Abstract
WD-repeat proteins are involved in a breadth of cellular processes. While the WD-repeat protein encoding gene NOTCHLESS has been involved in the regulation of the Notch signaling pathway in Drosophila, its yeast homolog Rsa4p was shown to participate in 60S ribosomal subunit biogenesis. The plant homolog ScNLE was previously characterized in Solanum chacoense (ScNLE) as being involved in seed development. However, expression data and reduced size of ScNLE underexpressing plants suggested in addition a role during shoot development. We here report the detailed phenotypic characterization of ScNLE underexpressing plants during shoot development. ScNLE was shown to be expressed in actively dividing cells of the shoot apex. Consistent with this, ScNLE underexpression caused pleiotropic defects such as a reduction in aerial organ size, a reduction in some organ numbers, delayed flowering, and an increase in stomatal index. Analysis of adaxial epidermal cells revealed that both cell number and cell size were reduced in mature leaves of ScNLE underexpressing lines. Two-hybrid screens with the Nle domain and the WD-repeat domain of ScNLE allowed the isolation of homologs of yeast MIDASIN and NSA2 genes, the products of which are involved in 60S ribosomal subunit biogenesis in yeast. A ScNLE-GFP chimeric protein was localized in both the cytoplasm and nucleus. These data altogether suggest that ScNLE likely plays a role in 60S ribosomal subunit biogenesis, which is essential for proper cellular growth and proliferation during plant development.
Similar content being viewed by others
Abbreviations
- DAP:
-
Days after pollination
- HAP:
-
Hours after pollination
- SAM:
-
Shoot apical meristem
References
Agatep R, Kirkpatrick RD, Parchaliuk DL, Woods RA, Gietz RD (1998) Transformation of Saccharomyces cerevisiae by the lithium acetate/single-stranded carrier DNA/polyethylene glycol (LiAc/ss-DNA/PEG) protocol. Technical Tips. Online: http://www.tto.trends.com
Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inze D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21:6036–6049
Bassler J, Grandi P, Gadal O, Lessmann T, Petfalski E, Tollervey D, Lechner J, Hurt E (2001) Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol Cell 8:517–529
Bussiere F, Ledu S, Girard M, Heroux M, Perreault J-P, Matton DP (2003) Development of an efficient cis–trans–cis ribozyme cassette to inactivate plant genes. Plant Biotechnol J 1:423–435
Chantha SC, Emerald BS, Matton DP (2006) Characterization of the plant Notchless homolog, a WD repeat protein involved in seed development. Plant Mol Biol (in press). DOI 10.1007/s11103-006-9064-4
Clarke AE (1940) Fertilization and early embryo development in the potato. Am Potato J 17:20–25
de la Cruz J, Sanz-Martinez E, Remacha M (2005) The essential WD-repeat protein Rsa4p is required for rRNA processing and intra-nuclear transport of 60S ribosomal subunits. Nucleic Acids Res 33:5728–5739
De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668
Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New York
Galani K, Nissan TA, Petfalski E, Tollervey D, Hurt E (2004) Rea1, a dynein-related nuclear AAA-ATPase, is involved in late rRNA processing and nuclear export of 60S subunits. J Biol Chem 279:55411–55418
Garbarino JE, Gibbons IR (2002) Expression and genomic analysis of midasin, a novel and highly conserved AAA protein distantly related to dynein. BMC Genom 3:18
Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, 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 MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141–147
Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086
Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391
Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96
Hemerly A, Engler Jde A, Bergounioux C, Van Montagu M, Engler G, Inze D, Ferreira P (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J 14:3925–3936
James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425–1436
Kimble J, Simpson P (1997) The LIN-12/Notch signaling pathway and its regulation. Annu Rev Cell Dev Biol 13:333–361
Koop HU, Steinmuller K, Wagner H, Rossler C, Eibl C, Sacher L (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199:193–201
Lagacé M, Chantha SC, Major G, Matton DP (2003) Fertilization induces strong accumulation of a histone deacetylase (HD2) and of other chromatin-remodeling proteins in restricted areas of the ovules. Plant Mol Biol 53:759–769
Lahmy S, Guilleminot J, Cheng CM, Bechtold N, Albert S, Pelletier G, Delseny M, Devic M (2004) DOMINO1, a member of a small plant-specific gene family, encodes a protein essential for nuclear and nucleolar functions. Plant J 39:809–820
Lantin S, O’Brien M, Matton DP (1999) Pollination, wounding and jasmonate treatments induce the expression of a developmentally regulated pistil dioxygenase at a distance, in the ovary, in the wild potato Solanum chacoense Bitt. Plant Mol Biol 41:371–386
Liu J, Jambunathan N, McNellis TW (2005) Transgenic expression of the von Willebrand A domain of the BONZAI 1/COPINE 1 protein triggers a lesion-mimic phenotype in Arabidopsis. Planta 221:85–94
Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9:1757–1766
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539
Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947
Neer EJ, Schmidt CJ, Nambudripad R, Smith TF (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371:297–300
Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21:5539–5547
Nissan TA, Galani K, Maco B, Tollervey D, Aebi U, Hurt E (2004) A pre-ribosome with a tadpole-like structure functions in ATP-dependent maturation of 60S subunits. Mol Cell 15:295–301
O’Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP (2002) 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 32:985–996
Parchaliuk DL, Kirkpatrick RD, Agatep R, Simon SL, Gietz RD (1999) Yeast two-hybrid system screening. Technical Tips. Online: http://www.tto.trends.com
Popescu SC, Tumer NE (2004) Silencing of ribosomal protein L3 genes in N. tabacum reveals coordinate expression and significant alterations in plant growth, development and ribosome biogenesis. Plant J 39:29–44
Royet J, Bouwmeester T, Cohen SM (1998) Notchless encodes a novel WD40-repeat-containing protein that modulates Notch signaling activity. EMBO J 17:7351–7360
Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ (2002) Functional proteomic analysis of human nucleolus. Mol Biol Cell 13:4100–4109
Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17:2340–2354
Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185
Tschochner H, Hurt E (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13:255–263
Tsukaya H (2002) Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol 217:1–39
Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292:2066–2069
van Nocker S, Ludwig P (2003) The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genom 4:50
Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 24:613–623
Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128:4289–4299
Whittaker CA, Hynes RO (2002) Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13:3369–3387
Wigge PA, Weigel D (2001) Arabidopsis genome: life without notch. Curr Biol 11:R112–R114
Williams EJ (1955) Seed failure in the Chippewa variety of Solanum tuberosum. Bot Gaz 10:10–15
Acknowledgments
We are very grateful to Alexandre Joyeux for providing the GFP vector and for assistance with the confocal microscope. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) and from the Canada Research Chair program. S.C. Chantha is the recipient of Ph.D. fellowships from NSERC and from Le Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT, QC, Canada). D.P. Matton holds a Canada Research Chair in Functional Genomics and Plant Signal Transduction.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chantha, SC., Matton, D.P. Underexpression of the plant NOTCHLESS gene, encoding a WD-repeat protein, causes pleitropic phenotype during plant development. Planta 225, 1107–1120 (2007). https://doi.org/10.1007/s00425-006-0420-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-006-0420-z