Disorganization of F-actin cytoskeleton precedes vacuolar disruption in pollen tubes during the in vivo self-incompatibility response in Nicotiana alata

Annals of Botany

Volumn 110, Issue 4, 2012, Pages 787-795

  Roldán, Juan A ^a   Rojas, Hernán J ^a   Goldraij, Ariel ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Confocal microscopy; F actin cytoskeleton; Nicotiana alata; pollen tube; S RNase; self incompatibility; vacuolar system

Indexed keywords

ACTIN; RIBONUCLEASE; RIBONUCLEASE S; VEGETABLE PROTEIN;

INHIBITION; MEMBRANE; POLLEN; POLLINATION; SELF INCOMPATIBILITY; TOBACCO;

ACTIN FILAMENT; ARTICLE; CELL VACUOLE; CONFOCAL MICROSCOPY; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; POLLEN TUBE; POLLINATION; SELF-INCOMPATIBILITY (PLANT); TOBACCO; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ACTINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PLANT PROTEINS; POLLEN TUBE; POLLINATION; RIBONUCLEASES; SELF-INCOMPATIBILITY IN FLOWERING PLANTS; TOBACCO; VACUOLES;

NICOTIANA; NICOTIANA ALATA;

EID: 84865458285     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcS153     Document Type: Article

References (55)

1. Bosch M, Franklin-Tong VE. 2007. Temporal and spatial activation of a caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proceedings of the National Academy of Sciences of the USA 104: 18327-18332.
2. Cai G, Cresti M. 2009. Organelle motility of pollen tube: a tale of 20 years. Journal of Experimental Botany 60: 495-508.
3. Chen CY, Wong EI, Vidali L, et al. 2002. The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. The Plant Cell 14: 2175-2190.
4. Chen T, Teng N, Wu X, et al. 2007. Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiology 48: 19-30.
5. Chen G, Zhang B, Zhao Z, Sui Z, Zhang H, Xue Y. 2010. 'A life or death decision' for pollen tubes in S-RNase-based self-incompatibility. Journal of Experimental Botany 61: 2027-2037.
6. Cheung AY, Wu HM. 2008. Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annual Review of Plant Biology 59: 547-572.
7. Cheung AY, Duan Qh, Santos Costa S, et al. 2008. The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubulebinding reporter proteins. Molecular Plant 1: 686-702.
8. Doris FP, Steer MW. 1996. Effects of fixatives and permeabilisation buffers on pollen tubes: implications for localisation of actin microfilaments using phalloidin staining. Protoplasma 195: 25-36.
9. Franklin-Tong VE. 2008. Self-incompatibility in Papaver rhoeas: progress in understanding mechanisms involved in regulating self-incompatibility in Papaver. In: Franklin-Tong VE. ed. Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Berlin: Springer, 237-258.
10. Franklin-Tong VE, Gourlay CW. 2008. A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochemical Journal 413: 389-404.
11. Geitmann A, Hudák J, Vennigerholz F, Walles B. 1995. Immunogold localization of pectine and callose in pollen grains and pollen tubes of Brugmansia suaveolens: implications for the self-incompatibility reaction. Journal of Plant Physiology 147: 225-235.
12. Geitmann A. 1999. Cell death of self-incompatible pollen tubes: necrosis or apoptosis? In: Cresti M, Cai G, Moscatelli A eds. Fertilization in higher plants: molecular and cytological aspects. Berlin: Springer, 113-137.
13. Geitmann A, Snowman BN, Emons AMC, Franklin-Tong VE. 2000. Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. The Plant Cell 12: 1239-1251.
14. Geitmann A, Franklin-Tong VE, Emons AC. 2004. The self-incompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death and Differentiation 11: 812-822.
15. Gibbon BC, Kovar DR, Staiger CJ. 1999. Latrunculin B has different effects on pollen germination and tube growth. The Plant Cell 11: 2349-2364.
16. Goldraij A, Kondo K, Lee CB, et al. 2006. Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439: 805-810.
17. Good-Avila SV, Mena-Aĺ JI, Stephenson AG. 2008. Genetic and environmental causes and evolutionary consequences of variations in self-fertility in self-incompatible species. In: Franklin-Tong VE. ed. Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Berlin: Springer, 33-51.
18. de Graaf BHJ, Lee C, McClure BA, Franklin-Tong VE. 2006. Cellular mechanisms for pollen tube growth inhibition in gametophytic selfincompatibility. In: Malhó R. ed. The pollen tube. Berlin: Springer, 201-221.
19. Hara-Nishimura I, Hatsugai N. 2011. The role of vacuole in plant cell death. Cell Death and Differentiation 18: 1298-1304.
20. Hicks GR, Rojo E, Hong S, Carter DC, Raikhel NV. 2004. Germinating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiology 134: 1227-1230.
21. Hiratsuka S, Zhang SL, Nakagawa E, Kawai Y. 2001. Selective inhibition of the growth of incompatible pollen tubes by S-protein in the Japanese pear. Sexual Plant Reproduction 13: 209-215.
22. Hua Z, Fields A, Kao T-h. 2008. Biochemical models for S-RNase-based self-incompatibility. Molecular Plant 1: 575-585.
23. Huang S, Lee HS, Karunandaa B, Kao T-h. 1994. Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. The Plant Cell 6: 1021-1028.
24. Jauh GY, Lord EM. 1995. Movement of the tube cell in the lily style in the absence of the pollen grain and the spent pollen tube. Sexual Plant Reproduction 8: 168-172.
25. Kho YO, Baer J. 1968. Observing pollen tubes by means of fluorescence. Euphytica 17: 299-302.
26. Liu Zq, Xu Gh, Zhang Sl. 2007. Pyrus pyrifolia stylar S-RNase induces alterations in the actin cytoskeleton in self-pollen and tubes in vitro. Protoplasma 232: 61-67.
27. Luhtala N, Parker R. 2010. T2 family ribonucleases: ancient enzymes with diverse roles. Trends in Biochemical Sciences 35: 253-259.
28. LushMW, Clarke AE. 1997. Observations of pollen tube growth in Nicotiana alata and their implications for the mechanism of self-incompatibility. Sexual Plant Reproduction 10: 27-35.
29. McClure BA, Gray JE, Anderson MA, Clarke AE. 1990. Selfincompatibility in Nicotiana alata involves degradation of rRNA. Nature 347: 757-760.
30. McClure BA, Cruz-Garća F, Romero C. 2011. Compatibility and incompatibility in S-RNase-based systems. Annals of Botany 108: 647-658.
31. Meng XY, Hua ZH,Wang N, Fields AM, Dowd PE, Kao T-h. 2009. Ectopic expression of S-RNase of Petunia inflata in pollen results in its sequestration and non-cytotoxic function. Sexual Plant Reproduction 22: 263-275.
32. Meng XY, Sun P, Kao T-H. 2010. S-RNase-based self-incompatibility in Petunia. Annals of Botany 108: 637-646.
33. de Nettancourt D, Devreux M, Bozzini A, Cresti M, Pacini E, Sarfatti G. 1973. Ultrastructural aspects of the self-incompatibility mechanism in Lycopersicum peruvianum Mill. Journal of Cell Science 12: 403-419.
34. Pandey KK. 1979. The genus Nicotiana: evolution of incompatibility in flowering plants. In: Hawkes JG, Lester RN, Skelding AD. eds. The biology and taxonomy of the Solanaceae. London: Academic Press, 421-434.
35. Poulter NS, Staiger CJ, Rappoport JZ, Franklin-Tong VE. 2010. Actin-binding proteins implicated in the formation of the punctate actin foci stimulated by the self-incompatibility response in Papaver. Plant Physiology 152: 1274-1283.
36. Poulter NS, Bosch M, Franklin-Tong VE. 2011. Proteins implicated in mediating self-incomaptibility-induced alterations to the actin cytoskeleton of Papaver pollen. Annals of Botany 108: 659-675.
37. Rea AC, Nasrallah JB. 2008. Self-incompatibility systems: barriers to selffertilization in flowering plants. International Journal of Developmental Biology 52: 627-636.
38. Roiz L, Smirnoff P, Bar-Eli M, Schwartz B, Shoseyov O. 2006. ACTIBIND, an actin-binding fungal T2-RNase with antiangiogenic and anticarcinogenic characteristics. Cancer 106: 2295-2308.
39. Roldán JA, Quiroga R, Goldraij A. 2010. Molecular and genetic characterization of novel S-RNases from a natural population of Nicotiana alata. Plant Cell Reports 29: 735-746.
40. Smertenko A, Franklin-Tong VE. 2011. Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death and Differentiation 18: 1263-1270.
41. Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ. 2002. Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. The Plant Cell 14: 2613-2626.
42. Staiger CJ. 2000. Signaling to the actin cytoskeleton in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51: 257-288.
43. Staiger CJ, Yuan M, Valenta R, Shaw PJ, Warn RM, Lloyd CW. 1994. Microinjected profilin affects cytoplasmic streaming in plant cells by rapidly depolymerizing actin microfilaments. Current Biology 4: 215-219.
44. Staiger CJ, Poulter NS, Henty JL, Franklin-Tong VE, Blanchoin L. 2010. Regulation of actin dynamics by actin-binding proteins in pollen. Journal of Experimental Botany 61: 1969-1986.
45. Thomas SG, Huang S, Li S, Satiger CJ, Franklin-Tong VE. 2006. Actin depolymerization is sufficient to induce programmed cell death in selfincompatible pollen. Journal of Cell Biology 174: 221-229.
46. Thompson DM, Parker R. 2009. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. Journal of Cell Biology 185: 43-50.
47. Vidali L, McKenna ST, Hepler PK. 2001. Actin polymerization is essential for pollen tube growth. Molecular Biology of the Cell 12: 2534-2545.
48. Wang CL, Zhang SL. 2011. A cascade signal pathway occurs in selfincompatibility of Pyrus pyrifolia. Plant Signaling & Behavior 6: 420-421.
49. Wang CL, Xu GH, Jiang XT, et al. 2009. S-RNase triggers mitochondrial alteration and DNA degradation in the incompatible pollen tube of Pyrus pyrifolia in vitro The Plant Journal 57: 220-229.
50. Wang CL, Wu J, Xu GH, et al. 2010. S-RNase disrupts tip-localized reactive oxygen species and induces nuclear DNA degradation in incompatible pollen tubes of Pyrus pyrifolia. Journal of Cell Science 123: 4301-4309.
51. Wang HY, Xue YB. 2005. Subcellular localization of the S locus F-box protein AhSLF-S2 in pollen and pollen tubes of self-incompatible Antirrhinum. Journal of Integrative Plant Biology 47: 76-83.
52. Wilkins KA, Bancroft J, Bosch M, Ings J, Smirnoff N, Franklin-Tong VE. 2011. Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the self-incompatibility response of Papaver. Plant Physiology 156: 404-416.
53. Wilsen KL, Lovy-Wheeler A, Voigt B, Menzel D, Kunkel JG, Hepler PK. 2006. Imaging the actin cytoskeleton in growing pollen tubes. Sexual Plant Reproduction 19: 51-62.
54. Zhang Y, Zhao Z, Xue Y. 2009. Roles of proteolysis in plant selfincompatibility. Annual Review of Plant Biology 60: 21-42.
55. Zhang Y, He J, Lee D, McCormick S. 2010. Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. Plant Physiology 152: 2200-2210.