Taking one for the team: Self-recognition and cell suicide in pollen

Journal of Experimental Botany

Volumn 65, Issue 5, 2014, Pages 1331-1342

  Wilkins, Katie A ^a,b   Poulter, Natalie S ^a   Franklin Tong, Vernonica E ^c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Centre for Cardiovascular Sciences Medical School University of Birmingham ^*

Author keywords

Actin cytoskeleton; Caspase; Nitric oxide (NO); Oxidative stress; Papaver rhoeas; Pollen; Programmed cell death (PCD); Reactive oxygen species (ROS); Self incompatibility (SI)

Indexed keywords

CASPASE; VEGETABLE PROTEIN;

ACTIN FILAMENT; APOPTOSIS; ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NITRIC OXIDE (NO); OXIDATIVE STRESS; PAPAVER; PAPAVER RHOEAS; PHYSIOLOGY; POLLEN; PROGRAMMED CELL DEATH (PCD); REACTIVE OXYGEN SPECIES (ROS); REVIEW; SELF-INCOMPATIBILITY (PLANT); SELF-INCOMPATIBILITY (SI).; SIGNAL TRANSDUCTION;

ACTIN CYTOSKELETON; CASPASE; NITRIC OXIDE (NO); OXIDATIVE STRESS; PAPAVER RHOEAS; POLLEN; PROGRAMMED CELL DEATH (PCD); REACTIVE OXYGEN SPECIES (ROS); SELF-INCOMPATIBILITY (SI).;

APOPTOSIS; ARABIDOPSIS; GENE EXPRESSION REGULATION; PAPAVER; PLANT PROTEINS; POLLEN; SELF-INCOMPATIBILITY IN FLOWERING PLANTS; SIGNAL TRANSDUCTION;

EID: 84897410944     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert468     Document Type: Review

References (69)

1. Allen AM, Hiscock SJ. 2008. Evolution and phylogeny of selfincompatibility systems in angiosperms. In: Franklin-Tong VE, editor, Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Berlin, Heidelberg: Springer-Verlag, pp 73-101.
2. Allwood EG. 2002. Regulation of the pollen-specific actindepolymerizing factor LlADF1. The Plant Cell 14, 2915-2927.
3. Asai S, Ohta K, Yoshioka H. 2008. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. The Plant Cell 20, 1390-1406.
4. Bamburg JR, McGough A, Ono S. 1999. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends in Cell Biology 9, 364-370.
5. Baxter A, Mittler R, Suzuki N. 2014. ROS as key players in plant stress signalling. Journal of Experimental Botany 65, 1229-1240.
6. Bell CD, Soltis DE, Soltis PS. 2010. The age and diversification of the angiosperms re-revisited. American Journal of Botany 97, 1296-1303.
7. Bonneau L, Ge Y, Drury GE, Gallois P. 2008. What happened to plant caspases? Journal of Experimental Botany 59, 491-499.
8. Bosch M, Franklin-Tong VE. 2007. Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proceedings of the National Academy of Sciences, USA 104, 18327-18332.
9. Bosch M, Poulter NS, Perry RM, Wilkins KA, Franklin-Tong VE. 2010. Characterization of a legumain/vacuolar processing enzyme and YVADase activity in Papaver pollen. Plant Molecular Biology 74, 381-393.
10. Bosch M, Poulter NS, Vatovec S, Franklin-Tong VE. 2008. Initiation of programmed cell death in self-incompatibility: role for cytoskeleton modifications and several caspase-like activities. Molecular Plant 1, 879-887.
11. Cárdenas L, Martínez A, Sánchez F, Quinto C. 2008. Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). The Plant Journal 56, 802-813.
12. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D. 1997. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: Implication in actin-based motility. Journal of Cell Biology 136, 1307-1322.
13. Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP, Kalinina NO, Taliansky ME, Vartapetian AB. 2004. A plant caspase-like protease activated during the hypersensitive response. The Plant Cell 16, 157-171.
14. Colcombet J, Hirt H. 2008. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. The Biochemical Journal 413, 217-226.
15. Dalle-Donne I, Milzani A, Giustarini D, Simplicio PD, Colombo R, Rossi R. 2000. S-NO-actin: S-nitrosylation kinetics and the effect on isolated vascular smooth muscle. Journal of Muscle Research and Cell Motility 21, 171-181.
16. de Graaf BH, Rudd JJ, Wheeler MJ, Perry RM, Bell EM, Osman K, Franklin FCH, Franklin-Tong VE. 2006. Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen. Nature 444, 490-493.
17. de Graaf BH, Vatovec S, Juárez-Díaz JA, Chai L, Kooblall K, Wilkins KA, Zou H, Forbes T, Franklin FC, Franklin-Tong VE. 2012. The Papaver self-incompatibility pollen S-determinant, PrpS, functions in Arabidopsis thaliana. Current Biology 22, 154-159.
18. +-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany 65, 1259-1270.
19. Foote HCC, Ride JP, Franklintong VE, Walker EA, Lawrence MJ, Franklin FCH. 1994. Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas L. Proceedings of the National Academy of Sciences, USA 91, 2265-2269.
20. Foyer CH, Noctor G. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866-1875.
21. Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FCH. 1993. The Self-Incompatibility Response in Papaver rhoeas Is Mediated by Cytosolic-Free Calcium. Plant Journal 4, 163-177.
22. Franklin-Tong VE, Gourlay CW. 2008. A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. The Biochemical Journal 413, 389.
23. Franklin-Tong VE, Hackett G, Hepler PK. 1997. Ratio-imaging of Ca-i(2+) in the self-incompatibility response in pollen tubes of Papaver rhoeas. The Plant Journal 12, 1375-1386.
24. Franklin-Tong VE, Lawrence MJ, Franklin FCH. 1988. An in vitro bioassay for the stigmatic product of the self-incompatibility gene in Papaver rhoeas L. New Phytologist 110, 109-118.
25. 2+ transient in pollen of Papaver rhoeas. The Plant Journal 8, 299-307.
26. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C. 2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28, 1091-1101.
27. Geitmann A, Franklin-Tong VE, Emons AC. 2004. The selfincompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death and Differentiation 11, 812-822.
28. 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.
29. Gibbon BC, Kovar DR, Staiger CJ. 1999. Latrunculin B has different effects on pollen germination and tube growth. The Plant Cell 11, 2349-2363.
30. Hatsugai N. 2004. A plant vacuolar protease, VPE, mediates virusinduced hypersensitive cell death. Science 305, 855-858.
31. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I. 2009. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes and Development 23, 2496-2506.
32. Hodgkin T, Lyon GD, Dickinson HG. 1988. Recognition in flowering plants: a comparison of the Brassica self-incompatibility system and plant pathogen interactions. New Phytologist 110, 557-569.
33. Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ. 2004. A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. Journal of Biological Chemistry 279, 23364-23375.
34. Jordan ND, Franklin FCH, Franklin-Tong VE. 2000. Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas. The Plant Journal 23, 471-479.
35. Kornberg A. 1962. On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions . New York: Academic Press.
36. Laloi C, Apel K, Danon A. 2004. Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7, 323-328.
37. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. The Plant Cell 14, 2627-2641.
38. Levine A, Pennell RI, Alverez ME, Palme R, Lamb C. 1997. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology 6, 427-437.
39. Li S, Samaj J, Franklin-Tong VE. 2007. A mitogen-activated protein kinase signals to programmed cell death induced by selfincompatibility in Papaver pollen. Plant Physiology 145, 236-245.
40. Lindermayr C, Saalbach G, Durner J. 2005. Proteomic identification of S-Nitrosylated proteins in Arabidopsis. Plant Physiology 137, 921-930.
41. Lozano-Juste J, Colom-Moreno R, León J. 2011. In vivo protein tyrosine nitration in Arabidopsis thaliana. Journal of Experimental Botany 62, 3501-3517.
42. Meng X, Zhang S. 2013. MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology 51, 245-266.
43. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. 2011. ROS signaling: the new wave? Trends in Plant Science 16, 300-309.
44. Moreau M, Lindermayr C, Durner J, Klessig DF. 2010. NO synthesis and signaling in plants - where do we stand? Physiologia Plantarum 138, 372-383.
45. Parrish AB, Freel CD, Kornbluth S. 2013. Cellular mechanisms controlling caspase activation and function. Cold Spring Harbor Perspectives in Biology 5, pii: a008672.
46. Passaia G, Queval G, Bai J, Margis-Pinheiro M, Foyer CH. 2014. The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. Journal of Experimental Botany 65, 1403-1413.
47. 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.
48. Poulter NS, Vatovec S, Franklin-Tong VE. 2008. Microtubules are a target for self-incompatibility signaling in Papaver pollen. Plant Physiology 146, 1358-1367.
49. Rentel MC, Lecourieux D, Ouaked F, et al. 2004. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858-861.
50. γ exhibits a caspase-like activity that contributes to defense against pathogens. Current Biology 14, 1897-1906.
51. Rudd JJ, Franklin F, Lord JM, Franklin-Tong VE. 1996. Increased phosphorylation of a 26-kD pollen protein is induced by the selfincompatibility response in Papaver rhoeas. The Plant Cell 8, 713-724.
52. Rudd JJ, Osman K, Franklin FCH, Franklin-Tong VE. 2003. Activation of a putative MAP kinase in pollen is stimulated by the selfincompatibility (SI) response. FEBS Letters 547, 223-227.
53. Sanabria N, Goring D, Nürnberger T, Dubery I. 2008. Self/nonself perception and recognition mechanisms in plants: a comparison of selfincompatibility and innate immunity. New Phytologist 178, 503-514.
54. Sawada H, Inoue N, Iwano ME. 2014. Sexual reproduction in animals and plants . Tokyo: Springer Japan.
55. Sheng X, Hu Z, Lu H, Wang X, Baluska F, Samaj J, Lin J. 2006. Roles of the ubiquitin/proteasome pathway in pollen tube growth with emphasis on MG132-induced alterations in ultrastructure, cytoskeleton, and cell wall components. Plant Physiology 141, 1578-1590.
56. Smertenko A, Franklin-Tong VE. 2011. Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death and Differentiation 18, 1263-1270.
57. 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.
58. Staiger CJ. 2000. Signalling to the actin cytoskeleton in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51, 257-288.
59. 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.
60. Thomas SG, Franklin-Tong VE. 2004. Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305-309.
61. Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE. 2006. Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. Journal of Cell Biology 174, 221-229.
62. Torres MA, Jones JD, Dangl JL. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 37, 1130-1134.
63. Torres MA, Jones JD, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373-378.
64. van Doorn WG, Beers EP, Dangl JL, et al. 2011. Morphological classification of plant cell deaths. Cell Death and Differentiation 18, 1241-1246.
65. Wang Y, Yun B-W, Kwon E, Hong JK, Yoon J, Loake GJ. 2006. S-Nitrosylation: an emerging redox-based post-translational modification in plants. Journal of Experimental Botany 57, 1777-1784.
66. Wheeler MJ, de Graaf BH, Hadjiosif N, Perry RM, Poulter NS, Osman K, Vatovec S, Harper A, Franklin FC, Franklin-Tong VE. 2009. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459, 992-995.
67. 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 selfincompatibility response of Papaver. Plant Physiology 156, 404-416.
68. +. Plant Physiology 155, 963-973.
69. Young B, Wightman R, Blanvillain R, Purcel S, Gallois P. 2010. pH-sensitivity of YFP provides an intracellular indicator of programmed cell death. Plant Methods 6, 27.