Targeted migration of pherophorin-S indicates extensive extracellular matrix dynamics in Volvox carteri.

Chlamydomonas reinhardtii Volvox carteri confocal laser scanning microscopy extracellular matrix (ECM) green algae multicellularity pherophorins sex-inducer protein

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
09 2020
Historique:
received: 06 02 2020
revised: 12 06 2020
accepted: 17 06 2020
pubmed: 1 7 2020
medline: 20 4 2021
entrez: 1 7 2020
Statut: ppublish

Résumé

Hydroxyproline-rich glycoproteins (HRGPs) constitute a major group of proteins of the extracellular matrix (ECM). The multicellular green alga Volvox carteri is a suitable model organism in which to study the evolutionary transition to multicellularity, including the basic principles and characteristics of an ECM. In Volvox, the ECM is dominated by a single HRGP family: the pherophorins. Our inventory amounts to 117 pherophorin-related genes in V. carteri. We focused on a pherophorin with an unexpected characteristic: pherophorin-S is a soluble, non-cross-linked ECM protein. Using transformants expressing a YFP-tagged pherophorin-S we observed the synthesis and secretion of pherophorin-S by somatic cells in vivo, and we then traced the protein during its conspicuous migration to the ECM around prehatching juveniles and its localized concentration there. Our results provide insights into how an ECM zone surrounding the progeny is remotely affected by distantly located parental somatic cells. In view of the properties and migration of pherophorin-S, we conclude that pherophorin-S is likely to act as an ECM plasticizer to allow for dynamic ECM remodeling.

Identifiants

pubmed: 32603539
doi: 10.1111/tpj.14901
doi:

Substances chimiques

Algal Proteins 0
Glycoproteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2301-2317

Informations de copyright

© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
Boratyn, G.M., Camacho, C., Cooper, P.S. et al. (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Res. 41, W29-33.
Bustin, S.A. (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25, 169-193.
Chakravarthy, A., Khan, L., Bensler, N.P., Bose, P. and De Carvalho, D.D. (2018) TGF-beta-associated extracellular matrix genes link cancer-associated fibroblasts to immune evasion and immunotherapy failure. Nat. Commun. 9, 4692.
Edwards, K., Johnstone, C. and Thompson, C. (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
Ender, F., Godl, K., Wenzl, S. and Sumper, M. (2002) Evidence for autocatalytic cross-linking of hydroxyproline-rich glycoproteins during extracellular matrix assembly in Volvox. Plant Cell, 14, 1147-1160.
Ender, F., Hallmann, A., Amon, P. and Sumper, M. (1999) Response to the sexual pheromone and wounding in the green alga Volvox: induction of an extracellular glycoprotein consisting almost exclusively of hydroxyproline. J. Biol. Chem. 274, 35023-35028.
Ertl, H., Mengele, R., Wenzl, S., Engel, J. and Sumper, M. (1989) The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment. J. Cell Biol. 109, 3493-3501.
Fukada, K., Inoue, T. and Shiraishi, H. (2006) A posttranslationally regulated protease, VheA, is involved in the liberation of juveniles from parental spheroids in Volvox carteri. Plant Cell, 18, 2554-2566.
Godl, K., Hallmann, A., Rappel, A. and Sumper, M. (1995) Pherophorins: a family of extracellular matrix glycoproteins from Volvox structurally related to the sex-inducing pheromone. Planta, 196, 781-787.
Godl, K., Hallmann, A., Wenzl, S. and Sumper, M. (1997) Differential targeting of closely related ECM glycoproteins: the pherophorin family from Volvox. EMBO J. 16, 25-34.
Goodstein, D.M., Shu, S., Howson, R. et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-1186.
Gruber, H., Kirzinger, S.H. and Schmitt, R. (1996) Expression of the Volvox gene encoding nitrate reductase: mutation-dependent activation of cryptic splice sites and intron-enhanced gene expression from a cDNA. Plant Mol. Biol. 31, 1-12.
Hallmann, A. (2003) Extracellular matrix and sex-inducing pheromone in Volvox. Int. Rev. Cytol. 227, 131-182.
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. (2011) Evolution of reproductive development in the volvocine algae. Sex. Plant Reprod. 24, 97-112.
Hallmann, A. and Kirk, D.L. (2000) The developmentally regulated ECM glycoprotein ISG plays an essential role in organizing the ECM and orienting the cells of Volvox. J. Cell Sci. 113, 4605-4617.
Hallmann, A. and Wodniok, S. (2006) Swapped green algal promoters: aphVIII-based gene constructs with Chlamydomonas flanking sequences work as dominant selectable markers in Volvox and vice versa. Plant Cell Rep. 25, 582-591.
Harris, E.H., Stern, D.B. and Witman, G.B. (2009) The Chlamydomonas Sourcebook, 2nd edn. San Diego, CA: Academic Press.
Higuchi, R., Krummel, B. and Saiki, R.K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367.
Holst, O., Christoffel, V., Fründ, R., Moll, H. and Sumper, M. (1989) A phosphodiester bridge between two arabinose residues as a structural element of an extracellular glycoprotein of Volvox carteri. Eur. J. Biochem. 181, 345-350.
Jean, C., Gravelle, P., Fournie, J.J. and Laurent, G. (2011) Influence of stress on extracellular matrix and integrin biology. Oncogene, 30, 2697-2706.
Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S. and Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Res. 36, W5-9.
Kianianmomeni, A. and Hallmann, A. (2013) Validation of reference genes for quantitative gene expression studies in Volvox carteri using real-time RT-PCR. Mol. Biol. Rep. 40, 6691-6699.
Kianianmomeni, A., Nematollahi, G. and Hallmann, A. (2008) A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development. Plant Cell, 20, 2399-2419.
Kianianmomeni, A., Ong, C.S., Rätsch, G. and Hallmann, A. (2014) Genome-wide analysis of alternative splicing in Volvox carteri. BMC Genom. 15, 1117.
Kirk, D.L. (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Cambridge: Cambridge University Press.
Kirk, D.L. (2001) Germ-soma differentiation in Volvox. Dev. Biol. 238, 213-223.
Kirk, D.L. (2003) Seeking the ultimate and proximate causes of Volvox multicellularity and cellular differentiation. Integr. Comp. Biol. 43, 247-253.
Kirk, D.L. (2005) A twelve-step program for evolving multicellularity and a division of labor. BioEssays, 27, 299-310.
Kirk, D.L., Birchem, R. and King, N. (1986) The extracellular matrix of Volvox: a comparative study and proposed system of nomenclature. J. Cell Sci. 80, 207-231.
Kirk, D.L. and Kirk, M.M. (1986) Heat shock elicits production of sexual inducer in Volvox. Science, 231, 51-54.
Kirk, M.M. and Kirk, D.L. (2004) Exploring germ-soma differentiation in Volvox. J. Biosci. 29, 143-152.
Klein, B., Wibberg, D. and Hallmann, A. (2017) Whole transcriptome RNA-Seq analysis reveals extensive cell type-specific compartmentalization in Volvox carteri. BMC Biol, 15, 111.
Kremers, G.J., Goedhart, J., van Munster, E.B. and Gadella, T.W. Jr (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry, 45, 6570-6580.
Lauersen, K.J., Kruse, O. and Mussgnug, J.H. (2015) Targeted expression of nuclear transgenes in Chlamydomonas reinhardtii with a versatile, modular vector toolkit. Appl. Microbiol. Biotechnol. 99, 3491-3503.
Lerche, K. and Hallmann, A. (2009) Stable nuclear transformation of Gonium pectorale. BMC Biotechnol. 9, 64.
Lerche, K. and Hallmann, A. (2013) Stable nuclear transformation of Eudorina elegans. BMC Biotechnol. 13, 11.
Lerche, K. and Hallmann, A. (2014) Stable nuclear transformation of Pandorina morum. BMC Biotechnol. 14, 65.
Lu, P., Takai, K., Weaver, V.M. and Werb, Z. (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol, 3.
Matsuda, Y., Koseki, M., Shimada, T. and Saito, T. (1995) Purification and characterization of a vegetative lytic enzyme responsible for liberation of daughter cells during the proliferation of Chlamydomonas reinhardtii. Plant Cell Physiol. 36, 681-689.
Matusiewicz, M. (2011) Extracellular matrix remodeling. In Encyclopedia of Cancer, (ed. M. Schwab), pp. Berlin, Heidelberg: Springer.
Merchant, S.S., Prochnik, S.E., Vallon, O. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318, 245-250.
Michod, R.E., Viossat, Y., Solari, C.A., Hurand, M. and Nedelcu, A.M. (2006) Life-history evolution and the origin of multicellularity. J. Theor. Biol. 239, 257-272.
Miller, D.H., Lamport, D.T.A. and Miller, M. (1972) Hydroxyproline heterooligosaccharides in Chlamydomonas. Science, 176, 918-920.
Mohan, V., Das, A. and Sagi, I. (2020) Emerging roles of ECM remodeling processes in cancer. Semin. Cancer Biol. 62, 192-200.
Nedelcu, A.M., Marcu, O. and Michod, R.E. (2004) Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc. R. Soc. Lond., B. Biol. Sci. 271, 1591-1596.
Nedelcu, Aurora M. and Michod, Richard E. (2003) Sex as a response to oxidative stress: the effect of antioxidants on sexual induction in a facultatively sexual lineage. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(suppl_2), 136-139.
Nishimura, M., Nagashio, R., Sato, Y. and Hasegawa, T. (2017) Late Somatic Gene 2 disrupts parental spheroids cooperatively with Volvox hatching enzyme A in Volvox. Planta, 245, 183-192.
Nozaki, H. (2003) Origin and evolution of the genera Pleodorina and Volvox (Volvocales). Biologia (Bratisl.), 58, 425-431.
Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
Prochnik, S.E., Umen, J., Nedelcu, A.M. et al. (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science, 329, 223-226.
Provasoli, L. and Pintner, I.J. (1959) Artificial media for fresh-water algae: problems and suggestions. In The Ecology of Algae, a symposium held at the Pymatuning Laboratory of Field Biology on June 18 and 19, 1959, (ed. C.A. Tryon and R.T. Hartman), pp. 84-96. Pittsburgh, PA: The Pymatuning Symposia in Ecology, Special Publication No. 2, University of Pittsburgh.
Sambrook, J. and Russell, D.W. (2001) Molecular cloning: A laboratory manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Schiedlmeier, B., Schmitt, R., Müller, W., Kirk, M.M., Gruber, H., Mages, W. and Kirk, D.L. (1994) Nuclear transformation of Volvox carteri. Proc. Natl. Acad. Sci. USA, 91, 5080-5084.
Schindelin, J., Arganda-Carreras, I., Frise, E. et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods, 9, 676-682.
Schmitt, R. (2003) Differentiation of germinal and somatic cells in Volvox carteri. Curr. Opin. Microbiol. 6, 608-613.
Showalter, A.M. and Basu, D. (2016) Extensin and arabinogalactan-protein biosynthesis: glycosyltransferases, research challenges, and biosensors. Front Plant Sci. 7, 814.
Sommer-Knudsen, J., Bacic, A. and Clarke, A.E. (1998) Hydroxyproline-rich plant glycoproteins. Phytochemistry, 47, 483-497.
Sonbol, H.S. (2018) Extracellular matrix remodeling in human disease. J. Microsc. Ultrastruct. 6, 123-128.
Starr, R.C. (1969) Structure, reproduction and differentiation in Volvox carteri f. nagariensis Iyengar, strains HK 9 & 10. Arch. Protistenkd. 111, 204-222.
Starr, R.C. (1970) Control of differentiation in Volvox. Dev. Biol. Suppl. 4, 59-100.
Starr, R.C. and Jaenicke, L. (1974) Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc. Natl. Acad. Sci. USA, 71, 1050-1054.
Strenkert, D., Schmollinger, S., Gallaher, S.D. et al. (2019) Multiomics resolution of molecular events during a day in the life of Chlamydomonas. Proc. Natl. Acad. Sci. USA, 116, 2374-2383.
Sumper, M., Berg, E., Wenzl, S. and Godl, K. (1993) How a sex pheromone might act at a concentration below 10-16 M. EMBO J. 12, 831-836.
Sumper, M. and Hallmann, A. (1998) Biochemistry of the extracellular matrix of Volvox. Int. Rev. Cytol. 180, 51-85.
Tian, Y., Gao, S., von der Heyde, E.L., Hallmann, A. and Nagel, G. (2018) Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biol. 16, 144.
Wenzl, S. and Sumper, M. (1981) Sulfation of a cell surface glycoprotein correlates with the developmental program during embryogenesis of Volvox carteri. Proc. Natl. Acad. Sci. USA, 78, 3716-3720.
Wenzl, S. and Sumper, M. (1982) The occurrence of different sulphated cell surface glycoproteins correlates with defined developmental events in Volvox. FEBS Lett. 143, 311-315.

Auteurs

Benjamin von der Heyde (B)

Department of Cellular and Developmental Biology of Plants, University of Bielefeld, Universitätsstr. 25, Bielefeld, 33615, Germany.

Armin Hallmann (A)

Department of Cellular and Developmental Biology of Plants, University of Bielefeld, Universitätsstr. 25, Bielefeld, 33615, Germany.

Articles similaires

Humans Endoribonucleases RNA, Messenger RNA Caps Gene Expression Regulation
Animals Lung India Sheep Transcriptome
Humans Circadian Rhythm Adult Aged Aging
Obesity Machine Learning Animals Biomarkers Computational Biology

Classifications MeSH