Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo and heterodimers when expressed in yeast

Plant Physiology

Volumn 163, Issue 2, 2013, Pages 696-712

  Boavida, Leonor C ^a,b   Qin, Peng ^b   Broz, Miranda ^b   Becker, Jörg D ^a   Mccormick, Sheila ^a,b  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; METAZOA; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; TETRASPANIN;

AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; ARABIDOPSIS; ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; GENE EXPRESSION REGULATION, PLANT; GERM CELLS, PLANT; GREEN FLUORESCENT PROTEINS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PHYLOGENY; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; REPRODUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SUBCELLULAR FRACTIONS; TETRASPANINS;

EID: 84885203239     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.216598     Document Type: Article

References (73)

1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11: 36-42
2. Baldwin G, Novitskaya V, Sadej R, Pochec E, Litynska A, Hartmann C, Williams J, Ashman L, Eble JA, Berditchevski F (2008) Tetraspanin CD151 regulates glycosylation of a3b1 integrin. J Biol Chem 283: 35445-35454
3. Barreiro O, Zamai M, Yáñez-Mó M, Tejera E, López-Romero P, Monk PN, Gratton E, Caiolfa VR, Sánchez-Madrid F (2008) Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 183: 527-542
4. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323: 1485-1488
5. Boavida LC, Borges F, Becker JD, Feijó JA (2011) Whole genome analysis of gene expression reveals coordinated activation of signaling and metabolic pathways during pollen-pistil interactions in Arabidopsis. Plant Physiol 155: 2066-2080
6. Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52: 570-582
7. Boavida LC, Vieira AM, Becker JD, Feijó JA (2005) Gametophyte interaction and sexual reproduction: how plants make a zygote. Int J Dev Biol 49: 615-632
8. Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijó JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148: 1168-1181
9. Charrin S, Manié S, Oualid M, Billard M, Boucheix C, Rubinstein E (2002) Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett 516: 139-144
10. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6: 325-330
11. Clough SJ (2005) Floral dip: agrobacterium-mediated germ line transformation. Methods Mol Biol 286: 91-102
12. Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, et al (2006) The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18: 852-866
13. Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development 127: 3385-3394
14. Copenhaver GP, Keith KC, Preuss D (2000) Tetrad analysis in higher plants. A budding technology. Plant Physiol 124: 7-16
15. Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15: 2514-2531
16. DeSalle R, Mares R, Garcia-España A (2010) Evolution of cysteine patterns in the large extracellular loop of tetraspanins from animals, fungi, plants and single-celled eukaryotes. Mol Phylogenet Evol 56: 486-491
17. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656-660
18. Evans JP (2012) Sperm-egg interaction. Annu Rev Physiol 74: 477-502
19. Faure JE, Rotman N, Fortuné P, Dumas C (2002) Fertilization in Arabidopsis thaliana wild type: developmental stages and time course. Plant J 30: 481-488
20. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS ONE 6: e18880
21. Ferrè F, Clote P (2006) DiANNA 1.1: an extension of the DiANNA web server for ternary cysteine classification. Nucleic Acids Res 34: W182-W185
22. Garcia-España A, DeSalle R (2009) Intron sliding in tetraspanins. Commun Integr Biol 2: 394-395
23. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/ single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96
24. Grefen C, Obrdlik P, Harter K (2009) The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS). Methods Mol Biol 479: 217-233
25. Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, Nakagawa T, Kanaoka MM, Sasaki N, Nakano A, Berger F, et al (2011) Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr Biol 21: 497-502
26. Hemler ME (2005) Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6: 801-811
27. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5: R85
28. Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, et al (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86: 674-684
29. Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130: 2149-2159
30. Hulskamp M, Schneitz K, Pruitt RE (1995) Genetic evidence for a longrange activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7: 57-64
31. Jégou A, Ziyyat A, Barraud-Lange V, Perez E, Wolf JP, Pincet F, Gourier C (2011) CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc Natl Acad Sci USA 108: 10946-10951
32. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacteriummediated plant transformation. Trends Plant Sci 7: 193-195
33. Kovalenko OV, Metcalf DG, DeGrado WF, Hemler ME (2005) Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct Biol 5: 11
34. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C (2000) Severely reduced female fertility in CD9-deficient mice. Science 287: 319-321
35. Levy S, Shoham T (2005a) The tetraspanin web modulates immunesignalling complexes. Nat Rev Immunol 5: 136-148
36. Levy S, Shoham T (2005b) Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 20: 218-224
37. Lieber D, Lora J, Schrempp S, Lenhard M, Laux T (2011) Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr Biol 21: 1009-1017
38. Liljegren SJ, Roeder AH, Kempin SA, Gremski K,Østergaard L, Guimil S, Reyes DK, Yanofsky MF (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116: 843-853
39. Mazurov D, Heidecker G, Derse D (2006) HTLV-1 Gag protein associates with CD82 tetraspanin microdomains at the plasma membrane. Virology 346: 194-204
40. McCue AD, Cresti M, Feijó JA, Slotkin RK (2011) Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited. J Exp Bot 62: 1621-1631
41. 2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332: 434-437
42. Mursalimov SR, Deineko EV (2011) An ultrastructural study of cytomixis in tobacco pollen mother cells. Protoplasma 248: 717-724
43. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51: 1126-1136
44. + channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc Natl Acad Sci USA 101: 12242-12247
45. Olmos E, Reiss B, Dekker K (2003) The ekeko mutant demonstrates a role for tetraspanin-like protein in plant development. Biochem Biophys Res Commun 310: 1054-1061
46. Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114: 47-59
47. Palanivelu R, Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6: 7
48. Pina C, Pinto F, Feijó JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138: 744-756
49. Pols MS, Klumperman J (2009) Trafficking and function of the tetraspanin CD63. Exp Cell Res 315: 1584-1592
50. Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131: 2707-2714
51. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5: e1000621
52. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 21: 639-644
53. Rokas A (2008) The molecular origins of multicellular transitions. Curr Opin Genet Dev 18: 472-478
54. Ron M, Alandete Saez M, Eshed Williams L, Fletcher JC, McCormick S (2010) Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24: 1010-1021
55. Rubinstein E (2011) The complexity of tetraspanins. Biochem Soc Trans 39: 501-505
56. Seigneuret M, Delaguillaumie A, Lagaudrière-Gesbert C, Conjeaud H (2001) Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion. J Biol Chem 276: 40055-40064
57. Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127: 4511-4518
58. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461-472
59. Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T (2012) Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338: 1093-1097
60. Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28: 106-112
61. Takada S, Jürgens G (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134: 1141-1150
62. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739
63. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62: 405-496
64. van Bel AJ (1996) Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with associated physiological software packages in dicotyledons? J Exp Bot 47: 1129-1140
65. Veneault-Fourrey C, Lambou K, Lebrun MH (2006) Fungal Pls1 tetraspanins as key factors of penetration into host plants: a role in reestablishing polarized growth in the appressorium? FEMS Microbiol Lett 256: 179-184
66. Wang F, Vandepoele K, Van Lijsebettens M (2012) Tetraspanin genes in plants. Plant Sci 190: 9-15
67. Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148: 1201-1211
68. Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenführer J, von Mering C, Grossniklaus U (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20: 506-512
69. Yáñez-Mó M, Tejedor R, Rousselle P, Sánchez -Madrid F (2001) Tetraspanins in intercellular adhesion of polarized epithelial cells: spatial and functional relationship to integrins and cadherins. J Cell Sci 114: 577-587
70. Yang X, Claas C, Kraeft SK, Chen LB, Wang Z, Kreidberg JA, Hemler ME (2002) Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell 13: 767-781
71. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
72. Yunta M, Lazo PA (2003) Tetraspanin proteins as organisers of membrane microdomains and signalling complexes. Cell Signal 15: 559-564
73. Zheng B, Chen X, McCormick S (2011) The anaphase-promoting complex is a dual integrator that regulates both microRNA-mediated transcriptional regulation of cyclin B1 and degradation of cyclin B1 during Arabidopsis male gametophyte development. Plant Cell 23: 1033-1046