Four Closely-related RING-type E3 Ligases, APD1-4, are Involved in Pollen Mitosis II Regulation in Arabidopsis

Journal of Integrative Plant Biology

Volumn 54, Issue 10, 2012, Pages 814-827

  Luo, Guo ^a   Gu, Hongya ^a,b   Liu, Jingjing ^a   Qu, Li Jia ^a,b  

^a Tsinghua University   (China)

^b National Plant Gene Research Center   (China)

Author keywords

Arabidopsis; E3 ligase; Male gametogenesis; Pollen mitosis II; RING finger

Indexed keywords

ARABIDOPSIS PROTEIN; UBIQUITIN PROTEIN LIGASE;

ENZYME ACTIVITY; EUKARYOTE; GAMETOGENESIS; GAMETOPHYTE; MUTATION; PATHOGEN; PHENOTYPE; POLLEN; PROTEIN; RNA; SIGNALING;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MITOSIS; MOLECULAR GENETICS; PHYSIOLOGY; POLLEN; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; MITOSIS; MOLECULAR SEQUENCE DATA; POLLEN; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN-PROTEIN LIGASES;

EID: 84867385667     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01152.x     Document Type: Article

References (56)

1. Alche JD, M'Rani-Alaoui M, Castro AJ, Rodriguez-Garcia MI (2004) Ole e 1, the major allergen from olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination. Plant Cell Physiol 45, 1149-1157.
2. Berthold J, Schenkova K, Ramos S, Miura Y, Furukawa M, Aspenstrom P, Rivero F (2008) Characterization of RhoBTB-dependent Cul3 ubiquitin ligase complexes - Evidence for an autoregulatory mechanism. Exp. Cell Res 314, 3453-3465.
3. Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23, 534-549.
4. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009a) A plant germline-specific integrator of sperm specification and cell cycle progression. PloS Genet. 5, e1000430.
5. Brownfield L, Hafidh S, Durbarry A, Khatab H, Sidorova A, Doerner P, Twell D (2009b) Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell 21, 1940-1956.
6. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16, 735-743.
7. Deshaies RJ, Joazeiro CAP (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
8. Devoto A, Muskett PR, Shirasu K (2003) Role of ubiquitination in the regulation of plant defence against pathogens. Curr. Opin. Plant Biol. 6, 307-311.
9. Dissmeyer N, Nowack MK, Pusch S, Stals H, Inze D, Grini PE, Schnittger A (2007) T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 19, 972-985.
10. Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol. 137, 297-307.
11. Feldman RMR, Correll CC, Kaplan KB, Deshaies RJ (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91, 221-230.
12. Gusti A, Baumberger N, Nowack M, Pusch S, Eisler H, Potuschak T, De Veylder L, Schnittger A, Genschik P (2009) The Arabidopsis thaliana F-box protein FBL17 is essential for progression through the second mitosis during pollen development. PloS One 4, e4780.
13. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132, 640-652.
14. Hou X, Li L, Peng Z, Wei B, Tang S, Ding M, Liu J, Zhang F, Zhao Y, Gu H, Qu LJ (2010) A platform of high-density INDEL/CAPS markers for map-based cloning in Arabidopsis. Plant J. 63, 880-888.
15. Hou X, Liu S, Pierri F, Dai X, Qu LJ, Zhao Y (2011) Allelic analyses of the Arabidopsis YUC1locus reveal residues and domains essential for the functions of YUC family of flavin monooxygenases. J. Integr. Plant Biol. 53, 54-62.
16. Huecas S, Villalba M, Rodriguez R (2001) Ole e 9, a major olive pollen allergen is a 1, 3-beta-glucanase - Isolation, characterization, amino acid sequence, and tissue specificity. J. Biol. Chem. 276, 27959-27966.
17. Imajuku Y, Ohashi Y, Aoyama T, Goto K, Oka A (2001) An upstream region of the Arabidopsis thaliana CDKA;1 (CDC2aAt) gene directs transcription during trichome development. Plant Mol. Biol. 46, 205-213.
18. Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J. 45, 819-831.
19. Jura N, Scotto-Lavino E, Sobczyk A, Bar-Sagi D (2006) Differential modification of Ras proteins by ubiquitination. Mol. Cell 21, 679-687.
20. Kawabe H, Neeb A, Dimova K, Young SM, Jr., Takeda M, Katsurabayashi S, Mitkovski M, Malakhova OA, Zhang DE, Ulmilkawa M, Kariya Ki, Goebbels S, Nave KA, Rosenmund C, Jahn O, Rhee J, Brose N (2010) Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65, 358-372.
21. Kieffer M, Master V, Waites R, Davies B (2011) TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 68, 147-158.
22. FBL17 degradation of cell cycle inhibitors. Nature 455, 1134-1137.
23. Kim SE, Yoon JY, Jeong WJ, Jeon SH, Park Y, Yoon JB, Park YN, Kim H, Choi KY (2009) H-Ras is degraded by Wnt/beta-catenin signaling via beta-TrCP-mediated polyubiquitylation. J. Cell Sci 122, 842-848.
24. Lei ZY, Zhao P, Cao MJ, Cui R, Chen X, Xiong LZ, Zhang QF, Oliver DJ, Xiang CB (2007) High-throughput binary vectors for plant gene function analysis. J. Integr. Plant Biol 49, 556-567.
25. Liu J, Qu LJ (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol. Plant 1, 564-574.
26. Liu J, Zhang Y, Qin G, Tsuge T, Sakaguchi N, Luo G, Sun K, Shi D, Aki S, Zheng N, Aoyama T, Oka A, Yang W, Umeda M, Xie Q, Gu H, Qu LJ (2008) Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell 20, 1538-1554.
27. Luo Y, Qin G, Zhang J, Liang Y, Song Y, Zhao M, Tsuge T, Aoyama T, Liu J, Gu H, Qu LJ (2011) D-myo-inositol-3-phosphate affects phosphatidylinositol-mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 23, 1352-1372.
28. McCormick S (2004) Control of male gametophyte development. Plant Cell 16, S142-S153.
29. 2+channels in pollen tubes and are regulated by pistil D-serine. Science 332, 434-437.
30. Moren A, Imamura T, Miyazono K, Heldin CH, Moustakas A (2005) Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J. Biol. Chem 280, 22115-22123.
31. + channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc. Natl. Acad. Sci.USA 101, 12242-12247.
32. Osterlund MT, Wei N, Deng XW (2000) The roles of photoreceptor systems and the COP1-targeted destabilization of HY5 in light control of Arabidopsis seedling development. Plant Physiol. 124, 1520-1524.
33. Ou B, Yin K, Liu S, Yang Y, Gu T, Hui JMW, Zhang L, Miao J, Kondou Y, Matsui M, Gu H, Qu LJ (2011) A high-through screening system for Arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol. Plant 4, 546-555.
34. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533.
35. Qin GJ, Gu HY, Zhao YD, Ma ZQ, Shi GL, Yang Y, Pichersky E, Chen HD, Liu MH, Chen ZL, Qu LJ (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17, 2693-2704.
36. 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.
37. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol 15, 244-248.
38. Rueda-Romero P, Barrero-Sicilia C, Gomez-Cadenas A, Carbonero P, Onate-Sanchez L (2012) Arabidopsis thaliana DOF6 negatively affects germination in non-after-ripened seeds and interacts with TCP14. J. Exp. Bot. 63, 1937-1949.
39. Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322.
40. Schwamborn JC, Mueller M, Becker AHM, Pueschel AW (2007) Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J. 26, 1410-1422.
41. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590.
42. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137, 13-30.
43. Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2008) Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J. 53, 42-52.
44. Twell D, Yamaguchi J, McCormick S (1990) Pollen-specific gene-expression in transgenic plants - coordinate regulation of 2 different tomato gene promoters during microsporogenesis. Development 109, 705-713.
45. van Hengel AJ, Roberts K (2003) AtAGP30, an arabinogalactan-protein in the cell walls of the primary root, plays a role in root regeneration and seed germination. Plant J. 36, 256-270.
46. Verkest A, Manes CLD, Vercruysse S, Maes S, Van der Schueren E, Beeckman T, Genschik P, Kuiper M, Inze D, De Veylder L (2005) The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17, 1723-1736.
47. Vernoud V, Horton AC, Yang ZB, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131, 1191-1208.
48. Wang WY, Zhang L, Xing SF, Ma ZQ, Liu JJ, Gu H, Qin GJ, Qu LJ (2012) Arabidopsis AtVPS15 plays essential roles in pollen germination possibly by interacting with AtVPS34. J. Genet. Genom. 39, 81-92.
49. Wang Y, Hou Y, Gu H, Kang D, Chen Z, Liu J, Qu LJ (2012) The Arabidopsis APC4 subunit of the anaphase-promoting complex/cyclosome (APC/C) is critical for both female gametogenesis and embryogenesis. Plant J. 69, 227-240.
50. Weissman AM (2001) Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2, 169-178.
51. Wilkins A, Ping QG, Carpenter CL (2004) RhoBTB2 is a substrate of the mammalian Cul3 ubiquitin ligase complex. Genes Dev. 18, 856-861.
52. Xie Q, Guo HS, Dallman G, Fang SY, Weissman AM, Chua NH (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167-170.
53. Yamamoto YY, Deng XW, Matsui M (2001) CIP4, a new COP1 target, is a nucleus-localized positive regulator of Arabidopsis photomorphogenesis. Plant Cell 13, 399-411.
54. Yamamoto YY, Matsui M, Ang LH, Deng XW (1998) Role of a COP1 interactive protein in mediating light-regulated gene expression in Arabidopsis. Plant Cell 10, 1083-1094.
55. Zhang Y, Wu R, Qin G, Chen Z, Gu H, Qu LJ (2011) Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. J. Integr. Plant Biol 53, 493-506.
56. Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19, 1912-1929.