华癸中慢生根瘤菌7653R细胞分裂相关基因ftsZ1的缺失突变和共生表型研究
|
摘要
ftsZ基因是一个重要的细胞分裂相关基因,在真细菌中保守存在,在部分古菌和真核生物中也有发现。FtsZ蛋白在原核细胞及叶绿体、线粒体等质体分裂过程中发挥重要作用。当染色质复制并完成拟核分离,FtsZ即最早出现在分裂位点,直接参与并起始细胞分裂环的形成。大多数物种一般只含有一个ftsZ基因,有些物种基因组含有两个或更多的ftsZ基因。研究发现多种根瘤菌基因组中含有两个ftsZ基因：ftsZ1和ftsZ2。FtsZ1和FtsZ2虽具有一定的同源性但存在结构上的差异。
华癸中慢生根瘤菌7653R与紫云英共生形成不定型根瘤,具有不定型根瘤类菌体的典型分化特征,且其基因组中含有两个细胞分裂相关基因ftsZ。本研究旨在探讨其细胞分裂相关基因ftsZ1在类菌体分化发育过程中的功能。首先通过构建同源重组置换载体,利用三亲本接合转移和选择培养基,筛选获得双交换的ftsZ1缺失突变株Z5-17。对突变株的培养特征和共生表型进行了进一步的检测分析等实验研究。结果表明：培养条件下的Z5-17形态、大小和生长速度与野生菌株7653R没有明显差异；在共生条件下,与突变株z5-17共生的宿主紫云英植株表现出明显的氮饥饿状态,形成白色小瘤,仅检测到极微弱的固氮酶活性,但结瘤数量明显增多。根瘤组织石蜡切片和电镜切片观察发现,突变株z5-17类菌体细胞分化异常,功能性共生体形成受阻,根瘤菌持续性侵染-结瘤固氮的过程中断,根瘤表现出明显的提前衰老特征。最后,采用荧光定量PCR检测了ftsZ1基因的表达水平和特性,发现其白生培养条件下的表达水平明显高于共生条件。综合以上结果,不难看出ftsZ1基因突变虽不影响华癸中慢生根瘤菌7653R培养条件下的生理特性,但显著影响了其与紫云英的共生固氮功能,ftsZ1的正常表达为类菌体分化、并形成功能性共生体所必需。
ftsZ is an important cell-division gene, which ubiquitously exists in eubacteria, also in some Archaeas and eukaryotes. FtsZ protein is crucial for the division processes of prokaryotic cell and plastids, such as chloroplast and mitochondria. Once chromosome replication and separation are completed, FtsZ protein appears at the division site earliest, then participate in the initiation of division ring formation. Normally there is only one ftsZ gene in most species, but some particular ones have more than one. Recent studies reveal that some rhizobia species have two ftsZs:namely ftsZl and ftsZ2, which encoded two FtsZs with significant sequence similarity but difference in ultrastructure.
Mesorhizobium huakuii 7653R, which could form indeterminate nodules on legume plant-Astragalus sinicus, has the typical characteristics of bacteroid differentiation in indeterminate nodules and two ftsZs gene in genome. This work aimed at investigating the function of M. huakuii 7653R cell-division gene ftsZl during the process of bacteroid differentiation. Firstly, a replacement vector, with which partial deletion in ftsZl gene, was constructed for the homologous recombination. Followed by tri-parental transconjugation and screening on selective medium, a mutant strain Z5-17 undergone double crossover was obtained. The phenotypes of mutant strain Z5-17 under both free-living and symbiotic conditions were further examined and analyzed in details. The results showed that Z5-17 displayed similar morphology, size and growth speed as compared with wild type strain 7653R under free-living condition. However, when host plant A. sinicus was in symbiosis with Z5-17, it showed obvious nitrogen-deficiency features and formed small-white-nodules with hardly nitrogenase activity, but the nodule number was dramatically increased. Furthermore, paraffin section and ultrastructure observations were carried out for the 25-dpi (day post inoculation) nodules formed by wild type strain 7653R and mutant Z5-17, respectively. It was found that the mutant strain Z5-17 displayed abnormal bacteroid differentiation, and the functional symbiosome development was blocked, consequently resulting in the interruption of rhizobial chronic infection programme and the lost of symbiotic nitrogen fixation ability. Paraffin section of nodules induced by mutant Z5-17 exhibited prematurely senescence features. Finally, by using the real time PCR, it was revealed that the expression level of ftsZl under free-living condition was much higher than that in symbiotic root nodules. In summary, although the mutation of ftsZl had no significant influences on the physiological attributes of free-living M. huakuii 7653R, it led to the impairment of symbiotic nitrogen fixation ability with A. sinicus. The results suggest that the normal expression of ftsZl is indispensable for bacteroid differentiation and functional symbiosome formation.
华癸中慢生根瘤菌7653R与紫云英共生形成不定型根瘤,具有不定型根瘤类菌体的典型分化特征,且其基因组中含有两个细胞分裂相关基因ftsZ。本研究旨在探讨其细胞分裂相关基因ftsZ1在类菌体分化发育过程中的功能。首先通过构建同源重组置换载体,利用三亲本接合转移和选择培养基,筛选获得双交换的ftsZ1缺失突变株Z5-17。对突变株的培养特征和共生表型进行了进一步的检测分析等实验研究。结果表明：培养条件下的Z5-17形态、大小和生长速度与野生菌株7653R没有明显差异；在共生条件下,与突变株z5-17共生的宿主紫云英植株表现出明显的氮饥饿状态,形成白色小瘤,仅检测到极微弱的固氮酶活性,但结瘤数量明显增多。根瘤组织石蜡切片和电镜切片观察发现,突变株z5-17类菌体细胞分化异常,功能性共生体形成受阻,根瘤菌持续性侵染-结瘤固氮的过程中断,根瘤表现出明显的提前衰老特征。最后,采用荧光定量PCR检测了ftsZ1基因的表达水平和特性,发现其白生培养条件下的表达水平明显高于共生条件。综合以上结果,不难看出ftsZ1基因突变虽不影响华癸中慢生根瘤菌7653R培养条件下的生理特性,但显著影响了其与紫云英的共生固氮功能,ftsZ1的正常表达为类菌体分化、并形成功能性共生体所必需。
ftsZ is an important cell-division gene, which ubiquitously exists in eubacteria, also in some Archaeas and eukaryotes. FtsZ protein is crucial for the division processes of prokaryotic cell and plastids, such as chloroplast and mitochondria. Once chromosome replication and separation are completed, FtsZ protein appears at the division site earliest, then participate in the initiation of division ring formation. Normally there is only one ftsZ gene in most species, but some particular ones have more than one. Recent studies reveal that some rhizobia species have two ftsZs:namely ftsZl and ftsZ2, which encoded two FtsZs with significant sequence similarity but difference in ultrastructure.
Mesorhizobium huakuii 7653R, which could form indeterminate nodules on legume plant-Astragalus sinicus, has the typical characteristics of bacteroid differentiation in indeterminate nodules and two ftsZs gene in genome. This work aimed at investigating the function of M. huakuii 7653R cell-division gene ftsZl during the process of bacteroid differentiation. Firstly, a replacement vector, with which partial deletion in ftsZl gene, was constructed for the homologous recombination. Followed by tri-parental transconjugation and screening on selective medium, a mutant strain Z5-17 undergone double crossover was obtained. The phenotypes of mutant strain Z5-17 under both free-living and symbiotic conditions were further examined and analyzed in details. The results showed that Z5-17 displayed similar morphology, size and growth speed as compared with wild type strain 7653R under free-living condition. However, when host plant A. sinicus was in symbiosis with Z5-17, it showed obvious nitrogen-deficiency features and formed small-white-nodules with hardly nitrogenase activity, but the nodule number was dramatically increased. Furthermore, paraffin section and ultrastructure observations were carried out for the 25-dpi (day post inoculation) nodules formed by wild type strain 7653R and mutant Z5-17, respectively. It was found that the mutant strain Z5-17 displayed abnormal bacteroid differentiation, and the functional symbiosome development was blocked, consequently resulting in the interruption of rhizobial chronic infection programme and the lost of symbiotic nitrogen fixation ability. Paraffin section of nodules induced by mutant Z5-17 exhibited prematurely senescence features. Finally, by using the real time PCR, it was revealed that the expression level of ftsZl under free-living condition was much higher than that in symbiotic root nodules. In summary, although the mutation of ftsZl had no significant influences on the physiological attributes of free-living M. huakuii 7653R, it led to the impairment of symbiotic nitrogen fixation ability with A. sinicus. The results suggest that the normal expression of ftsZl is indispensable for bacteroid differentiation and functional symbiosome formation.
引文
1.陈能场,黄维南.黄酮类物质在豆科植物结瘤固氮中的作用.植物生理学通讯,1994,30：368-374.
2.黄家风,李克梅,王爱英,刘升学.豆科植物-根瘤菌共生固氮的分子机理.石河子大学学报(自然科学版),2002,6：74-78.
3.黄志宏,吕柳新.微生物与植物共生结瘤固氮的分子遗传学研究进展.福建农林大学学报(自然科学版),2002,31：67-72.
4.孔冬冬,王东,胡勇,鞠传丽,王英典,何奕昆,孙敬三.ftsZ基因与质体的分裂.科学通报,2003,48：755-760.
5.鞠传丽,孔冬冬,王东,胡勇,何奕昆.原核生物细胞分裂的调控机制.中国生物工程杂志,2002,22：17-21.
6.潘小军,贾婧婧,张敏,胡勇,何奕昆.叶绿体增殖调控机制研究进展.生物学通报,2009,44：1-4.
7.周俊初,刘孔鑫,杨润英,彭开蔓,孙晓青.广谱型花生根瘤菌97-1菌株在花生和大豆根瘤中的分化和繁殖能力.微生物学报,1992,32：278-284.
8. Adams D. W., Errington J. Bacterial cell division:assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol,2009,7:642-653.
9. Addinall S. G., Bi E., Lutkenhaus J. FtsZ ring formation in fts mutants. J Bacteriol, 1996,178:3877-3884.
10. Amos L. A., van den Ent F., Lowe J. Structural/functional homology between the bacterial and eukaryotic cytoskeletons. Curr Opin Cell Biol,2004,16:24-31.
11. Ampe F., Kiss E., Sabourdy F., Batut J. Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biol,2003,4:R15.
12. Baier R., Puppel H., Zelder O., Heiming E., Bauer E., Syring J. [Yersinia infection can simulate acute appendicitis]. Med Klin,1981,76:511-512.
13. Beech P. L., Gilson P. R. FtsZ and organelle division in Protists. Protist,2000,151: 11-16.
14. Begg K. J., Donachie W. D. Cell shape and division in Escherichia coli:experiments with shape and division mutants. J Bacteriol,1985,163:615-622.
15. Bi E., Dai K., Subbarao S., Beall B., Lutkenhaus J. FtsZ and cell division. Res Microbiol,1991,142:249-252.
16. Brewin N. J. Plant Cell Wall Remodelling in the Rhizobium-Legume Symbiosis. Critical Reviews in Plant Sciences,2004,23:293-316.
17. Bright L. J., Liang Y., Mitchell D. M., Harris J. M. The LATD Gene of Medicago truncatula Is Required for Both Nodule and Root Development. Molecular Plant-Microbe Interactions,2005,18:521-532.
18. Broughton W. J., Jabbouri S., Perret X. Keys to symbiotic harmony. J Bacteriol,2000, 182:5641-5652.
19. Caetano-Anolles G., Gresshoff P. M. Plant genetic control of nodulation. Annu Rev Microbiol,1991a,45:345-382.
20. Caetano-Anolles G., Gresshoff P. M. Plant Genetic Control of Nodulation. Annual Review of Microbiology,1991b,45:345-382.
21. Cermola M., Fedorova E., Tate R., Riccio A., Favre R., Patriarca E. J. Nodule invasion and symbiosome differentiation during Rhizobium etli-Phaseolus vulgaris symbiosis. Mol Plant Microbe Interact,2000,13:733-741.
22. Cheng J., Sibley C. D., Zaheer R., Finan T. M. A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology,2007,153:375-387.
23. Cohen H. P., Sarath G., Lee K., Wagner F. W. Soybean root nodule ultrastructure during dark-induced stress and recovery. Protoplasma,1986,132:69-75.
24. Coque L., Neogi P., Pislariu C., Wilson K. A., Catalano C., Avadhani M., Sherrier D. J., Dickstein R. Transcription of ENOD8 in Medicago truncatula Nodules Directs ENOD8 Esterase to Developing and Mature Symbiosomes. Molecular Plant-Microbe Interactions,2008,21:404-410.
25. Dai K., Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol,1992,174:6145-6151.
26. Dai W. J., Zeng Y., Xie Z. P., Staehelin C. Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J Bacteriol, 2008,190:5101-5110.
27. Deakin W. J., Broughton W. J. Symbiotic use of pathogenic strategies:rhizobial protein secretion systems. Nature Reviews Microbiology,2009,7:312-320.
28. Djordjevic M. A., Chen H. C., Natera S., Van Noorden G., Menzel C., Taylor S., Renard C., Geiger O., Weiller G. F. A global analysis of protein expression profiles in Sinorhizobium meliloti:discovery of new genes for nodule occupancy and stress adaptation. Mol Plant Microbe Interact,2003,16:508-524.
29. Erickson H. P. FtsZ, a prokaryotic homolog of tubulin? Cell,1995,80:367-370.
30. Foucher F., Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol,2000,43:773-786.
31. Fujiwara M., Yoshida S. Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem Biophys Res Commun,2001,287:462-467.
32. Galibert F., Finan T. M., Long S. R., Puhler A., Abola P., Ampe F., Barloy-Hubler F., Barnett M. J., Becker A., Boistard P., Bothe G., Boutry M., Bowser L., Buhrmester J., Cadieu E., Capela D., Chain P., Cowie A., Davis R. W., Dreano S., et al. The composite genome of the legume symbiont Sinorhizobium meliloti. Science,2001, 293:668-672.
33. Gargantini P. R., Gonzalez-Rizzo S., Chinchilla D., Raices M., Giammaria V., Ulloa R. M., Frugier F., Crespi M. D. A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J,2006,48:843-856.
34. Goodner B., Hinkle G., Gattung S., Miller N., Blanchard M., Qurollo B., Goldman B. S., Cao Y., Askenazi M., Halling C., Mullin L., Houmiel K., Gordon J., Vaudin M., Iartchouk O., Epp A., Liu F., Wollam C., Allinger M., Doughty D., et al. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science,2001,294:2323-2328.
35. Haag A. F., Wehmeier S., Beck S., Marlow V. L., Fletcher V., James E. K., Ferguson G. P. The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J Bacteriol,2009,191:4681-4686.
36. Hahn M., Studer D. Competitiveness of anif-Bradyrhizobium japonicum mutant against the wild-type strain. FEMS Microbiology Letters,1986,33:143-148.
37. Hakoyama T., Niimi K., Watanabe H., Tabata R., Matsubara J., Sato S., Nakamura Y., Tabata S., Jichun L., Matsumoto T., Tatsumi K., Nomura M., Tajima S., Ishizaka M., Yano K., Imaizumi-Anraku H., Kawaguchi M., Kouchi H., Suganuma N. Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature,2009,462:514-517.
38. Hirsch A. M., Smith C. A. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J Bacteriol,1987,169:1137-1146.
39. Kaneko T., Nakamura Y., Sato S., Asamizu E., Kato T., Sasamoto S., Watanabe A., Idesawa K., Ishikawa A., Kawashima K., Kimura T., Kishida Y, Kiyokawa C., Kohara M., Matsumoto M., Matsuno A., Mochizuki Y, Nakayama S., Nakazaki N., Shimpo S., et al. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement). DNA Res,2000,7:381-406.
40. Kaneko T., Nakamura Y, Sato S., Minamisawa K., Uchiumi T., Sasamoto S., Watanabe A., Idesawa K., Iriguchi M., Kawashima K., Kohara M., Matsumoto M., Shimpo S., Tsuruoka H., Wada T., Yamada M., Tabata S. Complete Genomic Sequence of Nitrogen-fixing Symbiotic Bacterium Bradyrhizobium japonicum USDA110. DNA Research,2002,9:189-197.
41. Kijne J. W. The fine structure of pea root nodules.2. Senescence and disintegration of the bacteroid tissue. Physiological Plant Pathology,1975,7:17-18, IN19-IN14, 19-21.
42. Kneen B. E., Larue T. A., Hirsch A. M., Smith C. A., Weeden N. F. sym 13-A Gene Conditioning Ineffective Nodulation in Pisum sativum. Plant Physiol,1990,94: 899-905.
43. Kobayashi H., Naciri-Graven Y, Broughton W. J., Perret X. Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol,2004,51:335-347.
44. Krol E., Becker A. Global transcriptional analysis of the phosphate starvation response in<i> Sinorhizobium meliloti</i> strains 1021 and 2011. Molecular Genetics and Genomics,2004,272:1-17.
45. Kuppusamy K. T., Endre G, Prabhu R., Penmetsa R. V., Veereshlingam H., Cook D. R., Dickstein R., Vandenbosch K. A. LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol,2004, 136:3682-3691.
46. Lodwig E. M., Hosie A. H., Bourdes A., Findlay K., Allaway D., Karunakaran R., Downie J. A., Poole P. S. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature,2003,422:722-726.
47. Lodwig E. M., Leonard M., Marroqui S., Wheeler T. R., Findlay K., Downie J. A., Poole P. S. Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids. Mol Plant Microbe Interact,2005,18:67-74.
48. Lowe J., Amos L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature,1998,391:203-206.
49. Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol,1980,142:615-620.
50. Ma X., Margolin W. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol,1999,181:7531-7544.
51. Maple J., Aldridge C., Mφller S. G. Plastid division is mediated by combinatorial assembly of plastid division proteins. The Plant Journal,2005a,43:811-823.
52. Maple J., Aldridge C., Moller S. G. Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant Journal,2005b,43:811-823.
53. Margolin W., Corbo J. C., Long S. R. Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J Bacteriol,1991, 173:5822-5830.
54. Margolin W., Long S. R. Rhizobium meliloti contains a novel second homolog of the cell division gene ftsZ. J Bacteriol,1994,176:2033-2043.
55. Margolin W. Themes and variations in prokaryotic cell division. FEMS Microbiol Rev,2000,24:531-548.
56. Marlow V. L., Haag A. F., Kobayashi H., Fletcher V., Scocchi M., Walker G. C., Ferguson G. P. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol,2009,191:1519-1527.
57. Matamoros M. A., Baird L. M., Escuredo P. R., Dalton D. A., Minchin F. R., Iturbe-Ormaetxe I., Rubio M. C., Moran J. F., Gordon A. J., Becana M. Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol,1999,121:97-112.
58. McAndrew R. S., Froehlich J. E., Vitha S., Stokes K. D., Osteryoung K. W. Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZl and FtsZ2 in higher plants. Plant Physiol,2001,127:1656-1666.
59. McAndrew R. S., Olson B. J. S. C., Kadirjan-Kalbach D. K., Chi-Ham C. L., Vitha S., Froehlich J. E., Osteryoung K. W. In vivo quantitative relationship between plastid division proteins FtsZ 1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochemical Journal,2008,412:367-378.
60. Mergaert P., Uchiumi T., Alunni B., Evanno G, Cheron A., Catrice O., Mausset A. E., Barloy-Hubler F., Galibert F., Kondorosi A., Kondorosi E. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A,2006,103:5230-5235.
61. Moller-Jensen J., Lowe J. Increasing complexity of the bacterial cytoskeleton. Curr Opin Cell Biol,2005,17:75-81.
62. Monahan-Giovanelli H., Pinedo C. A., Gage D. J. Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol,2006,140:661-670.
63. Morgan J. A., Bending G. D., White P. J. Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot,2005,56:1729-1739.
64. Muller J., Wiemken A., Boller T. Redifferentiation of bacteria isolated from Lotus japonicus root nodules colonized by Rhizobium sp. NGR234. J Exp Bot,2001,52: 2181-2186.
65. Mulley G, White J. P., Karunakaran R., Prell J., Bourdes A., Bunnewell S., Hill L., Poole P. S. Mutation of GOGAT prevents pea bacteroid formation and N(2) fixation by globally down-regulating transport of organic nitrogen sources. Mol Microbiol, 2011.
66. Naito Y., Fujie M., Usami S., Murooka Y., Yamada T. The involvement of a cysteine proteinase in the nodule development in Chinese milk vetch infected with Mesorhizobium huakuii subsp. rengei. Plant Physiol,2000,124:1087-1096.
67. Nogales E., Wolf S. G., Downing K. H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature,1998,391:199-203.
68. Novak K., Pesina K., Nebesarova J., Skrdleta V., Lisa L., Nasinec V. Symbiotic Tissue Degradation Pattern in the Ineffective Nodules of Three Nodulation Mutants of Pea (Pisum sativum L.). Annals of Botany,1995,76:303-313.
69. NUTMAN P. S. Studies on the Physiology of Nodule Formation. Annals of Botany, 1952,16:79-103.
70. Oka-Kira E., Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol,2006,9:496-502.
71. Oke V., Long S. R. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol Microbiol,1999a,32:837-849.
72. Oke V., Long S. R. Bacteroid formation in the Rhizobium-legume symbiosis. Curr Opin Microbiol,1999b,2:641-646.
73. Oono R., Denison R. F., Kiers E. T. Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol,2009,183:967-979.
74. Oono R., Denison R. F. Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol,2010,154:1541-1548.
75. Osteryoung K. W., Stokes K. D., Rutherford S. M., Percival A. L., Lee W. Y. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell,1998,10:1991-2004.
76. Osteryoung K. W., McAndrew R. S. The Plastid Division Machine. Annu Rev Plant Physiol Plant Mol Biol,2001,52:315-333.
77. Ott T., Sullivan J., James E. K., Flemetakis E., Gunther C., Gibon Y, Ronson C., Udvardi M. Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Mol Plant Microbe Interact,2009,22:800-808.
78. Paau A. S., Bloch C. B., Brill W. J. Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules. J Bacteriol,1980,143:1480-1490.
79. Parniske M. Intracellular accommodation of microbes by plants:a common developmental program for symbiosis and disease? Curr Opin Plant Biol,2000,3: 320-328.
80. Prell J., Poole P. Metabolic changes of rhizobia in legume nodules. Trends Microbiol, 2006,14:161-168.
81. Puppo A., Groten K., Bastian F., Carzaniga R., Soussi M., Lucas M. M., de Felipe M. R., Harrison J., Vanacker H., Foyer C. H. Legume nodule senescence:roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol, 2005,165:683-701.
82. Ratcliff W. C., Kadam S. V., Denison R. F. Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiol Ecol,2008,65: 391-399.
83. Rothfield L., Justice S., Garcia-Lara J. Bacterial cell division. Annu Rev Genet,1999, 33:423-448.
84. Rothfield L., Taghbalout A., Shih Y. L. Spatial control of bacterial division-site placement. Nat Rev Microbiol,2005,3:959-968.
85. Rothfield L. I., Shih Y. L., King G. Polar explorers:membrane proteins that determine division site placement. Cell,2001,106:13-16.
86. Sagan M., Huguet T., Barker D., Due G. Characterization of two classes of non-fixing mutants of pea plants (Pisum sativum L.). Plant Science,1993,95:55-66.
87. Sagan M., Huguet T., Due G. Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). Plant Science,1994,100:59-70.
88. Sakr S., Jeanjean R., Zhang C. C., Arcondeguy T. Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol, 2006,188:1396-1404.
89. Schnabel E., Journet E. P., de Carvalho-Niebel F., Due G., Frugoli J. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol,2005,58:809-822.
90. Schulze J. Source-sink manipulations suggest an N-feedback mechanism for the drop in N2 fixation during pod-filling in pea and broad bean. J Plant Physiol,2003,160: 531-537.
91. Schumpp O., Crevecoeur M., Broughton W. J., Deakin W. J. Delayed maturation of nodules reduces symbiotic effectiveness of the Lotus japonicus-Rhizobium sp. NGR234 interaction. J Exp Bot,2009,60:581-590.
92. Schumpp O., Deakin W. J. How inefficient rhizobia prolong their existence within nodules. Trends in Plant Science,2010,15:189-195.
93. Szczyglowski K., Kapranov P., Hamburger D., de Bruijn F. J. The Lotus japonicus LjNOD70 nodulin gene encodes a protein with similarities to transporters. Plant Mol Biol,1998,37:651-661.
94. Timmers A. C., Auriac M. C., Truchet G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development,1999,126:3617-3628.
95. Tsyganov V. E., Morzhina E. V., Stefanov S. Y., Borisov A. Y., Lebsky V. K., Tikhonovich I. A. The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule function. Mol Gen Genet,1998,259: 491-503.
96. Tsyganov V. E., Voroshilova V. A., Herrera-Cervera J. A., Sanjuan-Pinilla J. M., Borisov A. Y, Tikhonovich I. A., Priefer U. B., Olivares J., Sanjuan J. Developmental downregulation of rhizobial genes as a function of symbiosome differentiation in symbiotic root nodules of Pisum sativum. New Phytologist,2003, 159:521-530.
97. Van de Velde W., Guerra J. C., De Keyser A., De Rycke R., Rombauts S., Maunoury N., Mergaert P., Kondorosi E., Holsters M., Goormachtig S. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol,2006,141:711-720.
98. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., Satiat-Jeunemaitre B., Alunni B., Bourge M, Kucho K., Abe M., Kereszt A., Maroti G., Uchiumi T., Kondorosi E., Mergaert P. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science,2010, 327:1122-1126.
99. van den Ent F., Amos L., Lowe J. Bacterial ancestry of actin and tubulin. Current Opinion in Microbiology,2001,4:634-638.
100.van Spronsen P. C, Bakhuizen R., van Brussel A. A., Kijne J. W. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol,1994,64:88-94.
101.Vaughan S., Wickstead B., Gull K., Addinall S. Molecular Evolution of FtsZ Protein Sequences Encoded Within the Genomes of Archaea, Bacteria, and Eukaryota. Journal of Molecular Evolution,2004,58:19-29.
102.Verma D. P., Hong Z. Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol,1996,4:364-368.
103.Vernie T., Moreau S., de Billy F., Plet J., Combier J. P., Rogers C., Oldroyd G., Frugier F., Niebel A., Gamas P. EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula. Plant Cell, 2008,20:2696-2713.
104.Vitha S., McAndrew R. S., Osteryoung K. W. Ftsz Ring Formation at the Chloroplast Division Site in Plants. The Journal of Cell Biology,2001,153:111-120.
105.Wan X., Hontelez J., Lillo A., Guarnerio C., van de Peut D., Fedorova E., Bisseling T., Franssen H. Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. J Exp Bot,2007,58:2033-2041.
106. Wang D., Kong D. D., Ju C. L., Hu Y., He Y. K., Sun J. S. Effects of tobacco plastid division genes NtFtsZl and NtFtsZ2 on the division and morphology of chloroplasts. Acta Botanica Sinica,2002,44:838-844.
107. Wang X., Lutkenhaus J. FtsZ ring:the eubacterial division apparatus conserved in archaebacteria. Mol Microbiol,1996,21:313-319.
108.Yang F. J., Cheng L. L., Zhang L., Dai W. J., Liu Z., Yao N., Xie Z. P., Staehelin C. Y41O of Rhizobium sp. strain NGR234 is a symbiotic determinant required for symbiosome differentiation. J Bacteriol,2009,191:735-746.
109. Young K. D. The selective value of bacterial shape. Microbiol Mol Biol Rev,2006, 70:660-703.
110.Zhang X. X., Turner S. L., Guo X. W., Yang H. J., Debelle F., Yang G. P., Denarie J., Young J. P., Li F. D. The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Appl Environ Microbiol,2000,66: 2988-2995.
2.黄家风,李克梅,王爱英,刘升学.豆科植物-根瘤菌共生固氮的分子机理.石河子大学学报(自然科学版),2002,6：74-78.
3.黄志宏,吕柳新.微生物与植物共生结瘤固氮的分子遗传学研究进展.福建农林大学学报(自然科学版),2002,31：67-72.
4.孔冬冬,王东,胡勇,鞠传丽,王英典,何奕昆,孙敬三.ftsZ基因与质体的分裂.科学通报,2003,48：755-760.
5.鞠传丽,孔冬冬,王东,胡勇,何奕昆.原核生物细胞分裂的调控机制.中国生物工程杂志,2002,22：17-21.
6.潘小军,贾婧婧,张敏,胡勇,何奕昆.叶绿体增殖调控机制研究进展.生物学通报,2009,44：1-4.
7.周俊初,刘孔鑫,杨润英,彭开蔓,孙晓青.广谱型花生根瘤菌97-1菌株在花生和大豆根瘤中的分化和繁殖能力.微生物学报,1992,32：278-284.
8. Adams D. W., Errington J. Bacterial cell division:assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol,2009,7:642-653.
9. Addinall S. G., Bi E., Lutkenhaus J. FtsZ ring formation in fts mutants. J Bacteriol, 1996,178:3877-3884.
10. Amos L. A., van den Ent F., Lowe J. Structural/functional homology between the bacterial and eukaryotic cytoskeletons. Curr Opin Cell Biol,2004,16:24-31.
11. Ampe F., Kiss E., Sabourdy F., Batut J. Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biol,2003,4:R15.
12. Baier R., Puppel H., Zelder O., Heiming E., Bauer E., Syring J. [Yersinia infection can simulate acute appendicitis]. Med Klin,1981,76:511-512.
13. Beech P. L., Gilson P. R. FtsZ and organelle division in Protists. Protist,2000,151: 11-16.
14. Begg K. J., Donachie W. D. Cell shape and division in Escherichia coli:experiments with shape and division mutants. J Bacteriol,1985,163:615-622.
15. Bi E., Dai K., Subbarao S., Beall B., Lutkenhaus J. FtsZ and cell division. Res Microbiol,1991,142:249-252.
16. Brewin N. J. Plant Cell Wall Remodelling in the Rhizobium-Legume Symbiosis. Critical Reviews in Plant Sciences,2004,23:293-316.
17. Bright L. J., Liang Y., Mitchell D. M., Harris J. M. The LATD Gene of Medicago truncatula Is Required for Both Nodule and Root Development. Molecular Plant-Microbe Interactions,2005,18:521-532.
18. Broughton W. J., Jabbouri S., Perret X. Keys to symbiotic harmony. J Bacteriol,2000, 182:5641-5652.
19. Caetano-Anolles G., Gresshoff P. M. Plant genetic control of nodulation. Annu Rev Microbiol,1991a,45:345-382.
20. Caetano-Anolles G., Gresshoff P. M. Plant Genetic Control of Nodulation. Annual Review of Microbiology,1991b,45:345-382.
21. Cermola M., Fedorova E., Tate R., Riccio A., Favre R., Patriarca E. J. Nodule invasion and symbiosome differentiation during Rhizobium etli-Phaseolus vulgaris symbiosis. Mol Plant Microbe Interact,2000,13:733-741.
22. Cheng J., Sibley C. D., Zaheer R., Finan T. M. A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology,2007,153:375-387.
23. Cohen H. P., Sarath G., Lee K., Wagner F. W. Soybean root nodule ultrastructure during dark-induced stress and recovery. Protoplasma,1986,132:69-75.
24. Coque L., Neogi P., Pislariu C., Wilson K. A., Catalano C., Avadhani M., Sherrier D. J., Dickstein R. Transcription of ENOD8 in Medicago truncatula Nodules Directs ENOD8 Esterase to Developing and Mature Symbiosomes. Molecular Plant-Microbe Interactions,2008,21:404-410.
25. Dai K., Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol,1992,174:6145-6151.
26. Dai W. J., Zeng Y., Xie Z. P., Staehelin C. Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J Bacteriol, 2008,190:5101-5110.
27. Deakin W. J., Broughton W. J. Symbiotic use of pathogenic strategies:rhizobial protein secretion systems. Nature Reviews Microbiology,2009,7:312-320.
28. Djordjevic M. A., Chen H. C., Natera S., Van Noorden G., Menzel C., Taylor S., Renard C., Geiger O., Weiller G. F. A global analysis of protein expression profiles in Sinorhizobium meliloti:discovery of new genes for nodule occupancy and stress adaptation. Mol Plant Microbe Interact,2003,16:508-524.
29. Erickson H. P. FtsZ, a prokaryotic homolog of tubulin? Cell,1995,80:367-370.
30. Foucher F., Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol,2000,43:773-786.
31. Fujiwara M., Yoshida S. Chloroplast targeting of chloroplast division FtsZ2 proteins in Arabidopsis. Biochem Biophys Res Commun,2001,287:462-467.
32. Galibert F., Finan T. M., Long S. R., Puhler A., Abola P., Ampe F., Barloy-Hubler F., Barnett M. J., Becker A., Boistard P., Bothe G., Boutry M., Bowser L., Buhrmester J., Cadieu E., Capela D., Chain P., Cowie A., Davis R. W., Dreano S., et al. The composite genome of the legume symbiont Sinorhizobium meliloti. Science,2001, 293:668-672.
33. Gargantini P. R., Gonzalez-Rizzo S., Chinchilla D., Raices M., Giammaria V., Ulloa R. M., Frugier F., Crespi M. D. A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J,2006,48:843-856.
34. Goodner B., Hinkle G., Gattung S., Miller N., Blanchard M., Qurollo B., Goldman B. S., Cao Y., Askenazi M., Halling C., Mullin L., Houmiel K., Gordon J., Vaudin M., Iartchouk O., Epp A., Liu F., Wollam C., Allinger M., Doughty D., et al. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science,2001,294:2323-2328.
35. Haag A. F., Wehmeier S., Beck S., Marlow V. L., Fletcher V., James E. K., Ferguson G. P. The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J Bacteriol,2009,191:4681-4686.
36. Hahn M., Studer D. Competitiveness of anif-Bradyrhizobium japonicum mutant against the wild-type strain. FEMS Microbiology Letters,1986,33:143-148.
37. Hakoyama T., Niimi K., Watanabe H., Tabata R., Matsubara J., Sato S., Nakamura Y., Tabata S., Jichun L., Matsumoto T., Tatsumi K., Nomura M., Tajima S., Ishizaka M., Yano K., Imaizumi-Anraku H., Kawaguchi M., Kouchi H., Suganuma N. Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature,2009,462:514-517.
38. Hirsch A. M., Smith C. A. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J Bacteriol,1987,169:1137-1146.
39. Kaneko T., Nakamura Y., Sato S., Asamizu E., Kato T., Sasamoto S., Watanabe A., Idesawa K., Ishikawa A., Kawashima K., Kimura T., Kishida Y, Kiyokawa C., Kohara M., Matsumoto M., Matsuno A., Mochizuki Y, Nakayama S., Nakazaki N., Shimpo S., et al. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement). DNA Res,2000,7:381-406.
40. Kaneko T., Nakamura Y, Sato S., Minamisawa K., Uchiumi T., Sasamoto S., Watanabe A., Idesawa K., Iriguchi M., Kawashima K., Kohara M., Matsumoto M., Shimpo S., Tsuruoka H., Wada T., Yamada M., Tabata S. Complete Genomic Sequence of Nitrogen-fixing Symbiotic Bacterium Bradyrhizobium japonicum USDA110. DNA Research,2002,9:189-197.
41. Kijne J. W. The fine structure of pea root nodules.2. Senescence and disintegration of the bacteroid tissue. Physiological Plant Pathology,1975,7:17-18, IN19-IN14, 19-21.
42. Kneen B. E., Larue T. A., Hirsch A. M., Smith C. A., Weeden N. F. sym 13-A Gene Conditioning Ineffective Nodulation in Pisum sativum. Plant Physiol,1990,94: 899-905.
43. Kobayashi H., Naciri-Graven Y, Broughton W. J., Perret X. Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol Microbiol,2004,51:335-347.
44. Krol E., Becker A. Global transcriptional analysis of the phosphate starvation response in<i> Sinorhizobium meliloti</i> strains 1021 and 2011. Molecular Genetics and Genomics,2004,272:1-17.
45. Kuppusamy K. T., Endre G, Prabhu R., Penmetsa R. V., Veereshlingam H., Cook D. R., Dickstein R., Vandenbosch K. A. LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol,2004, 136:3682-3691.
46. Lodwig E. M., Hosie A. H., Bourdes A., Findlay K., Allaway D., Karunakaran R., Downie J. A., Poole P. S. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature,2003,422:722-726.
47. Lodwig E. M., Leonard M., Marroqui S., Wheeler T. R., Findlay K., Downie J. A., Poole P. S. Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids. Mol Plant Microbe Interact,2005,18:67-74.
48. Lowe J., Amos L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature,1998,391:203-206.
49. Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol,1980,142:615-620.
50. Ma X., Margolin W. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol,1999,181:7531-7544.
51. Maple J., Aldridge C., Mφller S. G. Plastid division is mediated by combinatorial assembly of plastid division proteins. The Plant Journal,2005a,43:811-823.
52. Maple J., Aldridge C., Moller S. G. Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant Journal,2005b,43:811-823.
53. Margolin W., Corbo J. C., Long S. R. Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J Bacteriol,1991, 173:5822-5830.
54. Margolin W., Long S. R. Rhizobium meliloti contains a novel second homolog of the cell division gene ftsZ. J Bacteriol,1994,176:2033-2043.
55. Margolin W. Themes and variations in prokaryotic cell division. FEMS Microbiol Rev,2000,24:531-548.
56. Marlow V. L., Haag A. F., Kobayashi H., Fletcher V., Scocchi M., Walker G. C., Ferguson G. P. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol,2009,191:1519-1527.
57. Matamoros M. A., Baird L. M., Escuredo P. R., Dalton D. A., Minchin F. R., Iturbe-Ormaetxe I., Rubio M. C., Moran J. F., Gordon A. J., Becana M. Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol,1999,121:97-112.
58. McAndrew R. S., Froehlich J. E., Vitha S., Stokes K. D., Osteryoung K. W. Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZl and FtsZ2 in higher plants. Plant Physiol,2001,127:1656-1666.
59. McAndrew R. S., Olson B. J. S. C., Kadirjan-Kalbach D. K., Chi-Ham C. L., Vitha S., Froehlich J. E., Osteryoung K. W. In vivo quantitative relationship between plastid division proteins FtsZ 1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochemical Journal,2008,412:367-378.
60. Mergaert P., Uchiumi T., Alunni B., Evanno G, Cheron A., Catrice O., Mausset A. E., Barloy-Hubler F., Galibert F., Kondorosi A., Kondorosi E. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A,2006,103:5230-5235.
61. Moller-Jensen J., Lowe J. Increasing complexity of the bacterial cytoskeleton. Curr Opin Cell Biol,2005,17:75-81.
62. Monahan-Giovanelli H., Pinedo C. A., Gage D. J. Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol,2006,140:661-670.
63. Morgan J. A., Bending G. D., White P. J. Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot,2005,56:1729-1739.
64. Muller J., Wiemken A., Boller T. Redifferentiation of bacteria isolated from Lotus japonicus root nodules colonized by Rhizobium sp. NGR234. J Exp Bot,2001,52: 2181-2186.
65. Mulley G, White J. P., Karunakaran R., Prell J., Bourdes A., Bunnewell S., Hill L., Poole P. S. Mutation of GOGAT prevents pea bacteroid formation and N(2) fixation by globally down-regulating transport of organic nitrogen sources. Mol Microbiol, 2011.
66. Naito Y., Fujie M., Usami S., Murooka Y., Yamada T. The involvement of a cysteine proteinase in the nodule development in Chinese milk vetch infected with Mesorhizobium huakuii subsp. rengei. Plant Physiol,2000,124:1087-1096.
67. Nogales E., Wolf S. G., Downing K. H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature,1998,391:199-203.
68. Novak K., Pesina K., Nebesarova J., Skrdleta V., Lisa L., Nasinec V. Symbiotic Tissue Degradation Pattern in the Ineffective Nodules of Three Nodulation Mutants of Pea (Pisum sativum L.). Annals of Botany,1995,76:303-313.
69. NUTMAN P. S. Studies on the Physiology of Nodule Formation. Annals of Botany, 1952,16:79-103.
70. Oka-Kira E., Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol,2006,9:496-502.
71. Oke V., Long S. R. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol Microbiol,1999a,32:837-849.
72. Oke V., Long S. R. Bacteroid formation in the Rhizobium-legume symbiosis. Curr Opin Microbiol,1999b,2:641-646.
73. Oono R., Denison R. F., Kiers E. T. Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol,2009,183:967-979.
74. Oono R., Denison R. F. Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol,2010,154:1541-1548.
75. Osteryoung K. W., Stokes K. D., Rutherford S. M., Percival A. L., Lee W. Y. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell,1998,10:1991-2004.
76. Osteryoung K. W., McAndrew R. S. The Plastid Division Machine. Annu Rev Plant Physiol Plant Mol Biol,2001,52:315-333.
77. Ott T., Sullivan J., James E. K., Flemetakis E., Gunther C., Gibon Y, Ronson C., Udvardi M. Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Mol Plant Microbe Interact,2009,22:800-808.
78. Paau A. S., Bloch C. B., Brill W. J. Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules. J Bacteriol,1980,143:1480-1490.
79. Parniske M. Intracellular accommodation of microbes by plants:a common developmental program for symbiosis and disease? Curr Opin Plant Biol,2000,3: 320-328.
80. Prell J., Poole P. Metabolic changes of rhizobia in legume nodules. Trends Microbiol, 2006,14:161-168.
81. Puppo A., Groten K., Bastian F., Carzaniga R., Soussi M., Lucas M. M., de Felipe M. R., Harrison J., Vanacker H., Foyer C. H. Legume nodule senescence:roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol, 2005,165:683-701.
82. Ratcliff W. C., Kadam S. V., Denison R. F. Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiol Ecol,2008,65: 391-399.
83. Rothfield L., Justice S., Garcia-Lara J. Bacterial cell division. Annu Rev Genet,1999, 33:423-448.
84. Rothfield L., Taghbalout A., Shih Y. L. Spatial control of bacterial division-site placement. Nat Rev Microbiol,2005,3:959-968.
85. Rothfield L. I., Shih Y. L., King G. Polar explorers:membrane proteins that determine division site placement. Cell,2001,106:13-16.
86. Sagan M., Huguet T., Barker D., Due G. Characterization of two classes of non-fixing mutants of pea plants (Pisum sativum L.). Plant Science,1993,95:55-66.
87. Sagan M., Huguet T., Due G. Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). Plant Science,1994,100:59-70.
88. Sakr S., Jeanjean R., Zhang C. C., Arcondeguy T. Inhibition of cell division suppresses heterocyst development in Anabaena sp. strain PCC 7120. J Bacteriol, 2006,188:1396-1404.
89. Schnabel E., Journet E. P., de Carvalho-Niebel F., Due G., Frugoli J. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol,2005,58:809-822.
90. Schulze J. Source-sink manipulations suggest an N-feedback mechanism for the drop in N2 fixation during pod-filling in pea and broad bean. J Plant Physiol,2003,160: 531-537.
91. Schumpp O., Crevecoeur M., Broughton W. J., Deakin W. J. Delayed maturation of nodules reduces symbiotic effectiveness of the Lotus japonicus-Rhizobium sp. NGR234 interaction. J Exp Bot,2009,60:581-590.
92. Schumpp O., Deakin W. J. How inefficient rhizobia prolong their existence within nodules. Trends in Plant Science,2010,15:189-195.
93. Szczyglowski K., Kapranov P., Hamburger D., de Bruijn F. J. The Lotus japonicus LjNOD70 nodulin gene encodes a protein with similarities to transporters. Plant Mol Biol,1998,37:651-661.
94. Timmers A. C., Auriac M. C., Truchet G. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development,1999,126:3617-3628.
95. Tsyganov V. E., Morzhina E. V., Stefanov S. Y., Borisov A. Y., Lebsky V. K., Tikhonovich I. A. The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule function. Mol Gen Genet,1998,259: 491-503.
96. Tsyganov V. E., Voroshilova V. A., Herrera-Cervera J. A., Sanjuan-Pinilla J. M., Borisov A. Y, Tikhonovich I. A., Priefer U. B., Olivares J., Sanjuan J. Developmental downregulation of rhizobial genes as a function of symbiosome differentiation in symbiotic root nodules of Pisum sativum. New Phytologist,2003, 159:521-530.
97. Van de Velde W., Guerra J. C., De Keyser A., De Rycke R., Rombauts S., Maunoury N., Mergaert P., Kondorosi E., Holsters M., Goormachtig S. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol,2006,141:711-720.
98. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., Satiat-Jeunemaitre B., Alunni B., Bourge M, Kucho K., Abe M., Kereszt A., Maroti G., Uchiumi T., Kondorosi E., Mergaert P. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science,2010, 327:1122-1126.
99. van den Ent F., Amos L., Lowe J. Bacterial ancestry of actin and tubulin. Current Opinion in Microbiology,2001,4:634-638.
100.van Spronsen P. C, Bakhuizen R., van Brussel A. A., Kijne J. W. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol,1994,64:88-94.
101.Vaughan S., Wickstead B., Gull K., Addinall S. Molecular Evolution of FtsZ Protein Sequences Encoded Within the Genomes of Archaea, Bacteria, and Eukaryota. Journal of Molecular Evolution,2004,58:19-29.
102.Verma D. P., Hong Z. Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol,1996,4:364-368.
103.Vernie T., Moreau S., de Billy F., Plet J., Combier J. P., Rogers C., Oldroyd G., Frugier F., Niebel A., Gamas P. EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula. Plant Cell, 2008,20:2696-2713.
104.Vitha S., McAndrew R. S., Osteryoung K. W. Ftsz Ring Formation at the Chloroplast Division Site in Plants. The Journal of Cell Biology,2001,153:111-120.
105.Wan X., Hontelez J., Lillo A., Guarnerio C., van de Peut D., Fedorova E., Bisseling T., Franssen H. Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development. J Exp Bot,2007,58:2033-2041.
106. Wang D., Kong D. D., Ju C. L., Hu Y., He Y. K., Sun J. S. Effects of tobacco plastid division genes NtFtsZl and NtFtsZ2 on the division and morphology of chloroplasts. Acta Botanica Sinica,2002,44:838-844.
107. Wang X., Lutkenhaus J. FtsZ ring:the eubacterial division apparatus conserved in archaebacteria. Mol Microbiol,1996,21:313-319.
108.Yang F. J., Cheng L. L., Zhang L., Dai W. J., Liu Z., Yao N., Xie Z. P., Staehelin C. Y41O of Rhizobium sp. strain NGR234 is a symbiotic determinant required for symbiosome differentiation. J Bacteriol,2009,191:735-746.
109. Young K. D. The selective value of bacterial shape. Microbiol Mol Biol Rev,2006, 70:660-703.
110.Zhang X. X., Turner S. L., Guo X. W., Yang H. J., Debelle F., Yang G. P., Denarie J., Young J. P., Li F. D. The common nodulation genes of Astragalus sinicus rhizobia are conserved despite chromosomal diversity. Appl Environ Microbiol,2000,66: 2988-2995.