopus (74) Google Scholar) and a high content of hydroxyproline has been detected. Hydroxyproline-rich glycoproteins (HRGPs) represent a constituent of higher plant ECMs, and much work has been done to analyze the structures of these proteins (6Cooper J.B. Chen J.A. Varner J.E. Dugger W.M. Bartnicki-Garcia S. Structure, Function, and Biosynthesis of Plant Cell Walls. Waverly Press, Baltimore, MD1984: 75-88Google Scholar, 7Showalter A.M. Varner J.E. Stumpf P.K. Conn E.E. The Biochemistry of Plants. 15. Academic Press, New York1989: 485-520Google Scholar, 8Varner J.E. Lin L. Cell. 1989; 56: 231-239Abstract Full Text PDF PubMed Scopus (271) Google Scholar, 9Kieliszewski M.J. Lamport D.T.A. Plant J. 1994; 5: 157-172Crossref PubMed Scopus (439) Google Scholar, 10Knox J.P. FASEB J. 1995; 9: 1004-1012Crossref PubMed Scopus (119) Google Scholar, 11Knox J.P. Int. Rev. Cytol. 1997; 171: 79-120Crossref PubMed Google Scholar). However, there are few examples in the literature where multiple ECM proteins have been examined in molecular detail from a single species or from closely related species. This approach has been initiated with volvocine algae to allow a more integrated approach to elucidate the structure, assembly, and function of ECM proteins. A remarkably rapid remodelling of the ECM is observed under the influence of the sex-inducing pheromone (a glycoprotein) that triggers initiation of the sexual life cycle of Volvox carteri(12Wenzl S. Sumper M. FEBS Lett. 1982; 143: 311-315Crossref Scopus (27) Google Scholar, 13Wenzl S. Sumper M. Dev. Biol. 1986; 115: 119-128Crossref Scopus (24) Google Scholar, 14Gilles R. Gilles C. Jaenicke L. Naturwissenschaften. 1983; 70: 571-572Crossref Scopus (20) Google Scholar). In particular, synthesis of some members of the pherophorin family of ECM proteins (15Sumper M. Berg E. Wenzl S. Godl K. EMBO J. 1993; 12: 831-836Crossref PubMed Scopus (39) Google Scholar, 16Godl K. Hallmann A. Rappel A. Sumper M. Planta. 1995; 196: 781-787Crossref PubMed Google Scholar, 17Godl K. Hallmann A. Wenzl S. Sumper M. EMBO J. 1997; 16: 25-34Crossref PubMed Scopus (28) Google Scholar) is strongly induced by the pheromone. Pherophorins are ECM glycoproteins that contain a C-terminal domain with homology to the sex-inducing pheromone. By differential screening of a cDNA library, additional genes were recently identified that are transcribed under the control of the sex-inducing pheromone (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar). Unexpectedly, genes were found, in addition to those encoding the pherophorins, that encode extracellular chitinases and proteinases. In higher plants, similar protein families are known to play an important role in defense against fungi. Indeed, it could be demonstrated that the same set of genes triggered by the sex-inducing pheromone is also inducible by wounding ofVolvox spheroids. Pheromone-induced changes in the composition of the ECM have been characterized in detail within the cellular zone of the ECM (12Wenzl S. Sumper M. FEBS Lett. 1982; 143: 311-315Crossref Scopus (27) Google Scholar, 13Wenzl S. Sumper M. Dev. Biol. 1986; 115: 119-128Crossref Scopus (24) Google Scholar,15Sumper M. Berg E. Wenzl S. Godl K. EMBO J. 1993; 12: 831-836Crossref PubMed Scopus (39) Google Scholar, 16Godl K. Hallmann A. Rappel A. Sumper M. Planta. 1995; 196: 781-787Crossref PubMed Google Scholar, 19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar) and to a lesser extent within the deep zone (DZ) (17Godl K. Hallmann A. Wenzl S. Sumper M. EMBO J. 1997; 16: 25-34Crossref PubMed Scopus (28) Google Scholar), which contains all ECM components internal to the cellular zone (for nomenclature see Ref. 3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar). The DZ appears as a relatively amorphous component that fills the deepest regions of the spheroid and that may constitute more than 90% of the total volume of the organism. In this paper, we characterize a HRGP exhibiting an extreme composition that is expressed in response to the sex-inducing pheromone and to wounding and that is part of the DZ compartment of the ECM. DISCUSSIONThis paper describes the structure and properties of a novel component of the Volvox ECM with the striking feature of being composed of 68% hydroxyproline. Some of these hydroxyprolines are arranged in Ser-(Pro)3 and Ser-(Pro)4elements that are typical of higher plant extensins (9Kieliszewski M.J. Lamport D.T.A. Plant J. 1994; 5: 157-172Crossref PubMed Scopus (439) Google Scholar). Bradleyet al. (43Bradley D.J. Kjellbom P. Lamb C.J. Cell. 1992; 70: 21-30Abstract Full Text PDF PubMed Scopus (1004) Google Scholar) noted that tissue wounding in higher plants selectively stimulates the expression of tyrosine-rich extensins. In this respect, the algal DZ-HRPG is different because it contains only a single tyrosine residue. Similarly, it does not perfectly fit into the general class of higher plant extensins because the predominant basic amino acid lysine is replaced by arginine in the algal polypeptide. To our knowledge, there is no other protein described with a (hydroxy)-proline content as high as 68%. For example, the higher plant extensins with the highest (hydroxy)-proline contents are those of Vigna unguiculata (44Arsenijevic-Maksimovic I. Broughton W.J. Krause A. Mol. Plant Microbe Interact. 1997; 10: 95-101Crossref PubMed Scopus (26) Google Scholar), Nicotiana tabacum (45Keller B. Lamb C.J. Genes Dev. 1989; 3: 1639-1646Crossref PubMed Scopus (143) Google Scholar), and Gossypium barbadense (46John M.E. Keller G. Plant Physiol. 1995; 108: 669-676Crossref PubMed Scopus (60) Google Scholar), exhibiting 53, 44, and 40%, respectively. In the animal kingdom the mini-collagen of Hydra attenuata (47Kurz E.M. Holstein T.W. Petri B.M. Engel J. David C.N. J. Cell Biol. 1991; 115: 1159-1169Crossref PubMed Scopus (99) Google Scholar) exhibits 44%.A typical feature of algal ECM proteins characterized so far is a strictly modular composition, where hydroxyproline-rich (HR) sequences seem to serve as rod-shaped spacers separating modules that are completely devoid of hydroxyproline residues. It has been suggested that these hydroxyproline-rich stretches define a HR module family combining more specialized modules to yield chimeric and multifunctional ECM proteins (4Sumper M. Hallmann A. Int. Rev. Cytol. 1998; 180: 51-85Crossref PubMed Google Scholar). In this sense, DZ-HRGP represents the first volvocacean ECM glycoprotein being only composed of one (or more?) HR module(s). Electronmicroscopic studies have shown that main parts of the volvocacean ECM consist of a network of fibrous structures (48Goodenough U.W. Heuser J.E. J. Cell Biol. 1985; 101: 1550-1568Crossref PubMed Scopus (110) Google Scholar, 49Adair W.S. Steinmetz S.A. Mattson D.M. Goodenough U.W. Heuser J.E. J. Cell Biol. 1987; 105: 2373-2382Crossref PubMed Scopus (55) Google Scholar). Most probably, the rod-shaped HR modules mainly have a structural function and serve as building blocks to create these defined framework of the ECM. Where analyzed in more detail, these modules were found to be targets for extensive posttranslational modifications. Among the modifications identified in Volvoxare O-glycosylations with oligoarabinosides, attachment of saccharides containing phosphodiester bridges between arabinose residues, and in a single case, the additional attachment of a highly sulfated arabinomannan (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). As analyzed in more detail for the ECM protein SSG 185, the HR module is also involved in covalent cross-linking of the monomeric units (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). If DZ-HRPG serves a similar function, this rod-shaped molecule could be involved in the creation of the fibrous networks observed in the deep zone compartment (3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar). The fact that overexpression of DZ-HRPG did not create an aberrant ECM morphology could indicate the participation of a second ECM molecule in the cross-linking reaction. In this case, only the concomitant overexpression of both ECM partners interacting in a stoichiometric relation would be expected to cause a visible phenotype.The natural resistance of higher plants to diseases involves an array of inducible defense responses, including synthesis of extracellular hydrolytic enzymes such as proteases and chitinases and the accumulation of HRGPs within the ECM. The latter glycoproteins are hypothesized to function in defense as structural barriers (50Showalter A.M. Rumeau D. Adair W.S. Mecham R.P. Organization and Assembly of Plant and Animal Extracellular Matrix. Academic Press, New York1990: 247-281Crossref Google Scholar) or as specific microbial agglutinins (51Leach J.E. Cantrell M.A. Sequeira L. Plant Physiol. 1982; 70: 1353-1358Crossref PubMed Google Scholar, 52Mellon J.E. Helgeson J.P. Plant Physiol. 1982; 70: 401-405Crossref PubMed Google Scholar) against pathogen attack. Surprisingly, the simple multicellular green alga Volvoxresponds to wounding in much the same way as observed in higher plants. As was demonstrated recently (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar), Volvox responds to wounding with the synthesis of a chitinase as well as a protease that is combined with chitin-binding modules. With the additional demonstration of a typical HRGP that is produced in response to wounding, it now appears that much of the response scenario found in higher plants already exists in multicellular green algae. Even more surprising is the fact that these algal pathways are also triggered by the sex-inducing pheromone. However, Kirk and Kirk (53Kirk D.L. Kirk M.M. Science. 1986; 231: 51-54Crossref PubMed Scopus (58) Google Scholar) were able to demonstrate that synthesis of the sex-inducing pheromone can be triggered in somatic cells by a short heat shock applied to asexually growing organisms. This response induces the production of dormant zygotes that survive unfavorable conditions like drought. Although wounding is unable to induce pheromone production, similar biochemical responses are observed after wounding and pheromone application (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar). As induction of sexuality and subsequent production of zygotes obviously is part of the strategy of the organism to escape from environmental stress, it appears to make sense that apparently completely different stimuli (wounding and pheromone treatment) cause up-regulation of the same set of genes. Further studies on this algal system should confirm or deny an evolutionary relation of both the pheromone and the wound response systems. In addition, the possible relation of this algal system and the wound healing reactions in higher plants deserves further investigation. This paper describes the structure and properties of a novel component of the Volvox ECM with the striking feature of being composed of 68% hydroxyproline. Some of these hydroxyprolines are arranged in Ser-(Pro)3 and Ser-(Pro)4elements that are typical of higher plant extensins (9Kieliszewski M.J. Lamport D.T.A. Plant J. 1994; 5: 157-172Crossref PubMed Scopus (439) Google Scholar). Bradleyet al. (43Bradley D.J. Kjellbom P. Lamb C.J. Cell. 1992; 70: 21-30Abstract Full Text PDF PubMed Scopus (1004) Google Scholar) noted that tissue wounding in higher plants selectively stimulates the expression of tyrosine-rich extensins. In this respect, the algal DZ-HRPG is different because it contains only a single tyrosine residue. Similarly, it does not perfectly fit into the general class of higher plant extensins because the predominant basic amino acid lysine is replaced by arginine in the algal polypeptide. To our knowledge, there is no other protein described with a (hydroxy)-proline content as high as 68%. For example, the higher plant extensins with the highest (hydroxy)-proline contents are those of Vigna unguiculata (44Arsenijevic-Maksimovic I. Broughton W.J. Krause A. Mol. Plant Microbe Interact. 1997; 10: 95-101Crossref PubMed Scopus (26) Google Scholar), Nicotiana tabacum (45Keller B. Lamb C.J. Genes Dev. 1989; 3: 1639-1646Crossref PubMed Scopus (143) Google Scholar), and Gossypium barbadense (46John M.E. Keller G. Plant Physiol. 1995; 108: 669-676Crossref PubMed Scopus (60) Google Scholar), exhibiting 53, 44, and 40%, respectively. In the animal kingdom the mini-collagen of Hydra attenuata (47Kurz E.M. Holstein T.W. Petri B.M. Engel J. David C.N. J. Cell Biol. 1991; 115: 1159-1169Crossref PubMed Scopus (99) Google Scholar) exhibits 44%. A typical feature of algal ECM proteins characterized so far is a strictly modular composition, where hydroxyproline-rich (HR) sequences seem to serve as rod-shaped spacers separating modules that are completely devoid of hydroxyproline residues. It has been suggested that these hydroxyproline-rich stretches define a HR module family combining more specialized modules to yield chimeric and multifunctional ECM proteins (4Sumper M. Hallmann A. Int. Rev. Cytol. 1998; 180: 51-85Crossref PubMed Google Scholar). In this sense, DZ-HRGP represents the first volvocacean ECM glycoprotein being only composed of one (or more?) HR module(s). Electronmicroscopic studies have shown that main parts of the volvocacean ECM consist of a network of fibrous structures (48Goodenough U.W. Heuser J.E. J. Cell Biol. 1985; 101: 1550-1568Crossref PubMed Scopus (110) Google Scholar, 49Adair W.S. Steinmetz S.A. Mattson D.M. Goodenough U.W. Heuser J.E. J. Cell Biol. 1987; 105: 2373-2382Crossref PubMed Scopus (55) Google Scholar). Most probably, the rod-shaped HR modules mainly have a structural function and serve as building blocks to create these defined framework of the ECM. Where analyzed in more detail, these modules were found to be targets for extensive posttranslational modifications. Among the modifications identified in Volvoxare O-glycosylations with oligoarabinosides, attachment of saccharides containing phosphodiester bridges between arabinose residues, and in a single case, the additional attachment of a highly sulfated arabinomannan (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). As analyzed in more detail for the ECM protein SSG 185, the HR module is also involved in covalent cross-linking of the monomeric units (19Ertl H. Mengele R. Wenzl S. Engel J. Sumper M. J. Cell Biol. 1989; 109: 3493-3501Crossref PubMed Scopus (49) Google Scholar). If DZ-HRPG serves a similar function, this rod-shaped molecule could be involved in the creation of the fibrous networks observed in the deep zone compartment (3Kirk D.L. Birchem R. King N. J. Cell Sci. 1986; 80: 207-231PubMed Google Scholar). The fact that overexpression of DZ-HRPG did not create an aberrant ECM morphology could indicate the participation of a second ECM molecule in the cross-linking reaction. In this case, only the concomitant overexpression of both ECM partners interacting in a stoichiometric relation would be expected to cause a visible phenotype. The natural resistance of higher plants to diseases involves an array of inducible defense responses, including synthesis of extracellular hydrolytic enzymes such as proteases and chitinases and the accumulation of HRGPs within the ECM. The latter glycoproteins are hypothesized to function in defense as structural barriers (50Showalter A.M. Rumeau D. Adair W.S. Mecham R.P. Organization and Assembly of Plant and Animal Extracellular Matrix. Academic Press, New York1990: 247-281Crossref Google Scholar) or as specific microbial agglutinins (51Leach J.E. Cantrell M.A. Sequeira L. Plant Physiol. 1982; 70: 1353-1358Crossref PubMed Google Scholar, 52Mellon J.E. Helgeson J.P. Plant Physiol. 1982; 70: 401-405Crossref PubMed Google Scholar) against pathogen attack. Surprisingly, the simple multicellular green alga Volvoxresponds to wounding in much the same way as observed in higher plants. As was demonstrated recently (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar), Volvox responds to wounding with the synthesis of a chitinase as well as a protease that is combined with chitin-binding modules. With the additional demonstration of a typical HRGP that is produced in response to wounding, it now appears that much of the response scenario found in higher plants already exists in multicellular green algae. Even more surprising is the fact that these algal pathways are also triggered by the sex-inducing pheromone. However, Kirk and Kirk (53Kirk D.L. Kirk M.M. Science. 1986; 231: 51-54Crossref PubMed Scopus (58) Google Scholar) were able to demonstrate that synthesis of the sex-inducing pheromone can be triggered in somatic cells by a short heat shock applied to asexually growing organisms. This response induces the production of dormant zygotes that survive unfavorable conditions like drought. Although wounding is unable to induce pheromone production, similar biochemical responses are observed after wounding and pheromone application (18Amon P. Haas E. Sumper M. Plant Cell. 1998; 10: 781-789Crossref PubMed Scopus (56) Google Scholar). As induction of sexuality and subsequent production of zygotes obviously is part of the strategy of the organism to escape from environmental stress, it appears to make sense that apparently completely different stimuli (wounding and pheromone treatment) cause up-regulation of the same set of genes. Further studies on this algal system should confirm or deny an evolutionary relation of both the pheromone and the wound response systems. In addition, the possible relation of this algal system and the wound healing reactions in higher plants deserves further investigation. We thank Dr. R. Deutzmann and E. Hochmuth for mass spectrometry and for protein sequencing." @default.
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• W1985333595 title "Response to the Sexual Pheromone and Wounding in the Green Alga Volvox: Induction of an Extracellular Glycoprotein Consisting Almost Exclusively of Hydroxyproline" @default.
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