Nuclei in motion: Movement and positioning of plant nuclei in development, signaling, symbiosis, and disease

Frontiers in Plant Science

Volumn 5, Issue APR, 2014, Pages

  Griffis, Anna H N ^a   Groves, Norman R ^a   Zhou, Xiao ^a   Meier, Iris ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Arbuscular mycorrhiza; Cytoskeleton; KASH; Nodulation; Pollen tube; Root hair; SUN; Trichome

Indexed keywords

EID: 84901016345     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00129     Document Type: Review

References (66)

1. Åström, H., Sorri, O., and Raudaskoski, M. (1995). Role of microtubules in the movement of the vegetative nucleus and generative cell in tobacco pollen tubes. Sex. Plant Reprod. 8, 61-69. doi: 10.1007/BF00230890
2. Bakhuizen, R. (1988). The Plant Cytoskeleton in the Rhizobium-Legume Symbiosis. Ph.D. thesis, Leiden University, Leiden.
3. Bibikova, T. N., Blancaflor, E. B., and Gilroy, S. (1999). Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J. 17, 657-665. doi: 10.1046/j.1365-313X.1999.00415.x
4. Blatt, M. R., Weisenseel, M. H., and Haupt, W. (1981). A light-dependent current associated with chloroplast aggregation in the alga Vaucheria sessilis. Planta 152, 513-526. doi: 10.1007/BF00380822
5. Caillaud, M.-C., Piquerez, S. J. M., Fabro, G., Steinbrenner, J., Ishaque, N., Beynon, J., et al. (2012). Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 69, 252-265. doi: 10.1111/j.1365-313X.2011.04787.x
6. Daniel, R., and Guest, D. (2005). Defence responses induced by potassium phosphonate in Phytophthora palmivora-challenged Arabidopsis thaliana. Physiol. Mol. Plant Pathol. 67, 194-201. doi: 10.1016/j.pmpp.2006.01.003
7. Dumas, C., Knox, R. B., and Gaude, T. (1985). The spatial association of the sperm cells and vegetative nucleus in the pollen grain of Brassica. Protoplasma 124, 168-174. doi: 10.1007/BF01290767
8. Fåhraeus, G. (1957). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16, 374-381. doi: 10.1099/00221287-16-2-374
9. Folkers, U., Berger, J., and Hülskamp, M. (1997). Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124, 3779-3786.
10. Freytag, S., Arabatzis, N., Hahlbrock, K., and Schmelzer, E. (1994). Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defense-related gene activation in potato/Phytophthora infestans interactions. Planta 194, 123-135. doi: 10.1007/BF00201043
11. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280-300. doi: 10.1128/mmbr.68.2.280-300.2004
12. Genre, A., Chabaud, M., Faccio, A., Barker, D. G., and Bonfante, P. (2008). Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20, 1407-1420. doi: 10.1105/tpc.108.059014
13. Genre, A., Chabaud, M., Timmers, T., Bonfante, P., and Barker, D. G. (2005). Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489-3499. doi: 10.1105/tpc.105.035410
14. Genre, A., Ortu, G., Bertoldo, C., Martino, E., and Bonfante, P. (2009). Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol. 149, 1424-1434. doi: 10.1104/pp.108.132225
15. Giovannetti, M., Sbrana, C., and Logi, C. (1994). Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol. 127, 703-709. doi: 10.1111/j.1469-8137.1994.tb02973.x
16. Gollotte, A., Gianinazzi-Pearson, V., Giovannetti, M., Sbrana, C., Avio, L., and Gianinazzi, S. (1993). Cellular-localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a locus a Myc-mutant of Pisum sativum L. Planta 191, 112-122. doi: 10.1007/BF00240902
17. Guest, D. I. (1986). Evidence from light microscopy of living tissues that Fosetyl-Al modifies the defence response in tobacco seedlings following inoculation by Phytophthora nicotianae var nicotianae. Physiol. Mol. Plant Pathol. 29, 251-261. doi: 10.1016/S0048-4059(86)80025-X
18. Gundersen, G. G., and Worman, H. J. (2013). Nuclear positioning. Cell 152, 1376-1389. doi: 10.1016/J.Cell.2013.02.031
19. Gus-Mayer, S., Naton, B., Hahlbrock, K., and Schmelzer, E. (1998). Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc. Natl. Acad. Sci. U.S.A. 95, 8398-8403. doi: 10.1073/pnas.95.14.8398
20. Hardham, A. R., Takemoto, D., and White, R. G. (2008). Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol. 8:63. doi: 10.1186/1471-2229-8-63
21. Harrison, M. J. (2012). Cellular programs for arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 15, 691-698. doi: 10.1016/j.pbi.2012.08.010
22. Heath, M. C., Nimichuk, Z. L., and Xu, H. (1997). Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol. 135, 689-700. doi: 10.1046/j.1469-8137.1997.00710.x
23. Heslop-Harrison, J., and Heslop-Harrison, Y. (1989a). Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J. Cell Sci. 94, 319-325.
24. Heslop-Harrison, J., and Heslop-Harrison, Y. (1989b). Conformation and movement of the vegetative nucleus of the angiosperm pollen tube: association with the actin cytoskeleton. J. Cell Sci. 93, 299-308.
25. Heslop-Harrison, J., Heslop-Harrison, Y., Cresti, M., Tiezzi, A., and Moscatelli, A. (1988). Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube. J. Cell Sci. 91, 49-60.
26. Higa, T., Suetsugu, N., and Wada, M. (2013). Plant nuclear photorelocation movement. J. Exp. Bot. doi: 10.1093/jxb/ert414 [Epub ahead of print].
27. Iwabuchi, K., Sakai, T., and Takagi, S. (2007). Blue light-dependent nuclear positioning in Arabidopsis thaliana leaf cells. Plant Cell Physiol. 48, 1291-1298. doi: 10.1093/pcp/pcm095
28. Iwabuchi, K., and Takagi, S. (2010). Actin-based mechanisms for light-dependent intracellular positioning of nuclei and chloroplasts in Arabidopsis. Plant Signal. Behav. 5, 1010-1013. doi: 10.1104/pp.109.149526
29. Kagawa, T., and Wada, M. (1993). Light-dependent nuclear positioning in prothallial cells of Adiantum capillus-veneris. Protoplasma 177, 82-85. doi: 10.1007/BF01403402
30. Kagawa, T., and Wada, M. (1995). Polarized light induces nuclear migration in prothallial cells of Adiantum capillus-veneris L. Planta 196, 775-780. doi: 10.1007/BF01106773
31. Katsuta, J., and Shibaoka, H. (1988). The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol. 29, 403-413.
32. Kaul, V., Theunis, C. H., Palser, B. F., Knox, R. B., and Williams, E. G. (1987). Association of the generative cell and vegetative nucleus in pollen tubes of rhododendron. Ann. Bot. 59, 227-235.
33. Kennard, J. L., and Cleary, A. L. (1997). Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil. Cytoskeleton 36, 55-67. doi: 10.1002/(SICI)1097-0169(1997)36:1< 55::AID-CM5> 3.0.CO;2-G
34. Ketelaar, T., Faivre-Moskalenko, C., Esseling, J. J., De Ruijter, N. C. A., Grierson, C. S., Dogterom, M., et al. (2002). Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14, 2941-2955. doi: 10.1105/tpc.005892
35. Kodama, Y., Tsuboi, H., Kagawa, T., and Wada, M. (2008). Low temperature-induced chloroplast relocation mediated by a blue light receptor, phototropin 2, in fern gametophytes. J. Plant Res. 121, 441-448. doi: 10.1007/S10265-008-0165-9
36. Lawrence, C. J., Morris, N. R., Meagher, R. B., and Dawe, R. K. (2001). Dyneins have run their course in plant lineage. Traffic 2, 362-363. doi: 10.1034/J.1600-0854.2001.25020508.X
37. Lloyd, C. W., Pearce, K. J., Rawlins, D. J., Ridge, R. W., and Shaw, P. J. (1987). Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motil. Cytoskeleton 8, 27-36. doi: 10.1002/cm.970080105
38. Mathur, J., Spielhofer, P., Kost, B., and Chua, N.-H. (1999). The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126, 5559-5568.
39. McCue, A. D., Cresti, M., Feijó, J. A., and Slotkin, R. K. (2011). Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited. J. Exp. Bot. 62, 1621-1631. doi: 10.1093/jxb/err032
40. Miller, D. D., De Ruijter, N. C. A., Bisseling, T., and Emons, A. M. C. (1999). The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J. 17, 141-154. doi: 10.1046/j.1365-313X.1999.00358.x
41. Miller, D. D., Scordilis, S. P., and Hepler, P. K. (1995). Identification and localization of three classes of myosins in pollen tubes of Lilium longiflorum and Nicotiana alata. J. Cell Sci. 108, 2549-2563.
42. Moscatelli, A., Delcasino, C., Lozzi, L., Cai, G., Scali, M., Tiezzi, A., et al. (1995). High-molecular-weight polypeptides related to dynein heavy-chains in Nicotiana tabacum pollen tubes. J. Cell Sci. 108, 1117-1125.
43. Nagai, R. (1993). "Regulation of intracellular movements in plant cells by environmental stimuli, " in International Review of Cytology, eds K. W. Jeon and J. Jarvik. (San Diego, CA: Academic Press), 251-310.
44. Ogasawara, Y., Ishizaki, K., Kohchi, T., and Kodama, Y. (2013). Cold-induced organelle relocation in the liverwort Marchantia polymorpha L. Plant Cell Environ. 36, 1520-1528. doi: 10.1111/Pce.12085
45. Palevitz, B. A. (1993). Relationship between the generative cell and vegetative nucleus in pollen tubes of Nicotiana tabacum. Sex. Plant Reprod. 6, 1-10. doi: 10.1007/BF00227576
46. Qu, L.-H., and Sun, M.-X. (2007). The plant cell nucleus is constantly alert and highly sensitive to repetitive local mechanical stimulations. Plant Cell Rep. 26, 1187-1193. doi: 10.1007/s00299-007-03
47. Qu, L.-H., and Sun, M.-X. (2008a). Cytoplasmic compartmental response to local mechanical stimulation of internal tissue cells. Protoplasma 233, 51-59. doi: 10.1007/s00709-008-0304-0
48. Qu, L.-H., and Sun, M.-X. (2008b). The nucleus as a chief cellular organizer and active defender in response to mechanical stimulation. Plant Signal. Behav. 3, 678-680. doi: 10.4161/psb.3.9.5810
49. Sieberer, B., and Emons, A. M. C. (2000). Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214, 118-127. doi: 10.1007/BF02524268
50. Sieberer, B. J., Timmers, A. C. J., Lhuissier, F. G. P., and Emons, A. M. C. (2002). Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol. 130, 977-988. doi: 10.1104/pp.004267
51. Smith, L. G. (2001). Plant cell division: building walls in the right places. Nat. Rev. Mol. Cell Biol. 2, 33-39. doi: 10.1038/35048050
52. Smith, S. E., and Read, D. J. (2008). Arbuscular Mycorrhizal Symbiosis. London: Academic Press.
53. Starr, D. A., and Fridolfsson, H. N. (2010). Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26, 421-444. doi: 10.1146/annurev-cellbio-100109-104037
54. Takagi, S., Islam, M. S., and Iwabuchi, K. (2011). Dynamic behavior of double-membrane-bounded organelles in plant cells. Int. Rev. Cell Mol. Biol. 286, 181-222. doi: 10.1016/B978-0-12-385859-7.00004-5
55. Tamura, K., Iwabuchi, K., Fukao, Y., Kondo, M., Okamoto, K., Ueda, H., et al. (2013). Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr. Biol. 23, 1-6. doi: 10.1016/j.cub.2013.07.035
56. Tansengco, M. L., Imaizumi-Anraku, H., Yoshikawa, M., Takagi, S., Kawaguchi, M., Hayashi, M., et al. (2004). Pollen development and tube growth are affected in the symbiotic mutant of Lotus japonicus, crinkle. Plant Cell Physiol. 45, 511-520. doi: 10.1093/pcp/pch076
57. Timmers, A. C. J., Auriac, M.-C., and Truchet, G. (1999). Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126, 3617-3628.
58. Tirlapur, U. K., Cai, G., Faleri, C., Moscatelli, A., Scali, M., Del Casino, C., et al. (1995). Confocal imaging and immunogold electron microscopy of changes in distribution of myosin during pollen hydration, germination and pollen tube growth in Nicotiana tabacum L. Eur. J. Cell Biol. 67, 209-217.
59. Tsuboi, H., Suetsugu, N., Kawai-Toyooka, H., and Wada, M. (2007). Phototropins and Neochrome1 Mediate Nuclear Movement in the Fern Adiantum capillus-veneris. Plant Cell Physiol. 48, 892-896. doi: 10.1093/pcp/pcm057
60. van Bruaene, N., Joss, G., and Van Oostveldt, P. (2004). Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol. 136, 3905-3919. doi: 10.1104/pp.103.031591
61. van Brussel, A. A., Bakhuizen, R., Van Spronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J., et al. (1992). Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257, 70-72. doi: 10.2307/2877433
62. Veiga, R. S. L., Faccio, A., Genre, A., Pieterse, C. M. J., Bonfante, P., and Van Der Heijden, M. G. A. (2013). Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ. 36, 1936-1937. doi: 10.1111/pce.12102
63. Weerasinghe, R. R., Bird, D. M., and Allen, N. S. (2005). Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc. Natl. Acad. Sci. U.S.A. 102, 3147-3152. doi: 10.1073/pnas.0407926102
64. Williamson, R. E. (1993). Organelle movements. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 181-202. doi: 10.1146/annurev.pp.44.060193.001145
65. Zhao, Q., Brkljacic, J., and Meier, I. (2008). Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell 20, 1639-1651. doi: 10.1105/tpc.108.059220
66. Zhou, X., Graumann, K., Evans, D. E., and Meier, I. (2012). Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J. Cell Biol. 196, 203-211. doi: 10.1083/jcb.201108098