Adjustment of host cells for accommodation of symbiotic bacteria: Vacuole defunctionalization, HOPS suppression, and TIP1g retargeting in medicago

Plant Cell

Volumn 26, Issue 9, 2014, Pages 3809-3822

  Gavrin, Aleksandr ^a,e   Kaiser, Brent N ^b   Geiger, Dietmar ^c   Tyerman, Stephen D ^b   Wen, Zhengyu ^b   Bisseling, Ton ^a,d   Fedorova, Elena E ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; BIOLOGICAL MARKER; MULTIPROTEIN COMPLEX; VEGETABLE PROTEIN;

BARREL MEDIC; CELL MEMBRANE; CELL VACUOLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; NODULATION; PH; PROTEIN TRANSPORT; RNA INTERFERENCE; STAINING; SYMBIOSIS; TRANSGENIC PLANT;

ACIDS; BIOLOGICAL MARKERS; CELL MEMBRANE; GENE EXPRESSION REGULATION, PLANT; HYDROGEN-ION CONCENTRATION; MEDICAGO TRUNCATULA; MULTIPROTEIN COMPLEXES; NITROGEN FIXATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; RNA INTERFERENCE; ROOT NODULES, PLANT; STAINING AND LABELING; SYMBIOSIS; VACUOLES;

EID: 84908254966     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.128736     Document Type: Article

References (53)

1. Avila-Ospina, L., Moison, M., Yoshimoto, K., and Masclaux-Daubresse, C. (2014). Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot. 65: 3799-3811.
2. Bak, G., Lee, E.-J., Lee, Y., Kato, M., Segami, S., Sze, H., Maeshima, M., Hwang, J.-U., and Lee, Y. (2013). Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3, 5-bisphosphate. Plant Cell 25: 2202-2216.
3. Balderhaar, H. J., and Ungermann, C. (2013). CORVET and HOPS tethering complexes-Coordinators of endosome and lysosome fusion. J. Cell Sci. 126: 1307-1316.
4. Bassham, D. C., Laporte, M., Marty, F., Moriyasu, Y., Ohsumi, Y., Olsen, L. J., and Yoshimoto, K. (2006). Autophagy in development and stress responses of plants. Autophagy 2: 2-11.
5. Behnia, R., and Munro, S. (2005). Organelle identity and the signposts for membrane traffic. Nature 438: 597-604.
6. Brett, C. L., and Merz, A. J. (2008). Osmotic regulation of Rab-mediated organelle docking. Curr. Biol. 18: 1072-1077.
7. Brumell, J. H., and Scidmore, M. A. (2007). Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71: 636-652.
8. Catalano, C. M., Czymmek, K. J., Gann, J. G., and Sherrier, D. J. (2007). Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225: 541-550.
9. Chaumont, F., and Tyerman, S. D. (2014). Aquaporins: Highly regulated channels controlling plant water relations. Plant Physiol. 164: 1600-1618.
10. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.-D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
11. Dubrovsky, J. G., Guttenberger, M., Saralegui, A., Napsucialy-Mendivil, S., Voigt, B., Baluska, F., and Menzel, D. (2006). Neutral red as a probe for confocal laser scanning microscopy studies of plant roots. Ann. Bot. (Lond.) 97: 1127-1138.
12. Dupont, L., Alloing, G., Pierre, O., Msehli, S. E., Hopkins, J., and Hérouart, D. P. F. (2012). The legume root nodule: From symbiotic nitrogen fixation to senescence. In Senescence, T. Nagata, ed (In-Tech), pp. 137-168.
13. Etienne, A., Génard, M., Lobit, P., Mbeguié-A-Mbéguié, D., and Bugaud, C. (2013). What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J. Exp. Bot. 64: 1451-1469.
14. Farkas, A., Maróti, G., Durgő, H., Györgypál, Z., Lima, R. M., Medzihradszky, K. F., Kereszt, A., Mergaert, P., and Kondorosi, É. (2014). Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc. Natl. Acad. Sci. USA 111: 5183-5188.
15. Fedorova, E. E., and Brown, S. (2007). Cytochemistry of proteolytic activity and pH status of vacuoles in Medicago truncatula root nodules. Russ. J. Plant Physiol. 54: 25-31.
16. Fetter, K., Van Wilder, V., Moshelion, M., and Chaumont, F. (2004). Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16: 215-228.
17. Forrest, K. L., and Bhave, M. (2007). Major intrinsic proteins (MIPs) in plants: A complex gene family with major impacts on plant phenotype. Funct. Integr. Genomics 7: 263-289.
18. Gattolin, S., Sorieul, M., Hunter, P. R., Khonsari, R. H., and Frigerio, L. (2009). In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots. BMC Plant Biol. 9: 133.
19. Han, J., and Burgess, K. (2010). Fluorescent indicators for intracellular pH. Chem. Rev. 110: 2709-2728.
20. Hurth, M. A., Suh, S. J., Kretzschmar, T., Geis, T., Bregante, M., Gambale, F., Martinoia, E., and Neuhaus, H. E. (2005). Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiol. 137: 901-910.
21. Huynh, K. K., and Grinstein, S. (2007). Regulation of vacuolar pH and its modulation by some microbial species. Microbiol. Mol. Biol. Rev. 71: 452-462.
22. Hwang, J. H., Ellingson, S. R., and Roberts, D. M. (2010). Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett. 584: 4339-4343.
23. Isberg, R. R., O'Connor, T. J., and Heidtman, M. (2009). The Legionella pneumophila replication vacuole: Making a cosy niche inside host cells. Nat. Rev. Microbiol. 7: 13-24.
24. Ivanov, S., Fedorova, E. E., Limpens, E., De Mita, S., Genre, A., Bonfante, P., and Bisseling, T. (2012). Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. USA 109: 8316-8321.
25. Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjövall, S., Fraysse, L., Weig, A. R., and Kjellbom, P. (2001). The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126: 1358-1369.
26. Kaldenhoff, R., and Fischer, M. (2006). Aquaporins in plants. Acta Physiol. (Oxf.) 187: 169-176.
27. Li, L., et al. (2012). The invasion of tobacco mosaic virus RNA induces endoplasmic reticulum stress-related autophagy in HeLa cells. Biosci. Rep. 32: 171-186.
28. Limpens, E., Ivanov, S., van Esse, W., Voets, G., Fedorova, E., and Bisseling, T. (2009). Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21: 2811-2828.
29. Limpens, E., Mirabella, R., Fedorova, E., Franken, C., Franssen, H., Bisseling, T., and Geurts, R. (2005). Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl. Acad. Sci. USA 102: 10375-10380.
30. Maagd, R. A. d., Yang, W.-C., Roo, G.-d., Mulders, I. H. M., Roest, H. P., Spaink, H. P., Bisseling, T., and Lugtenberg, B. J. J. (1994). Down-regulation of expression of the Rhizobium leguminosarum outer membrane protein gene ropA occurs abruptly in interzone II-III of pea nodules and can be uncoupled from nif gene activation. Mol. Plant Microbe Interact. 7: 279-281.
31. Maurel, C., Santoni, V., Luu, D.-T., Wudick, M. M., and Verdoucq, L. (2009). The cellular dynamics of plant aquaporin expression and functions. Curr. Opin. Plant Biol. 12: 690-698.
32. Nickerson, D. P., Brett, C. L., and Merz, A. J. (2009). Vps-C complexes: Gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21: 543-551.
33. Reisen, D., Marty, F., and Leborgne-Castel, N. (2005). New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol. 5: 13.
34. Rojo, E., Gillmor, C. S., Kovaleva, V., Somerville, C. R., and Raikhel, N. V. (2001). VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1: 303-310.
35. Rojo, E., Zouhar, J., Kovaleva, V., Hong, S., and Raikhel, N. V. (2003). The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in Arabidopsis. Mol. Biol. Cell 14: 361-369.
36. Schnitzer, D., Seidel, T., Sander, T., Golldack, D., and Dietz, K.-J. (2011). The cellular energization state affects peripheral stalk stability of plant vacuolar H+-ATPase and impairs vacuolar acidification. Plant Cell Physiol. 52: 946-956.
37. Sujkowska, M., Górska-Czekaj, M., Bederska, M., and Borucki, W. (2011). Vacuolar organization in the nodule parenchyma is important for the functioning of pea root nodules. Symbiosis 54: 1-16.
38. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
39. Tarsio, M., Zheng, H., Smardon, A. M., Martínez-Muñoz, G. A., and Kane, P. M. (2011). Consequences of loss of Vph1 protein-containing vacuolar ATPases (V-ATPases) for overall cellular pH homeostasis. J. Biol. Chem. 286: 28089-28096.
40. Uemura, T., Yamamoto, M., Kametaka, A., Sou, Y. S., Yabashi, A., Yamada, A., Annoh, H., Kametaka, S., Komatsu, M., and Waguri, S. (2014). A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol. Cell. Biol. 34: 1695-1706.
41. Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., and Leunissen, J. A. M. (2007). Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35: W71-W74.
42. Van de Velde, W., Guerra, J. C. P., De Keyser, A., De Rycke, R., Rombauts, S., Maunoury, N., Mergaert, P., Kondorosi, E., Holsters, M., and Goormachtig, S. (2006). Aging in legume symbiosis: A molecular view on nodule senescence in Medicago truncatula. Plant Physiol. 141: 711-720.
43. Vasse, J., de Billy, F., Camut, S., and Truchet, G. (1990). Correlation between ultrastructural differentiation of bacteroids nitrogen fixation in alfalfa nodules. J. Bacteriol. 172: 4295-4306.
44. Vera-Estrella, R., Barkla, B. J., Bohnert, H. J., and Pantoja, O. (2004). Novel regulation of aquaporins during osmotic stress. Plant Physiol. 135: 2318-2329.
45. Vermeer, J. E. M., von Wangenheim, D., Barberon, M., Lee, Y., Stelzer, E. H. K., Maizel, A., and Geldner, N. (2014). A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343: 178-183.
46. Vijn, I., Christiansen, H., Lauridsen, P., Kardailsky, I., Quandt, H.-J., Broer, I., Drenth, J., Ostergaard Jensen, E., van Kammen, A., and Bisseling, T. (1995). A 200 bp region of the pea ENOD12 promoter is sufficient for nodule-specific and nod factor induced expression. Plant Mol. Biol. 28: 1103-1110.
47. von Bargen, K., Polidori, M., Becken, U., Huth, G., Prescott, J. F., and Haas, A. (2009). Rhodococcus equi virulence-associated protein A is required for diversion of phagosome biogenesis but not for cytotoxicity. Infect. Immun. 77: 5676-5681.
48. Wang, D., Griffitts, J., Starker, C., Fedorova, E., Limpens, E., Ivanov, S., Bisseling, T., and Long, S. (2010). A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126-1129.
49. White, J., Prell, J., James, E. K., and Poole, P. (2007). Nutrient sharing between symbionts. Plant Physiol. 144: 604-614.
50. Wudick, M. M., Luu, D.-T., and Maurel, C. (2009). A look inside: Localization patterns and functions of intracellular plant aquaporins. New Phytol. 184: 289-302.
51. Xu, L., Shen, X., Bryan, A., Banga, S., Swanson, M. S., and Luo, Z. Q. (2010). Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog. 6: e1000822.
52. Yang, W. C., Horvath, B., Hontelez, J., Van Kammen, A., and Bisseling, T. (1991). In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization. Mol. Plant Microbe Interact. 4: 464-468.
53. Zouhar, J., and Rojo, E. (2009). Plant vacuoles: Where did they come from and where are they heading? Curr. Opin. Plant Biol. 12: 677-684.