Skip to main content
Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2010 Aug 13;16(1):3–18. doi: 10.1007/s12298-010-0005-y

The MIDASIN and NOTCHLESS genes are essential for female gametophyte development in Arabidopsis thaliana

Sier-Ching Chantha 1, Madoka Gray-Mitsumune 1, Josée Houde 1, Daniel P Matton 1,
PMCID: PMC3550630  PMID: 23572950

Abstract

Female gametophyte development in Arabidopsis thaliana follows a well-defined program that involves many fundamental cellular processes. In this study, we report the involvement of the Arabidopsis thaliana MIDASIN1 (AtMDN1) gene during female gametogenesis through the phenotypic characterization of plants heterozygous for an insertional mdn1 mutant allele. The MDN1 yeast ortholog has previously been shown to encode a non-ribosomal protein involved in the maturation and assembly of the 60S ribosomal subunit. Heterozygous MDN1/mdn1 plants were semisterile and mdn1 allele transmission through the female gametophyte was severely affected. Development of mdn1 female gametophyte was considerably delayed compared to their wild-type siblings. However, delayed mdn1 female gametophytes were able to reach maturity and a delayed pollination experiment showed that a small proportion of the female gametophytes were functional. We also report that the Arabidopsis NOTCHLESS (AtNLE) gene is also required for female gametogenesis. The NLE protein has been previously shown to interact with MDN1 and to be also involved in 60S subunit biogenesis. The introduction of an AtNLE-RNA interference construct in Arabidopsis led to semisterility defects. Defective female gametophytes were mostly arrested at the one-nucleate (FG1) developmental stage. These data suggest that the activity of both AtMDN1 and AtNLE is essential for female gametogenesis progression.

Keywords: Female gametophyte, Embryo sac, Gametogenesis, Midasin, Notchless, Ribosome biogenesis

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

References

  1. Acosta-Garcia G., Vielle-Calzada J.P. A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell. 2004;16:2614–2628. doi: 10.1105/tpc.104.024588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., Gadrinab C., Heller C., Jeske A., Koesema E., Meyers C.C., Parker H., Prednis L., Ansari Y., Choy N., Deen H., Geralt M., Hazari N., Hom E., Karnes M., Mulholland C., Ndubaku R., Schmidt I., Guzman P., Aguilar-Henonin L., Schmid M., Weigel D., Carter D.E., Marchand T., Risseeuw E., Brogden D., Zeko A., Crosby W.L., Berry C.C., Ecker J.R. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301:653–657. doi: 10.1126/science.1086391. [DOI] [PubMed] [Google Scholar]
  3. Bajon C., Horlow C., Motamayor J.C., Sauvanet A., Robert D. Megasporogenesis in Arabidopsis thaliana L.: An ultrastructural study. Sexual Plant Reproduction. 1999;12:99–109. doi: 10.1007/s004970050178. [DOI] [Google Scholar]
  4. Bassler J., Grandi P., Gadal O., Lessmann T., Petfalski E., Tollervey D., Lechner J., Hurt E. Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell. 2001;8:517–529. doi: 10.1016/S1097-2765(01)00342-2. [DOI] [PubMed] [Google Scholar]
  5. Brukhin V., Curtis M.D., Grossniklaus U. The angiosperm female gametophyte: no longer the forgotten generation. Current Science. 2005;89:1844–1852. [Google Scholar]
  6. Capron A., Serralbo O., Fulop K., Frugier F., Parmentier Y., Dong A., Lecureuil A., Guerche P., Kondorosi E., Scheres B., Genschik P. The Arabidopsis anaphasepromoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell. 2003;15:2370–2382. doi: 10.1105/tpc.013847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chantha S.C., Emerald B.S., Matton D.P. Characterization of the plant Notchless homolog, a WD repeat protein involved in seed development. Plant Mol. Biol. 2006;62:897–912. doi: 10.1007/s11103-006-9064-4. [DOI] [PubMed] [Google Scholar]
  8. Chantha S.C., Matton D.P. Underexpression of the plant NOTCHLESS gene, encoding a WD repeat protein, causes pleitropic phenotype during plant development. Planta. 2007;225:1107–1120. doi: 10.1007/s00425-006-0420-z. [DOI] [PubMed] [Google Scholar]
  9. Christensen C.A., King E.J., Jordan J.R., Drews G.N. Megagametogenesis in Arabidopsis wild-type and Gf mutant. Sexual Plant Reproduction. 1997;10:49–64. doi: 10.1007/s004970050067. [DOI] [Google Scholar]
  10. Christensen C.A., Subramanian S., Drews G.N. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. 1998;202:136–151. doi: 10.1006/dbio.1998.8980. [DOI] [PubMed] [Google Scholar]
  11. Christensen C.A., Gorsich S.W., Brown R.H., Jones L.G., Brown J., Shaw J.M., Drews G.N. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell. 2002;14:2215–2232. doi: 10.1105/tpc.002170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. SJ C., AF B. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x. [DOI] [PubMed] [Google Scholar]
  13. Cormier S., Le Bras S., Souilhol C., Vandormael-Pournin S., Durand B., Babinet C., Baldacci P., Cohen-Tannoudji M. The murine ortholog of notchless, a direct regulator of the notch pathway in Drosophila melanogaster, is essential for survival of inner cell mass cells. Mol. Cell Biol. 2006;26:3541–3549. doi: 10.1128/MCB.26.9.3541-3549.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. de la Cruz J., Sanz-Martinez E., Remacha M. The essential WD-repeat protein Rsa4p is required for rRNA processing and intra-nuclear transport of 60S ribosomal subunits. Nucleic Acids Res. 2005;33:5728–5739. doi: 10.1093/nar/gki887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drews G.N., Lee D., Christensen C.A. Genetic analysis of female gametophyte development and function. Plant Cell. 1998;10:5–17. doi: 10.1105/tpc.10.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Drews G.N., Yadegari R. Development and function of the angiosperm female gametophyte. Annu. Rev. Genet. 2002;36:99–124. doi: 10.1146/annurev.genet.36.040102.131941. [DOI] [PubMed] [Google Scholar]
  17. Ebel C., Mariconti L., Gruissem W. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature. 2004;429:776–780. doi: 10.1038/nature02637. [DOI] [PubMed] [Google Scholar]
  18. Elbashir S.M., Martinez J., Patkaniowska A., Lendeckel W., Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. Embo J. 2001;20:6877–6888. doi: 10.1093/emboj/20.23.6877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Estrada-Luna A.A., Garcia-Aguilar M., Vielle-Calzada J.-P. Female reproductive development and pollen tube growth in diploid genotypes of Solanum cardiophyllum Lindl. Sexual Plant Reproduction. 2004;17:117–124. doi: 10.1007/s00497-004-0219-7. [DOI] [Google Scholar]
  20. Fatica A., Tollervey D. Making ribosomes. Curr. Opin. Cell Biol. 2002;14:313–318. doi: 10.1016/S0955-0674(02)00336-8. [DOI] [PubMed] [Google Scholar]
  21. Feldmann K.A., Coury D.A., Christianson M.L. Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics. 1997;147:1411–1422. doi: 10.1093/genetics/147.3.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fromont-Racine M., Senger B., Saveanu C., Fasiolo F. Ribosome assembly in eukaryotes. Gene. 2003;313:17–42. doi: 10.1016/S0378-1119(03)00629-2. [DOI] [PubMed] [Google Scholar]
  23. Galani K., Nissan T.A., Petfalski E., Tollervey D., Hurt E. Rea1, a dynein-related nuclear AAA-ATPase, is involved in late rRNA processing and nuclear export of 60 S subunits. J. Biol. Chem. 2004;279:55411–55418. doi: 10.1074/jbc.M406876200. [DOI] [PubMed] [Google Scholar]
  24. Garbarino J.E., Gibbons I.R. Expression and genomic analysis of midasin, a novel and highly conserved AAA protein distantly related to dynein. BMC Genomics. 2002;3:18. doi: 10.1186/1471-2164-3-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gavin A.C., Bosche M., Krause R., Grandi P., Marzioch M., Bauer A., Schultz J., Rick J.M., Michon A.M., Cruciat C.M., Remor M., Hofert C., Schelder M., Brajenovic M., Ruffner H., Merino A., Klein K., Hudak M., Dickson D., Rudi T., Gnau V., Bauch A., Bastuck S., Huhse B., Leutwein C., Heurtier M.A., Copley R.R., Edelmann A., Querfurth E., Rybin V., Drewes G., Raida M., Bouwmeester T., Bork P., Seraphin B., Kuster B., Neubauer G., Superti-Furga G. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature. 2002;415:141–147. doi: 10.1038/415141a. [DOI] [PubMed] [Google Scholar]
  26. Grossniklaus U., Schneitz K. The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev. Biol. 1998;9:227–238. doi: 10.1006/scdb.1997.0214. [DOI] [PubMed] [Google Scholar]
  27. Henras A., Henry Y., Bousquet-Antonelli C., Noaillac-Depeyre J., Gelugne J.P., Caizergues-Ferrer M. Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. Embo J. 1998;17:7078–7090. doi: 10.1093/emboj/17.23.7078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Howden R., Park S.K., Moore J.M., Orme J., Grossniklaus U., Twell D. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics. 1998;149:621–631. doi: 10.1093/genetics/149.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Huanca-Mamani W., Garcia-Aguilar M., Leon-Martinez G., Grossniklaus U., Vielle-Calzada J.P. CHR11, a chromatin-remodeling factor essential for nuclear proliferation during female gametogenesis in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2005;102:17231–17236. doi: 10.1073/pnas.0508186102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. B-Q H., SD R. Female germ unit: organization, isolation, and fonction. Int. Rev. Cytol. 1992;140:233–292. doi: 10.1016/S0074-7696(08)61099-2. [DOI] [Google Scholar]
  31. Iyer L.M., Leipe D.D., Koonin E.V., Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 2004;146:11–31. doi: 10.1016/j.jsb.2003.10.010. [DOI] [PubMed] [Google Scholar]
  32. Kerschen A., Napoli C.A., Jorgensen R.A., Muller A.E. Effectiveness of RNA interference in transgenic plants. FEBS Lett. 2004;566:223–228. doi: 10.1016/j.febslet.2004.04.043. [DOI] [PubMed] [Google Scholar]
  33. Kwee H.S., Sundaresan V. The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis. Plant J. 2003;36:853–866. doi: 10.1046/j.1365-313X.2003.01925.x. [DOI] [PubMed] [Google Scholar]
  34. Lagace M., Chantha S.C., Major G., Matton D.P. Fertilization induces strong accumulation of a histone deacetylase (HD2) and of other chromatin-remodeling proteins in restricted areas of the ovules. Plant Mol. Biol. 2003;53:759–769. doi: 10.1023/B:PLAN.0000023665.36676.89. [DOI] [PubMed] [Google Scholar]
  35. McCormick S. Male Gametophyte Development. Plant Cell. 1993;5:1265–1275. doi: 10.1105/tpc.5.10.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nissan T.A., Bassler J., Petfalski E., Tollervey D., Hurt E. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. Embo J. 2002;21:5539–5547. doi: 10.1093/emboj/cdf547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. O’Brien M., Kapfer C., Major G., Laurin M., Bertrand C., Kondo K., Kowyama Y., Matton D.P. Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J. 2002;32:985–996. doi: 10.1046/j.1365-313X.2002.01486.x. [DOI] [PubMed] [Google Scholar]
  38. Pagnussat G.C., Yu H.J., Ngo Q.A., Rajani S., Mayalagu S., Johnson C.S., Capron A., Xie L.F., Ye D., Sundaresan V. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development. 2005;132:603–614. doi: 10.1242/dev.01595. [DOI] [PubMed] [Google Scholar]
  39. Ramakrishnan C., Dani V.S., Ramasarma T. A conformational analysis of Walker motif A [GXXXXGKT (S)] in nucleotide-binding and other proteins. Protein Engineering. 2002;15:783–798. doi: 10.1093/protein/15.10.783. [DOI] [PubMed] [Google Scholar]
  40. Royet J., Bouwmeester T., Cohen S.M. Notchless encodes a novel WD40-repeat-containing protein that modulates Notch signaling activity. Embo J. 1998;17:7351–7360. doi: 10.1093/emboj/17.24.7351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schneitz K., Hülskamp M., Pruitt R.E. Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant Journal. 1995;7:731–749. doi: 10.1046/j.1365-313X.1995.07050731.x. [DOI] [Google Scholar]
  42. Shi D.Q., Liu J., Xiang Y.H., Ye D., Sundaresan V., Yang W.C. SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell. 2005;17:2340–2354. doi: 10.1105/tpc.105.033563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Smyth D.R., Bowman J.L., Meyerowitz E.M. Early flower development in Arabidopsis. Plant Cell. 1990;2:755–767. doi: 10.1105/tpc.2.8.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Springer P.S., McCombie W.R., Sundaresan V., Martienssen R.A. Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science. 1995;268:877–880. doi: 10.1126/science.7754372. [DOI] [PubMed] [Google Scholar]
  45. Tschochner H., Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 2003;13:255–263. doi: 10.1016/S0962-8924(03)00054-0. [DOI] [PubMed] [Google Scholar]
  46. Ulbrich C., Diepholz M., Bassler J., Kressler D., Pertschy B., Galani K., Bottcher B., Hurt E. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell. 2009;138:911–922. doi: 10.1016/j.cell.2009.06.045. [DOI] [PubMed] [Google Scholar]
  47. Whittaker C.A., Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 2002;13:3369–3387. doi: 10.1091/mbc.E02-05-0259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Willemse M.T.M., van Went J.L. The female gametophyte. In: Johri B.M., editor. Embryology of Angiosperms. Berlin: Springer-Verlag; 1984. pp. 159–196. [Google Scholar]
  49. Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 2004;136:2621–2632. doi: 10.1104/pp.104.046367. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Physiology and molecular biology of plants : an international journal of functional plant biology are provided here courtesy of Springer

RESOURCES