BnaC.Tic40, a plastid inner membrane translocon originating from Brassica oleracea, is essential for tapetal function and microspore development in Brassica napus

Plant Journal

Volumn 68, Issue 3, 2011, Pages 532-545

  Dun, Xiaoling ^a   Zhou, Zhengfu ^a   Xia, Shengqian ^a   Wen, Jing ^a   Yi, Bin ^a   Shen, Jinxiong ^a   Ma, Chaozhi ^a   Tu, Jinxing ^a   Fu, Tingdong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arabidopsis Brassica collinearity; Brassica napus; Male sterility; Map based cloning; Tapetal function; Tic40.

Indexed keywords

BRASSICA NAPUS; COLLINEARITY; MALE STERILITY; MAP-BASED CLONING; TAPETAL FUNCTION; TIC40.;

CHLOROPHYLL; CLONING; DISSOLUTION; GENES; TRANSMISSION ELECTRON MICROSCOPY;

PLANTS (BOTANY);

CHLOROPLAST PROTEIN; MEMBRANE PROTEIN; VEGETABLE PROTEIN;

ARTICLE; BRASSICA; CHLOROPLAST; CHROMOSOME MAP; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; MOLECULAR CLONING; PLANT INFERTILITY; POLLEN; PROTEIN TRANSPORT; RAPESEED;

BRASSICA; BRASSICA NAPUS; CHLOROPLAST PROTEINS; CHLOROPLASTS; CHROMOSOME MAPPING; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; LIPID METABOLISM; MEMBRANE PROTEINS; PLANT INFERTILITY; PLANT PROTEINS; POLLEN; PROTEIN TRANSPORT; SEQUENCE ANALYSIS, DNA;

ARABIDOPSIS; BRASSICA; BRASSICA NAPUS; BRASSICA OLERACEA; BRASSICA RAPA;

EID: 80755168453     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04708.x     Document Type: Article

References (66)

1. Akita, M., Nielsen, E. and Keegstra, K. (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical crosslinking. J. Cell Biol. 136, 983-994. (Pubitemid 27131731)
2. Ariizumi, T., Hatakeyama, K., Hinata, K., Inatsugi, R., Nishida, I., Sato, S., Kato, T., Tabata, S. and Toriyama, K. (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J. 39, 170-181. (Pubitemid 38940808)
3. Babula, D., Kaczmarek, M., Barakat, A., Delseny, M., Quiros, C.F. and Sadowski, J. (2003) Chromosomal mapping of Brassica oleracea based on ESTs from Arabidopsis thaliana: complexity of the comparative map. Mol. Genet. Genomics, 268, 656-665. (Pubitemid 36286509)
4. Brown, G.G., Formanová , N., Jin, H., Richard, W., Dendy, C., Patil, P., Laforest, M., Zhang, J.F., Cheung, W.Y. and Landry, B.S. (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35, 262-272. (Pubitemid 36901071)
5. Canales, C., Bhatt, A.M., Scott, R. and Dickinson, H. (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12, 1718-1727. (Pubitemid 35169787)
6. Cavell, A.C., Lydiate, D.J., Parkin, I.A.P., Dean, C. and Trick, M. (1998) Collinearity between a 30-centimorgan segment of Arabidopsis thaliana chromosome 4 and duplicated regions within the Brassica napus genome. Genome, 41, 62-69. (Pubitemid 28226457)
7. Chou, M.-L., Fitzpatrick, L.M., Tu, S.-L., Budziszewski, G., Potter- Lewis, S., Akita, M., Levin, J.Z., Keegstra, K. and Li, H.-m. (2003) Tic40, a membraneanchored co-chaperone homologue in the chloroplast protein translocon. EMBO J. 22, 2970-2980. (Pubitemid 36758618)
8. Chou, M.-L., Chu, C.-C., Chen, L.-J., Akita, M. and Li, H.-m. (2006) Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J. Cell Biol. 175, 893-900. (Pubitemid 44969195)
9. Cline, K. and Henry, R. (1996) Import and routing nucleus-encoded chloroplast protein. Annu. Rev. Cell Dev. Biol. 12, 1-26. (Pubitemid 26422707)
10. Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C.E. and Schroeder, J.I. (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell, 17, 3350-3361.
11. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. (Pubitemid 38832724)
12. Goldberg, R.B., Beals, T.P. and Sanders, P.M. (1993) Anther development: basic principles and practical applications. Plant Cell, 5, 1217-1229. (Pubitemid 2001858)
13. Hajdukiewicz, P., Svab, Z. and Maliga, P. (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994. (Pubitemid 2152867)
14. Höhfeld, J., Minami, Y. and Hartl, F.U. (1995) Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell, 83, 589-598.
15. Hord, C.L., Chen, C., DeYoung, B.J., Clark, S.E. and Ma, H. (2006) The BAM1/ BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell, 18, 1667-1680. (Pubitemid 44025551)
16. Hsieh, K. and Huang, A.H.C. (2005) Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J. 43, 889-899.
17. Huang, Z., Chen, Y.F., Yi, B., Xiao, L., Ma, C.Z., Tu, J.X. and Fu, T.D. (2007) Fine mapping of the recessive genic male sterility gene (BnMs3) in Brassica napus L. Theor. Appl. Genet. 115, 113-118. (Pubitemid 46980431)
18. Huang, Z., Xiao, L., Dun, X.L. et al. (2010) Improvement of the recessive genic male sterile lines with a subgenomic background in Brassica napus by molecular marker-assisted selection. Mol. Breeding, doi:10.1007/s11032-010-9536- 8.
19. Kessler, F. and Blobel, G. (1996) Interaction of the protein import and folding machineries in the chloroplast. Proc. Natl Acad. Sci. USA, 93, 7684-7689. (Pubitemid 26277097)
20. Kovacheva, S., Bédard, J., Patel, R., Dudley, P., Twell, D., Ríos, G., Koncz, C. and Jarvis, P. (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 41, 412-428. (Pubitemid 40252760)
21. Lagercrantz, U. (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics, 150, 1217-1228. (Pubitemid 28510049)
22. Lagercrantz, U. and Lydiate, D.J. (1996) Comparative genome mapping in Brassica. Genetics, 4, 1903-1910. (Pubitemid 26427934)
23. Lamb, J., Tugendreich, S. and Hieter, P. (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem. Sci. 20, 257-259.
24. Lukens, L., Zou, F., Lydiate, D., Parkin, I. and Osborn, T. (2003) Comparison of a Brassica oleracea genetic map with the genome of Arabidopsis thaliana. Genetics, 164, 359-372. (Pubitemid 36617719)
25. Lysak, M.A., Koch, M.A., Pecinka, A. and Schubert, I. (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res. 15, 516-525. (Pubitemid 41065010)
26. Ma, H. (2005) Molecular genetic analysis of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393-434. (Pubitemid 40802416)
27. Mariani, C., De Beuckeleer, M., Truettner, J., Leemans, J. and Goldberg, R.B. (1990) Induction of male sterility in plants by achimeric ribonuclease gene. Nature, 347, 737-741. (Pubitemid 120029014)
28. Millar, A.A. and Gubler, F. (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell, 17, 705-721. (Pubitemid 43138215)
29. Nielsen, E., Akita, M., Davila-Aponte, J. and Keegstra, K. (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16, 935-946. (Pubitemid 27113173)
30. Pacini, E., Franchi, G.G. and Hesse, M. (1985) The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Syst. Evol. 149, 155-185.
31. Panjabi, P., Jagannath, A., Bisht, N.C., Padmaja, K.L., Sharma, S., Gupta, V., Pradhan, A.K. and Pental, D. (2008) Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genomics, 9(1), 113.
32. Papini, A., Mosti, S. and Brighigna, L. (1999) Programmed-cell death events during tapetum development of angiosperms. Protoplasma, 207, 213-221. (Pubitemid 29334994)
33. Parish, R.W. and Li, S.F. (2010) Death of a tapetum: a programme of developmental altruism. Plant Sci. 178, 73-89.
34. Parkin, I.A.P., Sharpe, A.G., Keith, D.J. and Lydiate, D.J. (1995) Identification of the A and C genomes of the amphidiploid Brassica napus (oilseed rape). Genome, 38, 1122-1131. (Pubitemid 3015089)
35. Parkin, I.A.P., Lydiate, D.J. and Trick, M. (2002) Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome, 45, 356-366. (Pubitemid 34253911)
36. Parkin, I.A.P., Gulden, S.M., Sharpe, A.G., Lukens, L., Trick, M., Osborn, T.C. and Lydiate, D.J. (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics, 171, 765-781. (Pubitemid 43158406)
37. Piffanelli, P., Ross, J.H.E. and Murphy, D.J. (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11, 65-80. (Pubitemid 28278548)
38. Platt, K.A., Huang, A.H.C. and Thomson, W.W. (1998) Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Westar during microsporogenesis. Int. J. Plant Sci. 159, 724-737. (Pubitemid 28476481)
39. Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.C., Lee, P.Y., Truong, M.T., Beals, T.P. and Goldberg, B. (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322. (Pubitemid 29087638)
40. Scheufler, C., Brinker, A., Bourenkov, G., Pegpraro, S., Morder, L., Bartunik, H., Hartl, F. and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell, 101, 199-210. (Pubitemid 32004747)
41. Schmidt, R. (2002) Plant genome evolution: lessons from comparative genomics at the DNA level. Plant Mol. Biol. 48, 21-37. (Pubitemid 34128490)
42. Schmidt, R., Acarkan, A. and Boivin, K. (2001) Comparative structural genomics in the Brassicaceae family. Plant Physiol. Biochem. 39, 253-262. (Pubitemid 32333319)
43. Scott, R.J. (1994) Pollen exine: the sporopollenin enigma and the physics of pattern. In Molecular and Cellular Aspects of Plant Reproduction (Scott, R.J. and Stead, M.A., eds). Cambridge, UK: Cambridge University Press, pp. 49-81.
44. Scott, R.J., Spielman, M. and Dickinson, H.G. (2004) Stamen structure and function. Plant Cell, 16(Suppl 1), S46-S60. (Pubitemid 38774216)
45. Shi, J., Tan, H.X., Yu, X.H. et al. (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell, doi: 10.1105/tpc.111.087528.
46. Shivanna, K.R., Cresti, M. and Ciampolini, F. (1997). Pollen development and pollen-pistil interaction. In Pollen Biotechnology for Crop Production and Improvement (Shivanna, K.R. and Sawhney, V.K., eds). Cambridge, UK: Cambridge University Press, pp. 15-39.
47. Snowdon, R.J. and Friedt, W. (2004) Molecular markers in Brassica oilseed breeding: current status and future possibilities. Plant Breed. 123, 1-8. (Pubitemid 38370237)
48. Soll, J. and Schleiff, E. (2004) Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198-208. (Pubitemid 38325801)
49. Sorensen, A., Krober, S., Unte, U.S., Huijser, P., Dekker, K. and Saedler, H. (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33, 413-423. (Pubitemid 36174894)
50. Stahl, T., Glockmann, C., Soll, J. and Heins, L. (1999) Tic40, a new 'old' subunit of the chloroplast protein import translocon. J. Biol. Chem. 274, 37467-37472.
51. Stieglitz, H. and Stern, H. (1973) Regulation ofβ-1, 3-glucanase activity in developing anthers of Lilium. Dev. Biol. 34, 169-173.
52. Udall, J., Quijada, P. and Osborn, T.C. (2004) Detection of chromosomal rearrangements derived from homologous recombination in four mapping populations of Brassica napus L. Genetics, 169, 967-979. (Pubitemid 40404326)
53. Willemsen, V., Wolkenfelt, H., de Vrieze, G., Weisbeek, P. and Scheres, B. (1998) The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development, 125, 521-531. (Pubitemid 28102658)
54. Wilson, Z.A. and Zhang, D.B. (2009) From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479-1492.
55. Wu, H.M. and Cheung, A.Y. (2000) Programmed cell death in plant reproduction. Plant Mol. Biol. 44, 267-281. (Pubitemid 32139545)
56. Wu, S.S., Platt, K.A., Ratnayake, C., Wang, T.W., Ting, J.T. and Huang, A.H. (1997) Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proc. Natl Acad. Sci. USA, 94, 12711-12716. (Pubitemid 27492594)
57. Wu, S.S.H., Moreau, R.A., Whitaker, B.D. and Huang, A.H.C. (1999) Steryl esters in the elaioplasts of the tapetum in developing Brassica anthers and their recovery on the pollen surface. Lipids, 34, 517-523. (Pubitemid 29262597)
58. Yang, S.L., Xie, L.F., Mao, H.Z., Puah, C.S., Yang, W.C., Jiang, L., Sundaresan, V. and Ye, D. (2003) TAPETUM DETERMINANT 1 is required for cell specialization in the Arabidopsis anther. Plant Cell, 15, 2792-2804. (Pubitemid 37546251)
59. Yang, S.L., Jiang, L., Puah, C.S., Xie, L.F., Zhang, X.Q., Chen, L.Q., Yang, W.C. and Ye, D. (2005) Overexpression of TAPETUM DETERMINANT 1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with EXCESS MICROSPOROCYTES 1/EXTRA SPOROGENOUS CELLS. Plant Physiol. 139, 186-191. (Pubitemid 43951602)
60. Yi, B., Zheng, F.Q., Lei, S.L., Chen, Y.N., Yao, X.Q., Wen, J., Shen, J.X., Mao, C.Z., Tu, J.X. and Fu, T.D. (2010) Two duplicate CYP704B1 homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. Plant J. 63, 925-938.
61. Yoo, S.D., Cho, Y.H. and Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 7, 1565-1572. (Pubitemid 47028844)
62. Zhang, W., Sun, Y.J., Timofejeva, L., Chen, C.B., Grossniklaus, U. and Ma, H. (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development, 133, 3085-3095. (Pubitemid 44404332)
63. Zhang, J., Lu, Y., Yuan, Y., Zhang, X., Geng, J., Chen, Y., Cloutier, S., McVetty, P.B. and Li, G. (2008) Map-based cloning and characterization of a gene controlling hairiness and seed coat color traits in Brassica rapa. Plant Mol. Biol. 69, 553-563.
64. Zhao, D.Z., Wang, G.F., Speal, B. and Ma, H. (2002) The EXCESS MICROSPOROCYTES 1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021-2031. (Pubitemid 34832928)
65. Zhu, J., Chen, H., Li, H., Gao, J.F., Jiang, H., Wang, C., Guan, Y.F. and Yang, Z.N. (2008) Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55, 266-277.
66. Zhu, Y., Dun, X.L., Zhou, Z.F., Xia, S.Q., Yi, B., Wen, J., Shen, J.X., Ma, C.Z., Tu, J.X. and Fu, T.D. (2010) A separation defect of tapetum cells and microspore mother cells results in male sterility in Brassica napus: the role of abscisic acid in early anther development. Plant Mol. Biol. 72, 111-123.