Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates

Genes and Development

Volumn 27, Issue 10, 2013, Pages 1198-1215

  Ning, Jue ^a   Otto, Thomas D ^b   Pfander, Claudia ^b   Schwach, Frank ^b   Brochet, Mathieu ^b   Bushell, Ellen ^b   Goulding, David ^b   Sanders, Mandy ^b   Lefebvre, Paul A ^c   Pei, Jimin ^a,d   Grishin, Nick V ^a,d   Vanderlaan, Gary ^a   Billker, Oliver ^b   Snell, William J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Chlamydomonas; Fertilization; KAR5 GEX1 Brambleberry; Nuclear envelope fusion; Plasmodium; RNA sequencing

Indexed keywords

ARTICLE; CHLAMYDOMONAS; COMPARATIVE GENOMIC HYBRIDIZATION; CYTOLOGY; DISEASE TRANSMISSION; FERTILIZATION; FUNGUS; MALARIA; NONHUMAN; PLANT; PLASMODIUM; PRIORITY JOURNAL; PROGENY; PROTEIN FUNCTION; PROTIST; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; TRANSCRIPTOMICS; VERTEBRATE;

CHLAMYDOMONAS; FERTILIZATION; KAR5/GEX1/BRAMBLEBERRY; NUCLEAR ENVELOPE FUSION; PLASMODIUM; RNA SEQUENCING;

ANIMALS; ARABIDOPSIS PROTEINS; CHLAMYDOMONAS; FERTILIZATION; FUNGI; GENE EXPRESSION PROFILING; GENES, ESSENTIAL; MEIOSIS; MEMBRANE PROTEINS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PLANTS; PLASMODIUM; REPRODUCTION; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTOME; VERTEBRATES;

EID: 84877946500     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.212746.112     Document Type: Article

References (55)

1. Abrams E.W., Zhang H, Marlow FL, Kapp L, Lu S, Mullins MC. 2012. Dynamic assembly of brambleberry mediates nuclear envelope fusion during early development. Cell 150: 521-532.
2. Adair W.S., Apt KE. 1990. Cell wall regeneration in Chlamydomonas: Accumulation of mRNAs encoding cell wall hydroxyproline-rich glycoproteins. Proc Natl Acad Sci 87: 7355-7359.
3. Alandete-Saez M, Ron M, Leiboff S, McCormick S. 2011. Arabidopsis thaliana GEX1 has dual functions in gametophyte development and early embryogenesis. Plant J 68: 620-632.
4. Apweiler R., Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, et al. 2004. UniProt: The Universal Protein knowledgebase. Nucleic Acids Res 32: D115-D119.
5. Beh C.T., Brizzio V, Rose MD. 1997. KAR5 encodes a novel pheromone-inducible protein required for homotypic nuclear fusion. J Cell Biol 139: 1063-1076.
6. Bentley D.R., Balasubramanian S, Swerdlow HP, Smith GP, Milton J., Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, et al. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
7. Billker O., Dechamps S, Tewari R, Wenig G, Franke-Fayard B, Brinkmann V. 2004. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503-514.
8. Buchanan M.J., Snell WJ. 1985. Characterization of the walldegrading enzyme, lysin, released by Chlamydomonas gametes. J Cell Biol 101: 379a.
9. Buchanan M.J., Snell WJ. 1988. Biochemical studies on lysin, a cell wall degrading enzyme released during fertilization in Chlamydomonas. Exp Cell Res 179: 181-193.
10. Bushell E.S., Ecker A, Schlegelmilch T, Goulding D, Dougan G, Sinden R.E., Christophides GK, Kafatos FC, Vlachou D. 2009. Paternal effect of the nuclear formin-like protein MISFIT on Plasmodium development in the mosquito vector. PLoS Pathog 5: e1000539.
11. Ferris P.J., Goodenough UW. 1997. Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146: 859-869.
12. Ferris P.J., Armbrust EV, Goodenough UW. 2002. Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160: 181-200.
13. Finn R.D., Clements J, Eddy SR. 2011. HMMER Web server: Interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
14. Godl K., Hallmann A, Wenzl S, Sumper M. 1997. Differential targeting of closely related ECM glycoproteins: The pherophorin family from Volvox. EMBO J 16: 25-34.
15. Gonzalez-Ballester D, Pootakham W, Mus F, Yang W, Catalanotti C, Magneschi L, de Montaigu A, Higuera JJ, Prior M, Galvan A, et al. 2011. Reverse genetics in Chlamydomonas: A platform for isolating insertional mutants. Plant Methods 7: 24.
16. Grossmann S., Bauer S, Robinson PN, Vingron M. 2007. Improved detection of overrepresentation of gene-ontology annotations with parent child analysis. Bioinformatics 23: 3024-3031.
17. Hirai M., Arai M, Mori T, Miyagishima SY, Kawai S, Kita K, Kuroiwa T., Terenius O, Matsuoka H. 2008. Male fertility of malaria parasites is determined by GCS1, a plant-type reproduction factor. Curr Biol 18: 607-613.
18. Janse C.J., Franke-Fayard B, Waters AP. 2006a. Selection by flowsorting of genetically transformed, GFP-expressing blood stages of the rodent malaria parasite, Plasmodium berghei. Nat Protoc 1: 614-623.
19. Janse C.J., Ramesar J, Waters AP. 2006b. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356.
20. Kurvari V. 1997. Cell wall biogenesis in Chlamydomonas-molecular characterization of a novel protein whose expression is up-regulated during matrix formation. Mol Gen Genet 256: 572-580.
21. Kurvari V., Grishin NV, Snell WJ. 1998. A gamete-specific, sexlimited homeodomain protein in Chlamydomonas. J Cell Biol 143: 1971-1980.
22. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, et al. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
23. Lin H., Goodenough UW. 2007. Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176: 913-925.
24. Liu Y., Tewari R, Ning J, Blagborough AM, Garbom S, Pei J, Grishin N.V., Steele RE, Sinden RE, Snell WJ, et al. 2008. The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 22: 1051-1068.
25. Liu Y., Misamore MJ, Snell WJ. 2010. Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy in Chlamydomonas. Development 137: 1473-1481.
26. Lodha M., Schulz-Raffelt M, Schroda M. 2008. A new assay for promoter analysis in Chlamydomonas reveals roles for heat shock elements and the TATA box in HSP70A promotermediated activation of transgene expression. Eukaryot Cell 7: 172-176.
27. López-Barragán MJ, Lemieux J, Quinones M, Williamson KC, Molina-Cruz A, Cui K, Barillas-Mury C, Zhao K, Su XZ. 2011. Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics 12: 587.
28. Merchant S.S., Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman G.B., Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L., et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
29. Misamore M.J., Gupta S, Snell WJ. 2003. The Chlamydomonas Fus1 protein is present on the mating type plus fusion organelle and required for a critical membrane adhesion event during fusion with minus gametes. Mol Biol Cell 14: 2530-2542.
30. Moon R.W., Taylor CJ, Bex C, Schepers R, Goulding D, Janse CJ, Waters A.P., Baker DA, Billker O. 2009. A cyclic GMP signalling module that regulates gliding motility in a malaria parasite. PLoS Pathog 5: e1000599.
31. Mori T., Kuroiwa H, Higashiyama T, Kuroiwa T. 2006. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8: 64-71.
32. Nishimura Y., Shikanai T, Nakamura S, Kawai-Yamada M, Uchimiya H. 2012. Gsp1 triggers the sexual developmental program including inheritance of chloroplast DNA and mitochondrial DNA in Chlamydomonas reinhardtii. Plant Cell 24: 2401-2414.
33. Notredame C., Higgins DG, Heringa J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
34. Otto T.D., Sanders M, Berriman M, Newbold C. 2010. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26: 1704-1707.
35. Pasquale S.M., Goodenough UW. 1987. Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105: 2279-2292.
36. Pfander C., Anar B, Schwach F, Otto TD, Brochet M, Volkmann K, Quail MA, Pain A, Rosen B, Skarnes W, et al. 2011. A scalable pipeline for highly effective genetic modification of a malaria parasite. Nat Methods 8: 1078-1082.
37. Schroda M., Blocker D, Beck CF. 2000. The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J 21: 121-131.
38. Shimogawara K., Fujiwara S, Grossman A, Usuda H. 1998. Highefficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148: 1821-1828.
39. Sinden R.E. 2009. Malaria, sexual development and transmission: Retrospect and prospect. Parasitology 136: 1427-1434.
40. Sinden R.E., Canning EU, Spain B. 1976. Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: A transmission electron microscope study. Proc R Soc Lond B Biol Sci 193: 55-76.
41. Sinden R.E., Butcher GA, Billker O, Fleck SL. 1996. Regulation of infectivity of Plasmodium to the mosquito vector. Adv Parasitol 38: 53-117.
42. Sizova I., Fuhrmann M, Hegemann P. 2001. A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 277: 221-229.
43. Snell W.J. 1982. Study of the release of cell wall degrading enzymes during adhesion of Chlamydomonas gametes. Exp Cell Res 138: 109-119.
44. Snell W.J., Goodenough UW. 2009. Flagellar adhesion: Flagellar generated signaling and gamete fusion during mating. In The Chlamydomonas sourcebook (ed. Witman GB), pp. 369-394. Elsevier, San Diego.
45. Specht M., Stanke M, Terashima M, Naumann-Busch B, Janssen I, Hohner R, Hom EF, Liang C, Hippler M. 2011. Concerted action of the new Genomic Peptide Finder and AUGUSTUS allows for automated proteogenomic annotation of the Chlamydomonas reinhardtii genome. Proteomics 11: 1814-1823.
46. Stanke M., Diekhans M, Baertsch R, Haussler D. 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637-644.
47. Trapnell C., Pachter L, Salzberg SL. 2009. TopHat: Discovering splice junctions with RNA-seq. Bioinformatics 25: 1105-1111.
48. van Dijk MR, Janse CJ, Thompson J, Waters AP, Braks JA, Dodemont H.J., Stunnenberg HG, van Gemert GJ, Sauerwein RW, Eling W. 2001. A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153-164.
49. von Besser K, Frank AC, Johnson MA, Preuss D. 2006. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133: 4761-4769.
50. Wang Z., Gerstein M, Snyder M. 2009. RNA-seq: A revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
51. Ward J.J. 1963. Hierarchical grouping to optimize an objective function. Amer StatistAssoc 58: 236-244.
52. Wegener D., Beck CF. 1991. Identification of novel genes specifically expressed in Chlamydomonas reinhardtii zygotes. Plant Mol Biol 16: 937-946.
53. Wegener D., Treier U, Beck CF. 1989. Procedures for the generation of mature Chlamydomonas reinhardtii zygotes for molecular and biochemical analyses. Plant Physiol 90: 512-515.
54. Winck F.V., Kwasniewski M, Wienkoop S, Mueller-Roeber B. 2011. An optimized method for the isolation of nuclei from Chlamydomonas reinhardtii (chlorophyceae). J Phycol 47: 333-340.
55. Wong JL., Johnson MA. 2010. Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol 20: 134-141.