Members of the RKD transcription factor family induce an egg cell-like gene expression program

Plant Journal

Volumn 67, Issue 2, 2011, Pages 280-291

  Köszegi, Dávid ^a   Johnston, Amal J ^a   Rutten, Twan ^a   Czihal, Andreas ^a   Altschmied, Lothar ^a   Kumlehn, Jochen ^a   Wüst, Samuel E J ^b,c   Kirioukhova, Olga ^a,b   Gheyselinck, Jacqueline ^b,d   Grossniklaus, Ueli ^b   Bäumlein, Helmut ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Arabidopsis; egg cell; female gametophyte; RKD; transcription factor; transcriptome; wheat

Indexed keywords

ARABIDOPSIS; EGG CELLS; FEMALE GAMETOPHYTES; RKD; TRANSCRIPTOMES; WHEAT;

ANIMALS; CELL PROLIFERATION; CYTOLOGY; GENES; PLANTS (BOTANY); TRANSCRIPTION; TRANSCRIPTION FACTORS;

CELLS;

TRANSCRIPTION FACTOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MULTIGENE FAMILY; OVULE; PROMOTER REGION; PROTOPLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT; WHEAT;

ARABIDOPSIS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, PLANT; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; OVULE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTOPLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TRITICUM;

ANIMALIA; ARABIDOPSIS; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; MAGNOLIOPHYTA; TRITICUM AESTIVUM;

EID: 79957467977     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04592.x     Document Type: Article

References (69)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
2. Berardini, T.Z., Mundodi, S., Reiser, L., et al. (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 135, 745-755. (Pubitemid 38819021)
3. Bevan, M., (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711-8721.
4. Borisov, A.Y., Madsen, L.H., Tsyganov, V.E., et al. (2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol. 131, 1009-1017. (Pubitemid 36405304)
5. Brown, R.C., and, Lemmon, B.C., (1992) Cytoplasmic domain: a model for spatial control of cytokinesis in reproductive cells of plants. EMSA Bull. 22, 48-53.
6. Brownfield, L., Hafidh, S., Borg, M., Sidorova, A., Mori, T., and, Twell, D., (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet. 5, e1000430.
7. Chevreux, B., Pfister, T., Drescher, B., Driesel, A.J., Muller, W.E., Wetter, T., and, Suhai, S., (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14, 1147-1159. (Pubitemid 38811551)
8. Christensen, C.A., Subramanian, S., and, Drews, G.N., (1998) Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. 202, 136-151. (Pubitemid 28467253)
9. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
10. Cordts, S., Bantin, J., Wittich, P.E., Kranz, E., Lorz, H., and, Dresselhaus, T., (2001) ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J. 25, 103-114. (Pubitemid 32143330)
11. Coury, D.A., Zhang, C., Ko, A., Skaggs, M.I., Christensen, C.A., Drews, G.N., Feldmann, K.A., and, Yadegari, R., (2007) Segregation distortion in Arabidopsis gametophytic factor 1 (gfa1) mutants is caused by a deficiency of an essential splicing factor. Sex. Plant Reprod. 20, 87-97. (Pubitemid 46790927)
12. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469. (Pubitemid 37325657)
13. Ebel, C., Mariconti, L., and, Gruissem, W., (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature, 429, 776-780. (Pubitemid 38833130)
14. Evans, M.M., (2007) The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell, 19, 46-62. (Pubitemid 46852700)
15. Ferris, P.J., and, Goodenough, U.W., (1997) Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics, 146, 859-869. (Pubitemid 27290972)
16. Gross-Hardt, R., Kagi, C., Baumann, N., Moore, J.M., Baskar, R., Gagliano, W.B., Jurgens, G., and, Grossniklaus, U., (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol. 5, e47.
17. Grossniklaus, U., and, Schneitz, K., (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin. Cell Dev. Biol. 9, 227-238. (Pubitemid 128352276)
18. Hallmann, A., (2011) Evolution of reproductive development in the volvocine algae. Sex. Plant Reprod., doi:.
19. Hofmeister, W., (1851) Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farrn, Equisetaceen, Rhizocarpeen und Lycopodiaceen) und die Samenbildung der Coniferen. Vergleichende Untersuchungen der Keimung.
20. Ingouff, M., Sakata, T., Li, J., Sprunck, S., Dresselhaus, T., and, Berger, F., (2009) The two male gametes share equal ability to fertilize the egg cell in Arabidopsis thaliana. Curr. Biol. 19, R19-R20.
21. Ivanov, R., Tiedemann, J., Czihal, A., Schallau, A., Le, H.D., Mock, H.P., Claus, B., Tewes, A., and, Bäumlein, H., (2008) EFFECTOR OF TRANSCRIPTION2 is involved in xylem differentiation and includes a functional DNA single strand cutting domain. Dev. Biol. 313, 93-106. (Pubitemid 350298303)
22. Jefferson, R.A., Kavanagh, T.A., and, Bevan, M.W., (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
23. Johnston, A.J., Meier, P., Gheyselinck, J., Wuest, S.E., Federer, M., Schlagenhauf, E., Becker, J.D., and, Grossniklaus, U., (2007) Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol. 8, R204.
24. Johnston, A.J., Matveeva, E., Kirioukhova, O., Grossniklaus, U., and, Gruissem, W., (2008) A dynamic reciprocal RBR-PRC2 regulatory circuit controls Arabidopsis gametophyte development. Curr. Biol. 18, 1680-1686.
25. Johnston, A.J., Kirioukhova, O., Barrell, P.J., Moore, J.M., Baskar, R., Grossniklaus, U., and, Gruissem, W., (2010) Dosage-sensitive function of RETINOBLASTOMA-RELATED and convergent epigenetic control are required during the Arabidopsis life cycle. PLoS Genet. 6, e1000988.
26. Jones-Rhoades, M.W., Borevitz, J.O., and, Preuss, D., (2007) Genome-wide expression profiling of the Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genet. 3, 1848-1861. (Pubitemid 350072051)
27. Kägi, C., Baumann, N., Nielsen, N., Stierhof, Y.D., and, Gross-Hardt, R., (2010) The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells. Proc. Natl Acad. Sci. USA, 107, 22350-22355.
28. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
29. Kerk, N.M., Ceserani, T., Tausta, S.L., Sussex, I.M., and, Nelson, T.M., (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol. 132, 27-35. (Pubitemid 36590398)
30. Koltunow, A.M., and, Grossniklaus, U., (2003) Apomixis: a developmental perspective. Annu. Rev. Plant Biol. 54, 547-574. (Pubitemid 37400005)
31. Kumlehn, J., Loerz, H., and, Kranz, E., (1998) Differentiation of isolated wheat zygotes into embryos and normal plants. Planta 205, 327-333. (Pubitemid 28276344)
32. Kumlehn, J., Kirik, V., Czihal, A., Altschmied, L., Matzk, F., Lörz, H., and, Bäumlein, H., (2001) Parthenogenetic egg cells in wheat: cellular and molecular studies. Sex. Plant Reprod. 14, 239-243. (Pubitemid 34018139)
33. Le, Q., Gutierrez-Marcos, J.F., Costa, L.M., Meyer, S., Dickinson, H.G., Lorz, H., Kranz, E., and, Scholten, S., (2005) Construction and screening of subtracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene expression between maize egg cells and central cells. Plant J. 44, 167-178.
34. Le, B.H., Cheng, C., Bui, A.Q., et al. (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl Acad. Sci. USA, 107, 8063-8070.
35. Li, C., and, Wong, W.H., (2001a) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA, 98, 31-36. (Pubitemid 32095858)
36. Li, C., and, Wong, W.H., (2001b) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2, R0032.
37. Lin, H., and, Goodenough, U.W., (2007) Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics, 176, 913-925. (Pubitemid 46961095)
38. Marsh, J.F., Rakocevic, A., Mitra, R.M., Brocard, L., Sun, J., Eschstruth, A., Long, S.R., Schultze, M., Ratet, P., and, Oldroyd, G.E., (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144, 324-335. (Pubitemid 46941636)
39. Moll, C., von Lyncker, L., Zimmermann, S., Kagi, C., Baumann, N., Twell, D., Grossniklaus, U., and, Gross-Hardt, R., (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56, 913-921.
40. Moore, J.M., Calzada, J.P., Gagliano, W., and, Grossniklaus, U., (1997) Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harb. Symp. Quant. Biol. 62, 35-47. (Pubitemid 28198519)
41. Nozaki, H., Mori, T., Misumi, O., Matsunaga, S., and, Kuroiwa, T., (2006) Males evolved from the dominant isogametic mating type. Curr. Biol. 16, R1018-R1020. (Pubitemid 44894921)
42. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D., and, Sundaresan, V., (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development, 132, 603-614. (Pubitemid 40277699)
43. Pagnussat, G.C., Yu, H.J., and, Sundaresan, V., (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell, 19, 3578-3592.
44. Pagnussat, G.C., Alandete-Saez, M., Bowman, J.L., and, Sundaresan, V., (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science, 324, 1684-1689.
45. Riano-Pachon, D.M., Correa, L.G., Trejos-Espinosa, R., and, Mueller-Roeber, B., (2008) Green transcription factors: a chlamydomonas overview. Genetics, 179, 31-39.
46. Richert, J., Kranz, E., Lörz, H., and, Dresselhaus, T., (1996) A reverse transcriptase polymerase chain reaction assay for gene expression studies at the single cell level. Plant Sci. 114, 93-99.
47. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and, Weisshaar, B., (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53, 247-259. (Pubitemid 38105653)
48. Sambrook, J., Fritsch, E.F., and, Maniatis, T., (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
49. Schauser, L., Roussis, A., Stiller, J., and, Stougaard, J., (1999) A plant regulator controlling development of symbiotic root nodules. Nature, 402, 191-195.
50. Schauser, L., Wieloch, W., and, Stougaard, J., (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J. Mol. Evol. 60, 229-237. (Pubitemid 40568861)
51. Smyth, G.K., (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
52. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767. (Pubitemid 120015483)
53. Sprunck, S., and, Gross-Hardt, R., (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex. Plant Reprod., doi:.
54. Sprunck, S., Baumann, U., Edwards, K., Langridge, P., and, Dresselhaus, T., (2005) The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.). Plant J. 41, 660-672. (Pubitemid 40335998)
55. Srilunchang, K.O., Krohn, N.G., and, Dresselhaus, T., (2010) DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development, 137, 333-345.
56. Steffen, J.G., Kang, I.H., Macfarlane, J., and, Drews, G.N., (2007) Identification of genes expressed in the Arabidopsis female gametophyte. Plant J. 51, 281-292. (Pubitemid 47030122)
57. Suzuki, R., and, Shimodaira, H., (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540-1542. (Pubitemid 43985330)
58. Tam, L.W., and, Kirk, D.L., (1991) The program for cellular differentiation in Volvox carteri as revealed by molecular analysis of development in a gonidialess/somatic regenerator mutant. Development, 112, 571-580.
59. Vielle-Calzada, J.P., Thomas, J., Spillane, C., Coluccio, A., Hoeppner, M.A., and, Grossniklaus, U., (1999) Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13, 2971-2982.
60. Webb, M.C., and, Gunning, B.E.S., (1990) Embryo sac development in Arabidopsis thaliana. 1. Megasporogenesis, including the microtubular cytoskeleton. Sex. Plant Reprod. 3, 244-256.
61. Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I., Korthout, H., Chatterjee, J., Mariconti, L., Gruissem, W., and, Scheres, B., (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell, 123, 1337-1349. (Pubitemid 41821789)
62. Wuest, S.E., Vijverberg, K., Schmidt, A., Weiss, M., Gheyselinck, J., Lohr, M., Wellmer, F., Rahnenfuhrer, J., von Mering, C., and, Grossniklaus, U., (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20, 506-512.
63. Wyrzykowska, J., Schorderet, M., Pien, S., Gruissem, W., and, Fleming, A.J., (2006) Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol. 141, 1338-1348. (Pubitemid 44223286)
64. Yadegari, R., and, Drews, G.N., (2004) Female gametophyte development. Plant Cell, 16 (Suppl), S133-S141. (Pubitemid 38774223)
65. Yamanaka, S., (2008) Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif. 41 (Suppl 1), 51-56. (Pubitemid 350295862)
66. Yang, H., Kaur, N., Kiriakopolos, S., and, McCormick, S., (2006) EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. Planta, 224, 1004-1014. (Pubitemid 44435851)
67. Yu, H.J., Hogan, P., and, Sundaresan, V., (2005) Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol. 139, 1853-1869. (Pubitemid 43899823)
68. Zhong, L.P., Yang, X., Zhang, L., Wei, K.J., Pan, H.Y., Zhou, X.J., Li, J., Chen, W.T., and, Zhang, Z.Y., (2008) Overexpression of insulin-like growth factor binding protein 3 in oral squamous cell carcinoma. Oncol. Rep. 20, 1441-1447.
69. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632. (Pubitemid 41071302)