The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales

Hallmann A (2006)
Plant J. 45(2): 292-307.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Abstract / Bemerkung
Green algae of the order Volvocales provide an unrivalled opportunity for exploring the transition from unicellularity to multicellularity. They range from unicells, like Chlamydomonas, through homocytic colonial forms with increasing cooperation of individual cells, like Gonium or Pandorina, to heterocytic multicellular forms with different cell types and a complete division of labour, like Volvox. A fundamental requirement for the evolution of multicellularity is the development of a complex, multifunctional extracellular matrix (ECM). The ECM has many functions, which can change under developmental control or as a result of environmental factors. Here molecular data from 15 novel proteins are presented. These proteins have been identified in Chlamydomonas reinhardtii, Gonium pectorale, Pandorina morum and Volvox carteri, and all belong to a single protein family, the pherophorins. Pherophorin-V1 is shown to be a glycoprotein localized to the 'cellular zone' of the V. carteri ECM. Pherophorin-V1 and -V2 mRNAs are strongly induced not only by the sex inducer, which triggers sexual development at extremely low concentrations, but also by mechanical wounding. Like the extensins of higher plants, which are also developmentally controlled or sometimes inducible by wounding, the pherophorins contain a (hydroxy-)proline-rich (HR) rod-like domain and are abundant within the extracellular compartment. In contrast to most extensins, pherophorins have additional globular A and B domains on both ends of the HR domains. Therefore pherophorins most closely resemble a particular class of higher plant extensin, the solanaceous lectins (e.g. potato lectin), suggesting multivalent carbohydrate-binding functions are present within the A and B domains and are responsible for cross-linking. Our results suggest that pherophorins are used as the building blocks for the extracellular scaffold throughout the Volvocales, with the characteristic mesh sizes in different ECM structures being a result of the highly diverse extensions of the HR domains. Pherophorins have therefore been a versatile element during the evolution of ECM architecture in these green algae.
extracellular matrix; green algae; hydroxyproline-rich glycoproteins; solanaceous lectins; extensins; cell wall
Plant J.
Page URI


Hallmann A. The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J. 2006;45(2):292-307.
Hallmann, A. (2006). The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J., 45(2), 292-307.
Hallmann, Armin. 2006. “The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales”. Plant J. 45 (2): 292-307.
Hallmann, A. (2006). The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J. 45, 292-307.
Hallmann, A., 2006. The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J., 45(2), p 292-307.
A. Hallmann, “The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales”, Plant J., vol. 45, 2006, pp. 292-307.
Hallmann, A.: The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J. 45, 292-307 (2006).
Hallmann, Armin. “The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales”. Plant J. 45.2 (2006): 292-307.

26 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Proteases Shape the Chlamydomonas Secretome: Comparison to Classical Neuropeptide Processing Machinery.
Luxmi R, Blaby-Haas C, Kumar D, Rauniyar N, King SM, Mains RE, Eipper BA., Proteomes 6(4), 2018
PMID: 30249063
The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity.
Hanschen ER, Marriage TN, Ferris PJ, Hamaji T, Toyoda A, Fujiyama A, Neme R, Noguchi H, Minakuchi Y, Suzuki M, Kawai-Toyooka H, Smith DR, Sparks H, Anderson J, Bakarić R, Luria V, Karger A, Kirschner MW, Durand PM, Michod RE, Nozaki H, Olson BJ., Nat Commun 7(), 2016
PMID: 27102219
Green algae and the origins of multicellularity in the plant kingdom.
Umen JG., Cold Spring Harb Perspect Biol 6(11), 2014
PMID: 25324214
Multicellularity in green algae: upsizing in a walled complex.
Domozych DS, Domozych CE., Front Plant Sci 5(), 2014
PMID: 25477895
Genome-wide analysis of alternative splicing in Volvox carteri.
Kianianmomeni A, Ong CS, Rätsch G, Hallmann A., BMC Genomics 15(), 2014
PMID: 25516378
Genomics of Volvocine Algae.
Umen JG, Olson BJ., Adv Bot Res 64(), 2012
PMID: 25883411
Genomics of Volvocine Algae
Umen JG, Olson BJSC., Adv Bot Res 64(), 2012
PMID: IND601117399
Evolution of reproductive development in the volvocine algae.
Hallmann A., Sex Plant Reprod 24(2), 2011
PMID: 21174128
Fernández PV, Ciancia M, Miravalles AB, Estevez JM., J Phycol 46(3), 2010
PMID: IND44379819
Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri.
Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS., Science 329(5988), 2010
PMID: 20616280
Diverse evolutionary paths to cell adhesion.
Abedin M, King N., Trends Cell Biol 20(12), 2010
PMID: 20817460
Chemical and in situ characterization of macromolecular components of the cell walls from the green seaweed Codium fragile.
Estevez JM, Fernández PV, Kasulin L, Dupree P, Ciancia M., Glycobiology 19(3), 2009
PMID: 18832454
Structural features and gene-expression profiles of actin homologs in Porphyra yezoensis (Rhodophyta).
Kitade Y, Nakamura M, Uji T, Fukuda S, Endo H, Saga N., Gene 423(1), 2008
PMID: 18678234
Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri.
Nematollahi G, Kianianmomeni A, Hallmann A., BMC Genomics 7(), 2006
PMID: 17184518

86 References

Daten bereitgestellt von Europe PubMed Central.

Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
Mutational analysis of alpha-subunit of protein farnesyltransferase. Evidence for a catalytic role.
Andres DA, Goldstein JL, Ho YK, Brown MS., J. Biol. Chem. 268(2), 1993
PMID: 8419339
Generation of expressed sequence tags from low-CO2 and high-CO2 adapted cells of Chlamydomonas reinhardtii.
Asamizu E, Miura K, Kucho K, Inoue Y, Fukuzawa H, Ohyama K, Nakamura Y, Tabata S., DNA Res. 7(5), 2000
PMID: 11089912

Bannai, 2001
Extensive feature detection of N-terminal protein sorting signals.
Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S., Bioinformatics 18(2), 2002
PMID: 11847077

Bhatnagar, 1996
Multiple origins of colonial green flagellates from unicells: evidence from molecular and organismal characters.
Buchheim MA, McAuley MA, Zimmer EA, Theriot EC, Chapman RL., Mol. Phylogenet. Evol. 3(4), 1994
PMID: 7697190
Cassab GI., Annu. Rev. Plant Physiol. Plant Mol. Biol. 49(), 1998
PMID: 15012236
Structure and expression of a single actin gene in Volvox carteri.
Cresnar B, Mages W, Muller K, Salbaum JM, Schmitt R., Curr. Genet. 18(4), 1990
PMID: 2253273
Structure of pentameric human serum amyloid P component.
Emsley J, White HE, O'Hara BP, Oliva G, Srinivasan N, Tickle IJ, Blundell TL, Pepys MB, Wood SP., Nature 367(6461), 1994
PMID: 8114934
The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment.
Ertl H, Mengele R, Wenzl S, Engel J, Sumper M., J. Cell Biol. 109(6 Pt 2), 1989
PMID: 2689458
A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri.
Ertl H, Hallmann A, Wenzl S, Sumper M., EMBO J. 11(6), 1992
PMID: 1600938
Phylip - Phylogeny Inference Package (Version 3.2)
Felsenstein, Cladistics 5(), 1989
Plus and minus sexual agglutinins from Chlamydomonas reinhardtii.
Ferris PJ, Waffenschmidt S, Umen JG, Lin H, Lee JH, Ishida K, Kubo T, Lau J, Goodenough UW., Plant Cell 17(2), 2005
PMID: 15659633
Pheromone-binding and matrix-mediated events in sexual induction of Volvox carteri
Gilles, Z. Naturforsch. 39c(), 1984
Differential targeting of closely related ECM glycoproteins: the pherophorin family from Volvox.
Godl K, Hallmann A, Wenzl S, Sumper M., EMBO J. 16(1), 1997
PMID: 9009264
Extracellular matrix and sex-inducing pheromone in Volvox.
Hallmann A., Int. Rev. Cytol. 227(), 2003
PMID: 14518551
Reporter genes and highly regulated promoters as tools for transformation experiments in Volvox carteri.
Hallmann A, Sumper M., Proc. Natl. Acad. Sci. U.S.A. 91(24), 1994
PMID: 7972102

Harris, 1989
A molecular timescale of eukaryote evolution and the rise of complex multicellular life.
Hedges SB, Blair JE, Venturi ML, Shoe JL., BMC Evol. Biol. 4(), 2004
PMID: 15005799
Cycle sequencing through GC-rich regions.
Hengen PN., Trends Biochem. Sci. 21(1), 1996
PMID: 8848838
Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension.
Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR., Gene 77(1), 1989
PMID: 2744488
The biology and evolutionary significance of Devonian volvocaceans and their Precambrian relatives
Kazmierczak, Acta Paleontol. Pol. 26(), 1981
Simple cycle sequencing by labeling primer using Taq DNA polymerase.
Kim HJ, Kim BK., BioTechniques 16(4), 1994
PMID: 8024771

Kirk, 1998
WebPHYLIP: a web interface to PHYLIP.
Lim A, Zhang L., Bioinformatics 15(12), 1999
PMID: 10746002
The sexual inducer of Volvox carteri. Primary structure deduced from cDNA sequence.
Mages HW, Tschochner H, Sumper M., FEBS Lett. 234(2), 1988
PMID: 2839374
Organization and structure of Volvox alpha-tubulin genes.
Mages W, Salbaum JM, Harper JF, Schmitt R., Mol. Gen. Genet. 213(2-3), 1988
PMID: 3185511
Structure-independent DNA amplification by PCR using 7-deaza-2'-deoxyguanosine.
McConlogue L, Brow MA, Innis MA., Nucleic Acids Res. 16(20), 1988
PMID: 3186456
Hydroxyproline heterooligosaccharides in Chlamydomonas.
Miller DH, Lamport DT, Miller M., Science 176(4037), 1972
PMID: 5033634
The chemical composition of the cell wall of Chlamydomonas gymnogama and the concept of a plant cell wall protein.
Miller DH, Mellman IS, Lamport DT, Miller M., J. Cell Biol. 63(2 Pt 1), 1974
PMID: 4607708
Anhydrous hydrogen fluoride deglycosylates glycoproteins.
Mort AJ, Lamport DT., Anal. Biochem. 82(2), 1977
PMID: 71863
Matrix metalloproteinases.
Nagase H, Woessner JF Jr., J. Biol. Chem. 274(31), 1999
PMID: 10419448
GeneDoc: analysis and visualization of genetic variation
Nicholas, Embnet News 4(), 1997
Origin and evolution of the genera Pleodorina and Volvox (Volvocales)
Nozaki, Biologia (Bratisl.) 58(), 2003
Organic solvents as facilitators of polymerase chain reaction.
Pomp D, Medrano JF., BioTechniques 10(1), 1991
PMID: 2003924

Provasoli, 1959
The plant extracellular matrix: in a new expansive mood.
Roberts K., Curr. Opin. Cell Biol. 6(5), 1994
PMID: 7833049

Sambrook, 2001
DNA sequencing with chain-terminating inhibitors.
Sanger F, Nicklen S, Coulson AR., Proc. Natl. Acad. Sci. U.S.A. 74(12), 1977
PMID: 271968
Nuclear transformation of Volvox carteri.
Schiedlmeier B, Schmitt R, Muller W, Kirk MM, Gruber H, Mages W, Kirk DL., Proc. Natl. Acad. Sci. U.S.A. 91(11), 1994
PMID: 8197189
TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
Schmidt HA, Strimmer K, Vingron M, von Haeseler A., Bioinformatics 18(3), 2002
PMID: 11934758
Megascopic multicellular organisms from the 1700-million-year-old Tuanshanzi formation in the Jixian area, north China
Shixing, Science 270(), 1995
Structure and function of plant cell wall proteins.
Showalter AM., Plant Cell 5(1), 1993
PMID: 8439747
Arabinogalactan-proteins: structure, expression and function.
Showalter AM., Cell. Mol. Life Sci. 58(10), 2001
PMID: 11693522
Introduction: plant cell wall proteins.
Showalter AM., Cell. Mol. Life Sci. 58(10), 2001
PMID: 11693519

Showalter, 1989
Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information.
Shrager J, Hauser C, Chang CW, Harris EH, Davies J, McDermott J, Tamse R, Zhang Z, Grossman AR., Plant Physiol. 131(2), 2003
PMID: 12586865
Early evolution and the origin of eukaryotes.
Sogin ML., Curr. Opin. Genet. Dev. 1(4), 1991
PMID: 1822277
Structure, reproduction and differentiation in Volvox carteri f. nagariensis Iyengar, strains HK9 & 10
Starr, Arch. Protistenkd. 111(), 1969
Control of differentiation in Volvox
Starr, Dev. Biol. Suppl. 4(), 1970
How a sex pheromone might act at a concentration below 10(-16) M.
Sumper M, Berg E, Wenzl S, Godl K., EMBO J. 12(3), 1993
PMID: 8458341
Glycosylation motifs that direct arabinogalactan addition to arabinogalactan-proteins.
Tan L, Leykam JF, Kieliszewski MJ., Plant Physiol. 132(3), 2003
PMID: 12857818

Thompson, 1988
Potato lectin: an updated model of a unique chimeric plant protein.
Van Damme EJ, Barre A, Rouge P, Peumans WJ., Plant J. 37(1), 2004
PMID: 14675430
Plant cell wall architecture.
Varner JE, Lin LS., Cell 56(2), 1989
PMID: 2643477
Monophyletic origins of the metazoa: an evolutionary link with fungi.
Wainright PO, Hinkle G, Sogin ML, Stickel SK., Science 260(5106), 1993
PMID: 8469985
Volvocine cell walls and their constituent glycoproteins: an evolutionary perspective
Woessner, Protoplasma 181(), 1994
Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation.
Wu H, de Graaf B, Mariani C, Cheung AY., Cell. Mol. Life Sci. 58(10), 2001
PMID: 11693523

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 16367971
PubMed | Europe PMC

Suchen in

Google Scholar