The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis

Plant Cell

Volumn 25, Issue 4, 2013, Pages 1274-1287

  Demesa Arévalo, Edgar ^a   Vielle Calzada, Jean Philippe ^a  

^a Departamento de Ingeniería Genética de Plantas   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84878214195     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.106237     Document Type: Article

References (81)

1. Acosta-García, G., and Vielle-Calzada, J.P. (2004). A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16: 2614-2628.
2. Agashe, B., Prasad, C.K., and Siddiqi, I. (2002). Identification and analysis of DYAD: A gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development 129: 3935-3943.
3. Bachelier, J.B., and Friedman, W.E. (2011). Female gamete competition in an ancient angiosperm lineage. Proc. Natl. Acad. Sci. USA 108: 12360-12365.
4. Bajon, C., Horlow, C., Motamayor, J.C., Sauvanet, A., and Robert, D. (1999). Megasporogenesis in Arabidopsis thaliana L.: An ultrastructural study. Sex. Plant Reprod. 12: 99-109.
5. Bechtold, N., Jaudeau, B., Jolivet, S., Maba, B., Vezon, D., Voisin, R., and Pelletier, G. (2000). The maternal chromosome set is the target of the T-DNA in the in planta transformation of Arabidopsis thaliana. Genetics 155: 1875-1887.
6. Bell, P.R. (1996). Megaspore abortion: A consequence of selective apoptosis? Int. J. Plant Sci. 157: 1-7.
7. Bencivenga, S., Colombo, L., and Masiero, S. (2011). Cross talk between the sporophyte and the megagametophyte during ovule development. Sex. Plant Reprod. 24: 113-121.
8. Borner, G.H.H., Lilley, K.S., Stevens, T.J., and Dupree, P. (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol. 132: 568-577.
9. Borner, G.H.H., Sherrier, D.J., Stevens, T.J., Arkin, I.T., and Dupree, P. (2002). Prediction of glycosylphosphatidylinositolanchored proteins in Arabidopsis. A genomic analysis. Plant Physiol. 129: 486-499.
10. Chen, C.G., Pu, Z.Y., Moritz, R.L., Simpson, R.J., Bacic, A., Clarke, A.E., and Mau, S.L. (1994). Molecular cloning of a gene encoding an arabinogalactan-protein from pear (Pyrus communis) cell suspension culture. Proc. Natl. Acad. Sci. USA 91: 10305-10309.
11. Chen, J., et al. (2008). A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc. Natl. Acad. Sci. USA 105: 11436-11441.
12. Cheng, C.Y., Mathews, D.E., Eric Schaller, G., and Kieber, J.J. (2013). Cytokinin-dependent specification of the functional megaspore in the Arabidopsis female gametophyte. Plant J. 73: 929-940.
13. 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.
14. Coimbra, S., Almeida, J., Junqueira, V., Costa, M.L., and Pereira, L.G. (2007). Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J. Exp. Bot. 58: 4027-4035.
15. Couteau, F., Belzile, F., Horlow, C., Grandjean, O., Vezon, D., and Doutriaux, M.P. (1999). Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11: 1623-1634.
16. 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.
17. Curtis, M.J., Belcram, K., Bollmann, S.R., Tominey, C.M., Hoffman, P.D., Mercier, R., and Hays, J.B. (2009). Reciprocal chromosome translocation associated with TDNA-insertion mutation in Arabidopsis: Genetic and cytological analyses of consequences for gametophyte development and for construction of doubly mutant lines. Planta 229: 731-745.
18. Delker, C., Pöschl, Y., Raschke, A., Ullrich, K., Ettingshausen, S., Hauptmann, V., Grosse, I., and Quint, M. (2010). Natural variation of transcriptional auxin response networks in Arabidopsis thaliana. Plant Cell 22: 2184-2200.
19. Desfeux, C., Clough, S.J., and Bent, A.F. (2000). Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol. 123: 895-904.
20. Du, H., Simpson, R.J., Moritz, R.L., Clarke, A.E., and Bacic, A. (1994). Isolation of the protein backbone of an arabinogalactanprotein from the styles of Nicotiana alata and characterization of a corresponding cDNA. Plant Cell 6: 1643-1653.
21. Ebert, I., and Greilhuber, J. (2005). Developmental switch during embryo sac formation from a bisporic mode to the tetrasporic Fritillaria type in Hyacinthoides vincentina (Hoffmannsegg & Link) Rothm. (Hyacinthaceae). Acta Biol. Cracov. Bot. 47: 179-184.
22. Eisenhaber, B., Bork, P., and Eisenhaber, F. (1999). Prediction of potential GPI-modification sites in proprotein sequences. J. Mol. Biol. 292: 741-758.
23. Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q., Gerentes, D., Perez, P., and Smyth, D.R. (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8: 155-168.
24. Ellis, M., Egelund, J., Schultz, C.J., and Bacic, A. (2010). Arabinogalactanproteins: Key regulators at the cell surface? Plant Physiol. 153: 403-419.
25. Estévez, J.M., Kieliszewski, M.J., Khitrov, N., and Somerville, C. (2006). Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis. Plant Physiol. 142: 458-470.
26. Friedman, W.E., and Ryerson, K.C. (2009). Reconstructing the ancestral female gametophyte of angiosperms: Insights from Amborella and other ancient lineages of flowering plants. Am. J. Bot. 96: 129-143.
27. Hepworth, S.R., Valverde, F., Ravenscroft, D., Mouradov, A., and Coupland, G. (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21: 4327-4337.
28. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W., and Zimmermann, P. (2008). Genevestigator v3: A reference expression database for the metaanalysis of transcriptomes. Adv. Bioinforma. 2008: 420747.
29. Huang, B.-Q., Russell, S.D. (1992). Female germ unit: Organization, isolation and function. Int. Rev. Cytol. 140: 233-293.
30. 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.
31. Kapil, R.N., and Bhatnagar, A.K. (1981). Ultrastructure and biology of female gametophyte in flowering plants. Int. Rev. Cytol. 70: 291-341.
32. Klimyuk, V.I., and Jones, J.D. (1997). AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: Characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J. 11: 1-14.
33. Klucher, K.M., Chow, H., Reiser, L., and Fischer, R.L. (1996). The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8: 137-153.
34. Law, J.A., and Jacobsen, S.E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11: 204-220.
35. Le Gourrierec, J., Li, Y.-F., and Zhou, D.-X. (1999). Transcriptional activation by Arabidopsis GT-1 may be through interaction with TFIIA-TBP-TATA complex. Plant J. 18: 663-668.
36. Maheshwari, P. (1950). An Introduction to the Embryology of Angiosperms. (New York: McGraw-Hill).
37. McBride, K.E., and Summerfelt, K.R. (1990). Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 14: 269-276.
38. Misra, R.C. (1962). Contribution to the embryology of Arabidopsis thalianum (Gay and Monn.). Agra Univ. J. Res. 11: 191-199.
39. Noher de Halac, I., and Harte, C. (1977). Different patterns of callose wall formation during megasporogenesis in 2 species of Oenothera (Onagraceae). Plant Syst. Evol. 127: 23-38.
40. O'Connor, T.R., Dyreson, C., and Wyrick, J.J. (2005). Athena: A resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21: 4411-4413.
41. Olmedo-Monfil, V., Durán-Figueroa, N., Arteaga-Vázquez, M., DemesaArévalo, E., Autran, D., Grimanelli, D., Slotkin, R.K., Martienssen, R.A., and Vielle-Calzada, J.-P. (2010). Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632.
42. 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.
43. Pandey, S., Wang, R.S., Wilson, L., Li, S., Zhao, Z., Gookin, T.E., Assmann, S.M., and Albert, R. (2010). Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Mol. Syst. Biol. 6: 372.
44. Pennell, R.I., Janniche, L., Kjellbom, P., Scofield, G.N., Peart, J.M., and Roberts, K. (1991). Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3: 1317-1326.
45. Pennell, R.I., Janniche, L., Scofield, G.N., Booij, H., de Vries, S.C., and Roberts, K. (1992). Identification of a transitional cell state in the developmental pathway to carrot somatic embryogenesis. J. Cell Biol. 119: 1371-1380.
46. Pennell, R.I., and Roberts, K. (1990). Sexual development in the pea is presaged by altered expression of arabinogalactan protein. Nature 344: 547-549.
47. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
48. Qiu, Y.L., Liu, R.S., Xie, C.T., Russell, S.D., and Tian, H.Q. (2008). Calcium changes during megasporogenesis and megaspore degeneration in lettuce (Lactuca sativa L.). Sex. Plant Reprod. 21: 197-204.
49. Raj, A., Rifkin, S.A., Andersen, E., and van Oudenaarden, A. (2010). Variability in gene expression underlies incomplete penetrance. Nature 463: 913-918.
50. Ray, S.M., Park, S.S., and Ray, A. (1997). Pollen tube guidance by the female gametophyte. Development 124: 2489-2498.
51. Reiser, L., and Fischer, R.L. (1993). The ovule and the embryo sac. Plant Cell 5: 1291-1301.
52. Robinson-Beers, K., Pruitt, R.E., and Gasser, C.S. (1992). Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4: 1237-1249.
53. Rodkiewicz, B. (1970). Callose in cell walls during megasporogenesis in angiosperms. Planta 93: 39-47.
54. Russell, S.D. (1979). Fine structure of megagametophyte development in Zea mays. Can. J. Bot. 57: 1093-1110.
55. Sánchez-León, N., et al. (2012). Transcriptional analysis of the Arabidopsis ovule by massively parallel signature sequencing. J. Exp. Bot. 63: 3829-3842.
56. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and Schneitz, K. (1999). Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 11664-11669.
57. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P., McCann, M.C., and Benfey, P.N. (2001). COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 15: 1115-1127.
58. Schmidt, A., Wuest, S.E., Vijverberg, K., Baroux, C., Kleen, D., and Grossniklaus, U. (2011). Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9: e1001155.
59. Schultz, C., Gilson, P., Oxley, D., Youl, J., and Bacic, A. (1998). GPIanchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci. 3: 426-431.
60. Seifert, G.J., and Roberts, K. (2007). The biology of arabinogalactan proteins. Annu. Rev. Plant Biol. 58: 137-161.
61. Sherrier, D.J., Prime, T.A., and Dupree, P. (1999). Glycosylphosphatidylinositolanchored cell-surface proteins from Arabidopsis. Electrophoresis 20: 2027-2035.
62. Skriver, K., Olsen, F.L., Rogers, J.C., and Mundy, J. (1991). Cisacting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc. Natl. Acad. Sci. USA 88: 7266-7270.
63. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., Dolezal, K., Schlereth, A., Jürgens, G., and Alonso, J.M. (2008). TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177-191.
64. Sun, W., Zhao, Z.D., Hare, M.C., Kieliszewski, M.J., and Showalter, A.M. (2004). Tomato LeAGP-1 is a plasma membrane-bound, glycosylphosphatidylinositol-anchored arabinogalactan-protein. Physiol. Plant. 120: 319-327.
65. Tan, L., Showalter, A.M., Egelund, J., Hernandez-Sanchez, A., Doblin, M.S., and Bacic, A. (2012). Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans. Front. Plant Sci. 3: 140.
66. Tucker, M.R., and Koltunow, A.M. (2009). Sexual and asexual (apomictic) seed development in flowering plants: Molecular, morphological and evolutionary relationships. Funct. Plant Biol. 36: 490-504.
67. Tucker, M.R., Okada, T., Hu, Y., Scholefield, A., Taylor, J.M., and Koltunow, A.M. (2012). Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139: 1399-1404.
68. Ulmasov, T., Liu, Z.B., Hagen, G., and Guilfoyle, T.J. (1995). Composite structure of auxin response elements. Plant Cell 7: 1611-1623.
69. Velasquez, S.M., et al. (2011). O-glycosylated cell wall proteins are essential in root hair growth. Science 332: 1401-1403.
70. Webb, M.C., and Gunning, B.E.S. (1990). Embryo sac development in Arabidopsis thaliana. I. Megasporogenesis, including the microtubular cytoskeleton. Sex. Plant Reprod. 3: 244-256.
71. Wuest, S.E., Vijverberg, K., Schmidt, A., Weiss, M., Gheyselinck, J., Lohr, M., Wellmer, F., Rahnenführer, 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.
72. Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cisacting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251-264.
73. Yang, J., and Showalter, A.M. (2007). Expression and localization of AtAGP18, a lysine-rich arabinogalactan-protein in Arabidopsis. Planta 226: 169-179.
74. Yang, W.-C., Shi, D.-Q., and Chen, Y.-H. (2010). Female gametophyte development in flowering plants. Annu. Rev. Plant Biol. 61: 89-108.
75. Yang, W.-C., and Sundaresan, V. (2000). Genetics of gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. 3: 53-57.
76. Yang, W.-C., Ye, D., Xu, J., and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13: 2108-2117.
77. Yates, E.A., Valdor, J.-F., Haslam, S.M., Morris, H.R., Dell, A., Mackie, W., and Knox, J.P. (1996). Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6: 131-139.
78. Youl, J.J., Bacic, A., and Oxley, D. (1998). Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors. Proc. Natl. Acad. Sci. USA 95: 7921-7926.
79. Yu, J.H., Hamari, Z., Han, K.H., Seo, J.A., Reyes-Domínguez, Y., and Scazzocchio, C. (2004). Double-joint PCR: A PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41: 973-981.
80. Zhang, Y., Yang, J., and Showalter, A.M. (2011a). AtAGP18 is localized at the plasma membrane and functions in plant growth and development. Planta 233: 675-683.
81. Zhang, Y., Yang, J., and Showalter, A.M. (2011b). AtAGP18, a lysine-rich arabinogalactan protein in Arabidopsis thaliana, functions in plant growth and development as a putative co-receptor for signal transduction. Plant Signal. Behav. 6: 855-857.