Synchronization of cytoplasmic and transferred mitochondrial ribosomal protein gene expression in land plants is linked to Telo-box motif enrichment
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- 作者：Jie Wang (1)
Yu Wang (2)
Zhuo Wang (3)
Lei Liu (1)
Xin-Guang Zhu (2) (4)
Xiaotu Ma (5) (6) - 刊名：BMC Evolutionary Biology
- 出版年：2011
- 出版时间：December 2011
- 年：2011
- 卷：11
- 期：1
- 全文大小：5547KB
- 参考文献：1. Dyall SD, Brown MT, Johnson PJ: Ancient invasions: from endosymbionts to organelles. / Science 2004, 304:253鈥?57. CrossRef
2. Glockner G, Rosenthal A, Valentin K: The structure and gene repertoire of an ancient red algal plastid genome. / J Mol Evol 2000, 51:382鈥?90.
3. Gray MW, Burger G, Lang BF: Mitochondrial evolution. / Science 1999, 283:1476鈥?481. CrossRef
4. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D: Evolutionary analysis of Arabidopsis , cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. / Proc Natl Acad Sci USA 2002, 99:12246鈥?2251. CrossRef
5. Millar AH, Heazlewood JL, Kristensen B, Bruan HP, Moller IM: The Plant Mitochondrial Proteome. / Trends Plant Sci 2005, 10:36鈥?3. CrossRef
6. Giege P, Sweetlove LJ, Cognat V, Leaver CJ: Coordination of Nuclear and Mitochondrial Genome Expression during Mitochondrial Biogenesis in Arabidopsis. / Plant Cell 2005, 17:1497鈥?512. CrossRef
7. MacLean D, Jerome CA, Brown APC, Gary JC: Co-regulation of nuclear genes encoding plastid ribosomal proteins by light and plastid signals during seedling development in tobacco and Arabidopsis . / Plant Mol Biol 2008, 66:475鈥?90. CrossRef
8. Pfannschmidt T: Plastidial retrograde signalling - a true "plastid factor" or just metabolite signatures? / Trends Plant Sci 2010, 15:427鈥?35. CrossRef
9. Alberts B, Johnson A, Lewis J, Raf M, Roberts K, Walter P: / The molecular biology of the cell. 4th edition. Garland Science, Abingdon, New York; 2002:1268 pp.
10. Byrne ME: A role for the ribosome in development. / Trends Plant Sci 2009, 14:512鈥?19. CrossRef
11. Schippers JHM, Mueller-Roeber B: Ribosomal composition and control of leaf development. / Plant Sci 2010, 179:307鈥?15. CrossRef
12. Bailey TL, Elkan C: Fitting a mixture model by expectation maximization to discover motifs in biopolymers. / Proc Int Conf Intell Syst Mol Biol 1994, 2:28鈥?6.
13. Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P: Arabidopsis TCP20 links regulation of growth and cell division control pathways. / Proc Natl Acad Sci USA 2005, 102:12978鈥?2983. CrossRef
14. Hughes JD, Estep PW, Tavazoie S, Church GM: Computational identification of cis -regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae . / Journal of Molecular Biology 2000, 296:1205鈥?214. CrossRef
15. Smith AD, Sumazin P, Zhang MQ: Identifying tissue-selective transcription factor binding sites in vertebrate promoters. / Proc Natl Acad Sci USA 2005, 102:1560鈥?565. CrossRef
16. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. / Nat Protoc 2009, 4:44鈥?7. CrossRef
17. Ma X, Zhang K, Li X: Evolution of Drosophila ribosomal protein gene core promoters. / Gene 2009, 432:54鈥?9. CrossRef
18. Chen FW, Ioannou YA: Ribosomal proteins in cell proliferation and apoptosis. / Int Rev Immunol 1999, 18:429鈥?48. CrossRef
19. Manevski A, Bertoni G, Bardet C, Tremousaygue D, Lescure B: In synergy with various cis -acting elements, plant insterstitial telomere motifs regulate gene expression in Arabidopsis root meristems. / FEBS Lett 2000, 483:43鈥?6. CrossRef
20. Tremousaygue D, Garnier L, Bardet C, Dabos P, Herve C, Lescure B: Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. / Plant J 2003, 33:957鈥?66. CrossRef
21. Tremousaygue D, Manevski A, Bardet C, Lescure N, Lescure B: Plant interstitial telomere motifs participate in the control of gene expression in root meristems. / Plant J 1999, 20:553鈥?61. CrossRef
22. Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG: The genome sequence of Rickettsia prowazekii and the origin of mitochondria. / Nature 1998, 396:133鈥?40. CrossRef
23. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR: Mitochondrial origins. / Proc Natl Acad Sci USA 1985, 82:4443鈥?447. CrossRef
24. Raven JA, Allen JF: Genomics and chloroplast evolution: what did cyanobacteria do for plants? / Genome Biol 2003, 4:209. CrossRef
25. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collen J, Corre E, Silva CD, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CMM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Kupper FC, Lang D, Bail AL, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collen P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Segurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, von Dassow P, Yamagishi T, Van de Peer Y, Wincker P: The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. / Nature 2010, 465:617鈥?21. CrossRef
26. Dittami SM, Scornet D, Petit JL, Segurens B, Silva CD, Corre E, Dondrup M, Glatting KH, Konig R, Sterck L, Rouze P, Van de Peer Y, Cock JM, Boyen C, Tonon T: Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. / Genome Biol 2009, 10:R66. CrossRef
27. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Chlamydomonas Annotation Team, JGI Annotation Team, Grigoriev IV, Rokhsar DS, Grossman AR: The Chlamydomonas genome reveals the evolution of key animal and plant functions. / Science 2007, 318:245鈥?51. CrossRef
28. Tanay A, Regev A, Shamir A: Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. / Proc Natl Acad Sci USA 2005, 102:7203鈥?208. CrossRef
29. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, Barkai N: Rewiring of the yeast transcriptional network through the evolution of motif usage. / Science 2005, 309:938鈥?40. CrossRef
30. Li W, Saunders MA: The chimpanzee and us. / Nature 2005, 437:50鈥?1. CrossRef
31. Herve C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D: In v ivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. / Plant Physiol 2009, 149:1462鈥?477. CrossRef
32. Perry RP: The architecture of mammalian ribosomal protein promoters. / BMC Evol Biol 2005, 5:15. CrossRef
33. Richards EJ, Ausubel FM: Isolation of a higher eukaryotic telomere from Arabidopsis thaliana . / Cell 1988, 53:127鈥?36. CrossRef
34. Axelos M, Bardet C, Liboz T, Le Van Thai A, Curie C, Lescure B: The gene family encoding the Arabidopsis thaliana translation elongation factor EF-1伪: molecular cloning, characterization and expression. / Mol Gen Genet 1989, 219:106鈥?12. CrossRef
35. Curie C, Liboz T, Bardet C, Gander E, Medale C, Axelos M, Lescure B: Cis and trans -acting elements involved in the activation of the Arabidopsis thaliana A1 gene encoding the translation elongation factor EF-1 伪 . / Nucleic Acids Res 1991, 19:1305鈥?310. CrossRef
36. Liboz T, Bardet C, Le Van Thai A, Axelos M, Lescure B: The four members of the gene family encoding the Arabidopsis thaliana translation elongation factor EF-1伪 are actively transcribed. / Plant Mol Biol 1989, 14:107鈥?10. CrossRef
37. Shewmaker CK, Ridge NP, Pokalsky AR, Rose RE, Hiatt WR: Nucleotide sequence of an EF-1 alpha genomic clone from tomato. / Nucleic Acids Res 1990, 18:4276. CrossRef
38. Maaloe O, Kjeligard NO: / Control of macromolecular synthesis. WA Benjamin, Inc, New York; 1966.
39. Beemster GTS, Fiorani F, Inz D: Cell cycle: the key to plant growth control? / Trends Plant Sci 2003, 8:154鈥?58. CrossRef
40. Tyson JJ, Chen K, Novak B: Network dynamics and cell physiology. / Nat Rev Mol Cell Biol 2001, 2:908鈥?16. CrossRef
41. Bergemann AD, Johnson EM: The HeLa Pur factor binds single-stranded DNA at a specific element conserved in gene flanking regions and origins of DNA replication. / Mol Cell Biol 1992, 12:1257鈥?265.
42. Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV: Gene transfer to the nucleus and the evolution of chloroplasts. / Nature 1998, 393:162鈥?65. CrossRef
43. Woodson JD, Chory J: Coordination of gene expression between organellar and nuclear genomes. / Nature 2008, 9:383鈥?95.
44. Wang Z, Zhu XG, Chang X, Chen YZ, Li YX, Liu L: Though with constraints imposed by endosymbiosis, preferential attachment is still a plausible mechanism responsible for the evolution of the chloroplast metabolic network. / J Evol Biol 2009, 22:71鈥?9. CrossRef
45. Wang Z, Zhu XG, Chen YZ, Li YY, Hou J, Li Y, Liu L: Exploring photosynthesis evolution by comparative analysis of metabolic networks between chloroplasts and photosynthetic bacteria. / BMC Genomics 2006., 7:
46. Voss I, Koelmann M, Wojtera J, Holtgrefe S, Kitzmann C, Backhausen JE, Scheibe R: Knockout of major leaf ferredoxin reveals new redox-regulatory adaptations in Arabidopsis thaliana . / Physiol Plant 2008, 133:584鈥?98. CrossRef
47. Arai T, Kelly VP, Minowa O, Noda T, Nishimura S: High accumulation of oxidative DNA damage, 8-hydroxyguanine, in Mmh/Ogg1 deficient mice by chronic oxidative stress. / Carcinogenesis 2002, 23:2005鈥?010. CrossRef
48. Ledford HK, Niyogi KK: Singlet oxygen and photo-oxidative stress management in plants and algae. / Plant Cell and Environ 2005, 28:1037鈥?045. CrossRef
49. Niyogi KK: Photoprotection revisited: Genetic and molecular approaches. / Annu Rev Plant Physiol Plant Mol Biol 1999, 50:333鈥?59. CrossRef
50. Pregueiro AM, Liu QY, Baker CL, Dunlap JC, Loros JJ: The Neurospora checkpoint kinase 2: A regulatory link between the circadian and cell cycles. / Science 2006, 313:644鈥?49. CrossRef
51. Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A: Coupling of human circadian and cell cycles by the timeless protein. / Mol and Cell Biol 2005, 25:3109鈥?116. CrossRef
52. Medina M: Genomes, phylogeny, and evolutionary systems biology. / Proc Natl Acad Sci USA 2005, 102:6630鈥?635. CrossRef
53. Hedges SB: The origin and evolution of model organisms. / Nat Rev Genet 2002, 3:838鈥?49. CrossRef
54. Nielsen H, Engelbrecht J, Brunak S, von Heijne G: Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. / Protein Eng 1997, 10:1鈥?. CrossRef
55. Nakao A, Yoshihama M, Kenmochi N: RPG: the ribosomal protein gene database. / Nucleic Acids Res 2004, 32:D168-D170. CrossRef
56. Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates JR III, Mayfield SP: Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome: identification of proteins unique to the 70S ribosome. / J Biol Chem 2003, 278:33774鈥?3785. CrossRef
57. Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, Yates JR III, Mayfield SP: Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. / The Plant Cell 2002, 14:2957鈥?974. CrossRef
58. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU: A gene expression map of Arabidopsis thaliana development. / Nat Genet 2005, 37:501鈥?06. CrossRef
59. Baerenfaller K, Grossmann J, Grobei MA, Hull R, Hirsch-Hoffmann M, Yalovsky S, Zimmermann P, Grossniklaus U, Gruissem W, Baginsky S: Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. / Science 2008, 320:938鈥?41. CrossRef
60. Hyams J, Davies DR: The induction and characterization of cell wall mutants of Chlamydomonas reinhardi . / Mutat Res 1972, 14:381鈥?89.
61. Gorman DS, Levine RP: Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi . / Proc Natl Acad Sci USA 1965, 54:1665鈥?669. CrossRef
62. Vila M, Couso I, Leon R: Carotenoid content in mutants of the chlorophyte Chlamydomonas reinhardtii with low expression levels of phytoene desaturase. / Proc Biochem 2008, 43:1147鈥?152. CrossRef
63. Gonzalez-Ballester D, Camargo A, Fernandez E: Ammonium transported genes in Chlamydomonas : the nitrate-specific regulatory gene Nit2 is involved in Amt1 ;1 expression. / Plant Mol Biol 2004, 56:863鈥?78. CrossRef - 作者单位：Jie Wang (1)
Yu Wang (2)
Zhuo Wang (3)
Lei Liu (1)
Xin-Guang Zhu (2) (4)
Xiaotu Ma (5) (6)
1. Key Laboratory of Systems Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 320 Yueyang Road, Shanghai, China
2. Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Room 342, Physiology Building, 320 Yueyang Road, Shanghai, China
3. School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, China
4. Institute of Plant Physiology and Ecology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, China
5. Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, China
6. Department of Molecular and Cell Biology, Center for Systems Biology, University of Texas at Dallas, 800 W. Campbell Road, Richardson, TX, 75080, USA
文摘
Background Chloroplasts and mitochondria evolved from the endosymbionts of once free-living eubacteria, and they transferred most of their genes to the host nuclear genome during evolution. The mechanisms used by plants to coordinate the expression of such transferred genes, as well as other genes in the host nuclear genome, are still poorly understood. Results In this paper, we use nuclear-encoded chloroplast (cpRPGs), as well as mitochondrial (mtRPGs) and cytoplasmic (euRPGs) ribosomal protein genes to study the coordination of gene expression between organelles and the host. Results show that the mtRPGs, but not the cpRPGs, exhibit strongly synchronized expression with euRPGs in all investigated land plants and that this phenomenon is linked to the presence of a telo-box DNA motif in the promoter regions of mtRPGs and euRPGs. This motif is also enriched in the promoter regions of genes involved in DNA replication. Sequence analysis further indicates that mtRPGs, in contrast to cpRPGs, acquired telo-box from the host nuclear genome. Conclusions Based on our results, we propose a model of plant nuclear genome evolution where coordination of activities in mitochondria and chloroplast and other cellular functions, including cell cycle, might have served as a strong selection pressure for the differential acquisition of telo-box between mtRPGs and cpRPGs. This research also highlights the significance of physiological needs in shaping transcriptional regulatory evolution.