SUMO E3 ligase AtMMS21 is required for normal meiosis and gametophyte development in Arabidopsis

详细信息    查看全文

• 作者：Ming Liu (1) (2)
  Songfeng Shi (1)
  Shengchun Zhang (1)
  Panglian Xu (1)
  Jianbin Lai (1)
  Yiyang Liu (1)
  Dongke Yuan (1)
  Yaqin Wang (1)
  Jinju Du (1)
  Chengwei Yang (1)
  
  1. Guangdong Key Lab of Biotechnology for Plant Development ; College of Life Science ; South China Normal University ; Guangzhou ; 510631 ; China
  2. Vegetable Research Institute Guangdong Academy of Agriculture Sciences ; Guangzhou ; Guangdong ; 510640 ; China
  
• 关键词：AtMMS21 ; SUMOylation ; Gametophyte development ; Meiosis ; Arabidopsis thaliana
• 刊名：BMC Plant Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：1,206 KB
• 参考文献：1. Ma, H, Sundaresan, V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91: pp. 379-412 CrossRef
  2. Yang, WC, Shi, DQ, Chen, YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61: pp. 89-108 CrossRef
  3. Borg, M, Brownfield, L, Twell, D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60: pp. 1465-1478 CrossRef
  4. Alvarez-Buylla, ER, Benitez, M, Corvera-Poire, A, Chaos Cador, A, de Folter, S, de Buen, AG, Garay-Arroyo, A, Garcia-Ponce, B, Jaimes-Miranda, F, Perez-Ruiz, RV, Pineyro-Nelson, A, Sanchez-Corrales, YE (2010) Flower development. Arabidopsis Book 8: pp. e0127 CrossRef
  5. Gallois, JL, Guyon-Debast, A, Lecureuil, A, Vezon, D, Carpentier, V, Bonhomme, S, Guerche, P (2009) The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 21: pp. 442-459 CrossRef
  6. Harrison, CJ, Alvey, E, Henderson, IR (2010) Meiosis in flowering plants and other green organisms. J Exp Bot 61: pp. 2863-2875 CrossRef
  7. Jones, GH, Armstrong, SJ, Caryl, AP, Franklin, FC (2003) Meiotic chromosome synapsis and recombination in Arabidopsis thaliana; an integration of cytological and molecular approaches. Chromosome Res 11: pp. 205-215 CrossRef
  8. Murnane, JP (2006) Telomeres and chromosome instability. DNA Repair (Amst) 5: pp. 1082-1092 CrossRef
  9. Liu, Z, Makaroff, CA (2006) Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 18: pp. 1213-1225 CrossRef
  10. Schubert, V (2009) SMC proteins and their multiple functions in higher plants. Cytogenet Genome Res 124: pp. 202-214 CrossRef
  11. Yuan, L, Yang, X, Ellis, JL, Fisher, NM, Makaroff, CA (2012) The Arabidopsis SYN3 cohesin protein is important for early meiotic events. Plant J 71: pp. 147-160 CrossRef
  12. Jiang, L, Xia, M, Strittmatter, LI, Makaroff, CA (2007) The Arabidopsis cohesin protein SYN3 localizes to the nucleolus and is essential for gametogenesis. Plant J 50: pp. 1020-1034 CrossRef
  13. Cai, X, Dong, F, Edelmann, RE, Makaroff, CA (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116: pp. 2999-3007 CrossRef
  14. Lam, WS, Yang, X, Makaroff, CA (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci 118: pp. 3037-3048 CrossRef
  15. Chelysheva, L, Diallo, S, Vezon, D, Gendrot, G, Vrielynck, N, Belcram, K, Rocques, N, Marquez-Lema, A, Bhatt, AM, Horlow, C, Mercier, R, Mezard, C, Grelon, M (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: pp. 4621-4632 CrossRef
  16. Siddiqui, NU, Rusyniak, S, Hasenkampf, CA, Riggs, CD (2006) Disruption of the Arabidopsis SMC4 gene, AtCAP-C, compromises gametogenesis and embryogenesis. Planta 223: pp. 990-997 CrossRef
  17. Siddiqui, NU, Stronghill, PE, Dengler, RE, Hasenkampf, CA, Riggs, CD (2003) Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis. Development 130: pp. 3283-3295 CrossRef
  18. Liu Cm, CM, McElver, J, Tzafrir, I, Joosen, R, Wittich, P, Patton, D, Van Lammeren, AA, Meinke, D (2002) Condensin and cohesin knockouts in Arabidopsis exhibit a titan seed phenotype. Plant J 29: pp. 405-415 CrossRef
  19. Watanabe, K, Pacher, M, Dukowic, S, Schubert, V, Puchta, H, Schubert, I (2009) The structural maintenance of chromosomes 5/6 complex promotes sister chromatid alignment and homologous recombination after DNA damage in Arabidopsis thaliana. Plant Cell 21: pp. 2688-2699 CrossRef
  20. Tzafrir, I, Pena-Muralla, R, Dickerman, A, Berg, M, Rogers, R, Hutchens, S, Sweeney, TC, McElver, J, Aux, G, Patton, D, Patton, D, Meinke, D (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135: pp. 1206-1220 CrossRef
  21. Huang, L, Yang, S, Zhang, S, Liu, M, Lai, J, Qi, Y, Shi, S, Wang, J, Wang, Y, Xie, Q, Yang, C (2009) The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J 60: pp. 666-678 CrossRef
  22. Ishida, T, Fujiwara, S, Miura, K, Stacey, N, Yoshimura, M, Schneider, K, Adachi, S, Minamisawa, K, Umeda, M, Sugimoto, K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21: pp. 2284-2297 CrossRef
  23. Zhang, S, Qi, Y, Yang, C (2010) Arabidopsis SUMO E3 ligase AtMMS21 regulates root meristem development. Plant Signal Behav 5: pp. 53-55 CrossRef
  24. Xu, P, Yuan, D, Liu, M, Li, C, Liu, Y, Zhang, S, Yao, N, Yang, C (2013) AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in arabidopsis roots. Plant Physiol 161: pp. 1755-1768 CrossRef
  25. Berr, A, McCallum, EJ, M茅nard, R, Meyer, D, Fuchs, J, Dong, A, Shen, W-H (2010) Arabidopsis set domain group2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development. Plant Cell 22: pp. 3232 CrossRef
  26. Alexander, MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: pp. 117-122
  27. 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: pp. 297-322 CrossRef
  28. Armstrong, SJ, Caryl, AP, Jones, GH, Franklin, FCH (2002) Asy1, a protein required for melotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: pp. 3645-3655 CrossRef
  29. Higgins, JD, Sanchez-Moran, E, Armstrong, SJ, Jones, GH, Franklin, FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: pp. 2488-2500 CrossRef
  30. Klimyuk, VI, Jones, JDG (1997) AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J 11: pp. 1-14 CrossRef
  31. Wang, Y (2004) Progression through Meiosis I and Meiosis II in arabidopsis anthers is regulated by an a-type cyclin predominately expressed in prophase I. Plant Physiol 136: pp. 4127-4135 CrossRef
  32. Higgins, JD, Armstrong, SJ, Franklin, FCH, Jones, GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18: pp. 2557-2570 CrossRef
  33. Ronceret, A, Doutriaux, M-P, Golubovskaya, IN, Pawlowski, WP (2009) PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proc Natl Acad Sci U S A 106: pp. 20121-20126 CrossRef
  34. Doutriaux, MP, Couteau, F, Bergounioux, C, White, C (1998) Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol Gen Genet 257: pp. 283-291 CrossRef
  35. Abe, K (2005) Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiol 139: pp. 896-908 CrossRef
  36. Chen, Z, Higgins, JD, Hui, JTL, Li, J, Franklin, FCH, Berger, F (2011) Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J 30: pp. 744-755 CrossRef
  37. Grelon, M, Vezon, D, Gendrot, G, Pelletier, G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20: pp. 589-600 CrossRef
  38. Stacey, NJ, Kuromori, T, Azumi, Y, Roberts, G, Breuer, C, Wada, T, Maxwell, A, Roberts, K, Sugimoto-Shirasu, K (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48: pp. 206-216 CrossRef
  39. Saracco, SA, Miller, MJ, Kurepa, J, Vierstra, RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145: pp. 119-134 CrossRef
  40. Park, HJ, Kim, WY, Park, HC, Lee, SY, Bohnert, HJ, Yun, DJ (2011) SUMO and SUMOylation in plants. Mol Cells 32: pp. 305-316 CrossRef
  41. Ishida, T, Yoshimura, M, Miura, K, Sugimoto, K (2012) MMS21/HPY2 and SIZ1, two Arabidopsis SUMO E3 ligases, have distinct functions in development. PLoS ONE 7: pp. e46897 CrossRef
  42. Ling, Y, Zhang, C, Chen, T, Hao, H, Liu, P, Bressan, RA, Hasegawa, PM, Jin, JB, Lin, J (2012) Mutation in SUMO E3 ligase, SIZ1, disrupts the mature female gametophyte in Arabidopsis. PLoS ONE 7: pp. e29470 CrossRef
  43. Bergerat, A, de Massy, B, Gadelle, D, Varoutas, PC, Nicolas, A, Forterre, P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386: pp. 414-417 CrossRef
  44. Bickel, JS, Chen, L, Hayward, J, Yeap, SL, Alkers, AE, Chan, RC (2010) Structural maintenance of chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability. PLoS Genet 6: pp. e1001028 CrossRef
  45. Lichten, M, Farmer, S, San-Segundo, PA, Arag贸n, L (2011) The Smc5鈥揝mc6 complex is required to remove chromosome junctions in meiosis. PLoS ONE 6: pp. e20948 CrossRef
  46. Pebernard, S (2004) Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol Biol Cell 15: pp. 4866-4876 CrossRef
  47. McAleenan, A, Cordon-Preciado, V, Clemente-Blanco, A, Liu, IC, Sen, N, Leonard, J, Jarmuz, A, Aragon, L (2012) SUMOylation of the alpha-kleisin subunit of cohesin is required for DNA damage-induced cohesion. Curr Biol 22: pp. 1564-1575 CrossRef
  48. Boavida, LC, McCormick, S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52: pp. 570-582 CrossRef
  49. Smyth, DR, Bowman, JL, Meyerowitz, EM (1990) Early flower development in Arabidopsis. Plant Cell 2: pp. 755-767 CrossRef
  50. Mori, T, Kuroiwa, H, Higashiyama, T, Kuroiwa, T (2006) Generative cell specific 1 is essential for angiosperm fertilization. Nat Cell Biol 8: pp. 64-71 CrossRef
  51. Ross, KJ, Fransz, P, Jones, GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: pp. 507-516 CrossRef
  52. Zhu, J, Chen, H, Li, H, Gao, JF, Jiang, H, Wang, C, Guan, YF, Yang, ZN (2008) Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55: pp. 266-277 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background MMS21 is a SUMO E3 ligase that is conserved in eukaryotes, and has previously been shown to be required for DNA repair and maintenance of chromosome integrity. Loss of the Arabidopsis MMS21 causes defective meristems and dwarf phenotypes. Results Here, we show a role for AtMMS21 during gametophyte development. AtMMS21 deficient plants are semisterile with shorter mature siliques and abortive seeds. The mms21-1 mutant shows reduced pollen number, and viability, and germination and abnormal pollen tube growth. Embryo sac development is also compromised in the mutant. During meiosis, chromosome mis-segregation and fragmentation is observed, and the products of meiosis are frequently dyads or irregular tetrads. Several transcripts for meiotic genes related to chromosome maintenance and behavior are altered. Moreover, accumulation of SUMO-protein conjugates in the mms21-1 pollen grains is distinct from that in wild-type. Conclusions Thus, these results suggest that AtMMS21 mediated SUMOylation may stabilize the expression and accumulation of meiotic proteins and affect gametophyte development.