A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development

Kianianmomeni A, Nematollahi G, Hallmann A (2008)
Plant Cell 20(9): 2399-2419.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
Here, we describe the cloning and characterization of RETINOBLASTOMA-RELATED PROTEIN1 (RBR1) from the green alga Volvox carteri. RBR1 expression increases substantially during embryogenesis and in response to the sex-inducer glycoprotein, but it decreases significantly under heat stress. While RBR1 is expressed in gonidia (asexual reproductive cells) and embryos, the largest proportion of RBR1 mRNA is found in parental somatic cells. The presence of 4 splice variants and 15 potential cyclin-dependent kinase phosphorylation sites suggests that RBR1 is subject to control at the posttranscriptional and posttranslational levels. Surprisingly, RBR1 is a gender-specific gene, mapping exclusively to the female mating-type locus. A procedure for stable nuclear transformation of males was established to generate RBR1-expressing males. These transformants exhibit enlarged reproductive cells, altered growth characteristics, and a prolonged embryogenesis. The results suggest that a functionally related analog of RBR1 exists in males. The reason for the divergent evolution of RBRs in females and males appears to be based on sexual development: males and females respond to the same sex-inducer with different cleavage programs and substantial differences in cellular differentiation. Thus, the gender-specific presence of RBR1 provides evidence for an additional, novel role for retinoblastoma family proteins in sexual development.
Erscheinungsjahr
Zeitschriftentitel
Plant Cell
Band
20
Zeitschriftennummer
9
Seite
2399-2419
ISSN
eISSN
PUB-ID

Zitieren

Kianianmomeni A, Nematollahi G, Hallmann A. A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development. Plant Cell. 2008;20(9):2399-2419.
Kianianmomeni, A., Nematollahi, G., & 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(9), 2399-2419. doi:10.1105/tpc.107.057836
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., Nematollahi, G., & 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(9), p 2399-2419.
A. Kianianmomeni, G. Nematollahi, and A. Hallmann, “A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development”, Plant Cell, vol. 20, 2008, pp. 2399-2419.
Kianianmomeni, A., Nematollahi, G., Hallmann, A.: 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 (2008).
Kianianmomeni, Arash, Nematollahi, G., and Hallmann, Armin. “A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development”. Plant Cell 20.9 (2008): 2399-2419.

17 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The 4-Celled Tetrabaena socialis Nuclear Genome Reveals the Essential Components for Genetic Control of Cell Number at the Origin of Multicellularity in the Volvocine Lineage.
Featherston J, Arakaki Y, Hanschen ER, Ferris PJ, Michod RE, Olson BJSC, Nozaki H, Durand PM., Mol Biol Evol 35(4), 2018
PMID: 29294063
Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases.
Tian Y, Gao S, von der Heyde EL, Hallmann A, Nagel G., BMC Biol 16(1), 2018
PMID: 30522480
The inducible nitA promoter provides a powerful molecular switch for transgene expression in Volvox carteri.
von der Heyde EL, Klein B, Abram L, Hallmann A., BMC Biotechnol 15(), 2015
PMID: 25888095
Novel roles of plant RETINOBLASTOMA-RELATED (RBR) protein in cell proliferation and asymmetric cell division.
Desvoyes B, de Mendoza A, Ruiz-Trillo I, Gutierrez C., J Exp Bot 65(10), 2014
PMID: 24323507
Genome-wide analysis of alternative splicing in Volvox carteri.
Kianianmomeni A, Ong CS, Rätsch G, Hallmann A., BMC Genomics 15(), 2014
PMID: 25516378
Evolution of reproductive development in the volvocine algae.
Hallmann A., Sex Plant Reprod 24(2), 2011
PMID: 21174128
Germline specification and function in plants.
Berger F, Twell D., Annu Rev Plant Biol 62(), 2011
PMID: 21332359
A shift toward smaller cell size via manipulation of cell cycle gene expression acts to smoothen Arabidopsis leaf shape.
Kuwabara A, Backhaus A, Malinowski R, Bauch M, Hunt L, Nagata T, Monk N, Sanguinetti G, Fleming A., Plant Physiol 156(4), 2011
PMID: 21632970
Regulation and function of retinoblastoma-related plant genes
Sabelli PaoloA, Larkins BrianA., Plant Sci 177(6), 2009
PMID: IND44277128

90 References

Daten bereitgestellt von Europe PubMed Central.

Targets of the cyclin-dependent kinase Cdk1.
Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, Morgan DO., Nature 425(6960), 2003
PMID: 14574415
Control of differentiation in Volvox.
Starr RC., Symp Soc Dev Biol 29(), 1970
PMID: 4950154
Genetic control of sexual development in Volvox.
Callahan AM, Huskey RJ., Dev. Biol. 80(2), 1980
PMID: 7450290
Effects of senescence on somatic cell physiology in the green alga Volvox carteri.
Pommerville J, Kochert G., Exp. Cell Res. 140(1), 1982
PMID: 7106202
Heat shock elicits production of sexual inducer in Volvox.
Kirk DL, Kirk MM., Science 231(4733), 1986
PMID: 3941891
A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma.
Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM, Albert DM, Dryja TP., Nature 323(6089), 1986
PMID: 2877398
Mating type linked mutations which disrupt the uniparental transmission of chloroplast genes in chlamydomonas.
Gillham NW, Boynton JE, Johnson AM, Burkhart BD., Genetics 115(4), 1987
PMID: 3582961
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
Mating type and mating strategies in Neurospora.
Metzenberg RL, Glass NL., Bioessays 12(2), 1990
PMID: 2140508
Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri.
Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL., Curr. Genet. 18(2), 1990
PMID: 1977526
Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
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
Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri.
Robbens S, Khadaroo B, Camasses A, Derelle E, Ferraz C, Inze D, Van de Peer Y, Moreau H., Mol. Biol. Evol. 22(3), 2004
PMID: 15537805
The signals and pathways activating cellular senescence.
Ben-Porath I, Weinberg RA., Int. J. Biochem. Cell Biol. 37(5), 2004
PMID: 15743671
The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots.
Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B., Cell 123(7), 2005
PMID: 16377572
Retinoblastoma family proteins: insights gained through genetic manipulation of mice.
Wikenheiser-Brokamp KA., Cell. Mol. Life Sci. 63(7-8), 2006
PMID: 16465443
Retinoblastoma protein partners.
Morris EJ, Dyson NJ., Adv. Cancer Res. 82(), 2001
PMID: 11447760
Alternative splicing and genome complexity.
Brett D, Pospisil H, Valcarcel J, Reich J, Bork P., Nat. Genet. 30(1), 2001
PMID: 11743582
A genomic view of alternative splicing.
Modrek B, Lee C., Nat. Genet. 30(1), 2002
PMID: 11753382
Retinoblastoma family genes.
Du W, Pogoriler J., Oncogene 25(38), 2006
PMID: 16936737
Cell size checkpoint control by the retinoblastoma tumor suppressor pathway.
Fang SC, de los Reyes C, Umen JG., PLoS Genet. 2(10), 2006
PMID: 17040130
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
Dicot and monocot plants differ in retinoblastoma-related protein subfamilies.
Lendvai A, Pettko-Szandtner A, Csordas-Toth E, Miskolczi P, Horvath GV, Gyorgyey J, Dudits D., J. Exp. Bot. 58(7), 2007
PMID: 17389586
The Chlamydomonas genome reveals the evolution of key animal and plant functions.
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR., Science 318(5848), 2007
PMID: 17932292
E2F-associated chromatin modifiers and cell cycle control.
Blais A, Dynlacht BD., Curr. Opin. Cell Biol. 19(6), 2007
PMID: 18023996
Synteny and collinearity in plant genomes.
Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH., Science 320(5875), 2008
PMID: 18436778
Retinoblastoma proteins in plants.
de Jager SM, Murray JA., Plant Mol. Biol. 41(3), 1999
PMID: 10598097
The hallmarks of cancer.
Hanahan D, Weinberg RA., Cell 100(1), 2000
PMID: 10647931
Rb function in cell-cycle regulation and apoptosis.
Harbour JW, Dean DC., Nat. Cell Biol. 2(4), 2000
PMID: 10783254
The E2F transcription factor is a cellular target for the RB protein.
Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR., Cell 65(6), 1991
PMID: 1828392
The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle.
Goodrich DW, Wang NP, Qian YW, Lee EY, Lee WH., Cell 67(2), 1991
PMID: 1655277
Early evolution and the origin of eukaryotes.
Sogin ML., Curr. Opin. Genet. Dev. 1(4), 1991
PMID: 1822277
Regulation of retinoblastoma protein functions by ectopic expression of human cyclins.
Hinds PW, Mittnacht S, Dulic V, Arnold A, Reed SI, Weinberg RA., Cell 70(6), 1992
PMID: 1388095
Monophyletic origins of the metazoa: an evolutionary link with fungi.
Wainright PO, Hinkle G, Sogin ML, Stickel SK., Science 260(5106), 1993
PMID: 8469985
Functional interactions of the retinoblastoma protein with mammalian D-type cyclins.
Ewen ME, Sluss HK, Sherr CJ, Matsushime H, Kato J, Livingston DM., Cell 73(3), 1993
PMID: 8343202
Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation.
Helin K, Wu CL, Fattaey AR, Lees JA, Dynlacht BD, Ngwu C, Harlow E., Genes Dev. 7(10), 1993
PMID: 8405995
The relationship between cell size and cell fate in Volvox carteri.
Kirk MM, Ransick A, McRae SE, Kirk DL., J. Cell Biol. 123(1), 1993
PMID: 8408198
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
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
The retinoblastoma protein and cell cycle control.
Weinberg RA., Cell 81(3), 1995
PMID: 7736585
Genetic structure of the mating-type locus of Chlamydomonas reinhardtii.
Ferris PJ, Armbrust EV, Goodenough UW., Genetics 160(1), 2002
PMID: 11805055
Cancer cell cycles.
Sherr CJ., Science 274(5293), 1996
PMID: 8939849
The retinoblastoma protein pathway and the restriction point.
Bartek J, Bartkova J, Lukas J., Curr. Opin. Cell Biol. 8(6), 1996
PMID: 8939678
RB kinases and RB-binding proteins: new points of view.
Taya Y., Trends Biochem. Sci. 22(1), 1997
PMID: 9020586
Rapid evolution of sex-related genes in Chlamydomonas.
Ferris PJ, Pavlovic C, Fabry S, Goodenough UW., Proc. Natl. Acad. Sci. U.S.A. 94(16), 1997
PMID: 9238029
Sexual conflict and speciation.
Parker GA, Partridge L., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 353(1366), 1998
PMID: 9533125
The highly efficient sex-inducing pheromone system of Volvox.
Hallmann A, Godl K, Wenzl S, Sumper M., Trends Microbiol. 6(5), 1998
PMID: 9614342
Coordination of growth and cell division in the Drosophila wing.
Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA., Cell 93(7), 1998
PMID: 9657151
The regulation of E2F by pRB-family proteins.
Dyson N., Genes Dev. 12(15), 1998
PMID: 9694791
The retinoblastoma pathway in plant cell cycle and development.
Gutierrez C., Curr. Opin. Plant Biol. 1(6), 1998
PMID: 10066630
Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP.
Zheng N, Fraenkel E, Pabo CO, Pavletich NP., Genes Dev. 13(6), 1999
PMID: 10090723
Control of the cell cycle and apoptosis.
Lundberg AS, Weinberg RA., Eur. J. Cancer 35(4), 1999
PMID: 10492624
Function of alternative splicing.
Stamm S, Ben-Ari S, Rafalska I, Tang Y, Zhang Z, Toiber D, Thanaraj TA, Soreq H., Gene 344(), 2004
PMID: 15656968
The Pezcoller lecture: cancer cell cycles revisited.
Sherr CJ., Cancer Res. 60(14), 2000
PMID: 10919634
Alternative pre-mRNA splicing: the logic of combinatorial control.
Smith CW, Valcarcel J., Trends Biochem. Sci. 25(8), 2000
PMID: 10916158
Role of the LXCXE binding site in Rb function.
Dahiya A, Gavin MR, Luo RX, Dean DC., Mol. Cell. Biol. 20(18), 2000
PMID: 10958676
Retinoblastoma-related proteins in plants: homologues or orthologues of their metazoan counterparts?
Durfee T, Feiler HS, Gruissem W., Plant Mol. Biol. 43(5-6), 2000
PMID: 11089866
Control of cell division by a retinoblastoma protein homolog in Chlamydomonas.
Umen JG, Goodenough UW., Genes Dev. 15(13), 2001
PMID: 11445540
The retinoblastoma family: twins or distant cousins?
Claudio PP, Tonini T, Giordano A., Genome Biol. 3(9), 2002
PMID: 12225593
Linking cyclins to transcriptional control.
Coqueret O., Gene 299(1-2), 2002
PMID: 12459251
The retinoblastoma tumour suppressor in development and cancer.
Classon M, Harlow E., Nat. Rev. Cancer 2(12), 2002
PMID: 12459729
A revised picture of the E2F transcriptional network and RB function.
Stevaux O, Dyson NJ., Curr. Opin. Cell Biol. 14(6), 2002
PMID: 12473340
Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence.
Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, Spector DL, Hannon GJ, Lowe SW., Cell 113(6), 2003
PMID: 12809602
Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry.
Sage J, Miller AL, Perez-Mancera PA, Wysocki JM, Jacks T., Nature 424(6945), 2003
PMID: 12853964

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 18790828
PubMed | Europe PMC

Suchen in

Google Scholar