Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Cloning and expression analysis of TSK1, a wheat SKP1 homologue, and functional comparison with Arabidopsis ASK1 in male meiosis and auxin signalling

Chijun Li A C , Yu Liang A , Changbin Chen A B , Junhua Li A C , Yunyuan Xu A , Zhihong Xu A , Hong Ma B and Kang Chong A D
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, People’s Republic of China.

B Department of Biology and the Huck Institutes of the Life Sciences, 405D Life Sciences Building, The Pennsylvania State University, University Park, PA 16802, USA.

C Graduate School of the Chinese Academy of Sciences, Beijing 100049, People’s Republic of China.

D Corresponding author. Email: chongk@ibcas.ac.cn

Functional Plant Biology 33(4) 381-390 https://doi.org/10.1071/FP06026
Submitted: 26 January 2006  Accepted: 2 March 2006   Published: 3 April 2006

Abstract

Plants possess multiple homologues of the SKP1 gene encoding an essential subunit of the SCF ubiquitin ligases, but only ASK1 (Arabidopsis SKP1-like 1) and ASK2 have been characterised genetically. In addition, little is known about the function of SKP1 homologues in monocots. Here we report on a winter wheat homologue of SKP1 named TSK1 (Triticum aestivum SKP1-like 1). Expression analyses revealed that it was expressed predominantly in young roots and floral buds. RNA in situ hybridisation showed that it was expressed in the shoot apical meristem (SAM) and anthers, especially the tapetum and microsporocytes at the time of meiosis. It was also expressed in almost the entire meristematic and elongation zones of the root. These observations indicated that TSK1 might function in dividing cells. The Arabidopsis ask1-1 mutant with overexpressed TSK1 driven by the CaMV 35S promoter exhibited partial fertility, suggesting that TSK1 could partially restore function in meiosis to the ask1-1 mutant. In addition, overexpression of TSK1 in wild type Arabidopsis resulted in changes in auxin responses and auxin-related phenotypes, consistent with a role of ASK1 in Arabidopsis auxin response. These results suggest possible functional conservation between TSK1 and ASK1.

Keywords: Arabidopsis, auxin response, meiosis, SKP1, TSK1, wheat.


Acknowledgments

The BA3-GUS seeds were kindly provided by Professor Athanasios Theologis (University of California, Berkeley). This work was supported by the Outstanding Young Research Fund of NSFC (30525026) and innovation grants from the Chinese Academy of Sciences, as well as the Major State Basic Research Program of the People’s Republic of China (2005CB120806).


References


Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technology 44, 117–122.
PubMed |
open url image1

Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86, 263–274.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Callis J, Vierstra RD (2000) Protein degradation in signaling. Current Opinion in Plant Biology 3, 381–386.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ciechanover A (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO Journal 17, 7151–7160.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Connelly C, Hieter P (1996) Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86, 275–285.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dong C, Thomas S, Becker D, Lörz H, Whitford R, Sutton T, Able JA, Langridge P (2005) WM5: Isolation and characterisation of a gene expressed during early meiosis and shoot meristem development in wheat. Functional Plant Biology 32, 249–258.
Crossref | GoogleScholarGoogle Scholar | open url image1

Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Research 19, 1349.
PubMed |
open url image1

Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proceedings of the National Academy of Sciences USA 99, 11519–11524.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ge L, Chen H, Jiang JF, Zhao Y, Xu ML, Xu YY, Tan KH, Xu ZH, Chong K (2004) Overexpression of OsRAA1 causes pleiotropic phenotypes in transgenic rice plants, including altered leaf, flower, and root development and root response to gravity. Plant Physiology 135, 1502–1513.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes & Development 13, 1678–1691.
PubMed |
open url image1

Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX / IAA proteins. Nature 414, 271–276.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297, 793–797.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kong H, Leebens-Mack J, Ni W, dePamphilis CW, Ma H (2004) Highly heterogeneous rates of evolution in the SKP1 gene family in plants and animals: functional and evolutionary implications. Molecular Biology and Evolution 21, 117–128.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu F, Ni W, Griffith ME, Huang Z, Chang C, Peng W, Ma H, Xie D (2004) The ASK1 and ASK2 genes are essential for Arabidopsis early development. The Plant Cell 16, 5–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Marrocco K, Lecureuil A, Nicolas P, Guerche P (2003) The Arabidopsis SKP1-like genes present a spectrum of expression profiles. Plant Molecular Biology 52, 715–727.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–479. open url image1

Ni W, Xie D, Hobbie L, Feng B, Zhao D, Akkara J, Ma H (2004) Regulation of flower development in Arabidopsis by SCF complexes. Plant Physiology 134, 1574–1585.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oono Y, Chen QG, Overvoorde PJ, Kohler C, Theologis A (1998) age mutants of Arabidopsis exhibit altered auxin-regulated gene expression. The Plant Cell 10, 1649–1662.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Porat R, Lu P, O’Neill SD (1998) Arabidopsis SKP1, a homologue of a cell cycle regulator gene, is predominantly expressed in meristematic cells. Planta 204, 345–351.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Risseeuw EP, Daskalchuk TE, Banks TW, Liu E, Cotelesage J, Hellmann H, Estelle M, Somers DE, Crosby WL (2003) Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. The Plant Journal 34, 753–767.
Crossref | PubMed |
open url image1

Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes & Development 12, 198–207.
PubMed |
open url image1

Sambrook, J , Fritsch, EF ,  and  Maniatis, T (1989). ‘Molecular cloning: a laboratory manual.’ 2nd edn . (Cold Spring Harbor Laboratory Press: Cold Spring Harbor)

Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K , et al. (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ERE, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP , et al. (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2 complex. Nature 408, 381–386.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Takahashi N, Kuroda H, Kuromori T, Hirayama T, Seki M, Shinozaki K, Shimada H, Matsui M (2004) Expression and interaction analysis of Arabidopsis Skp1-related genes. Plant & Cell Physiology 45, 83–91.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

ten Hoopen R, Manteuffel R, Dolezel J, Malysheva L, Schubert I (2000) Evolutionary conservation of kinetochore protein sequences in plants. Chromosoma 109, 482–489.
PubMed |
open url image1

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
PubMed |
open url image1

Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M (2005) The tomato Aux / IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. The Plant Cell 17, 2676–2692.
Crossref | GoogleScholarGoogle Scholar | open url image1

Xiao W, Jang J (2000) F-box proteins in Arabidopsis. Trends in Plant Science 5, 454–457.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Development 14, 3024–3036.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xu YY, Chong K, Xu ZH, Tan KH (2001) Expression patterns of a vernalization-related gene responding to jasmonate. Acta Botanica Sinica 43, 871–873. open url image1

Yang M, Hu Y, Lodhi M, McCombie WR, Ma H (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proceedings of the National Academy of Sciences USA 96, 11416–11421.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhao D, Yang M, Solava J, Ma H (1999) The Arabidopsis ASK1 gene regulates vegetative and floral development and interacts with UFO to control floral organ identity. Developmental Genetics 25, 209–223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao D, Yu Q, Chen M, Ma H (2001) The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis. Development 128, 2735–2746.
PubMed |
open url image1

Zhao D, Han T, Risseeuw E, Crosby WL, Ma H (2003a) Conservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopsis thaliana. Plant Molecular Biology 53, 163–173.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao D, Ni W, Feng B, Han T, Petrasek MG, Ma H (2003b) Members of the Arabidopsis-SKP1-like gene family exhibit a variety of expression patterns and may play diverse roles in Arabidopsis. Plant Physiology 133, 203–217.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhuang X, Xu Y, Chong K, Lan L, Xue Y, Xu Z (2005) OsAGAP, an ARF-GAP from rice, regulates root development mediated by auxin in Arabidopsis. Plant, Cell & Environment 28, 147–156.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1