Release of apical dominance in potato tuber is accompanied by programmed cell death in the apical bud meristem

Plant Physiology

Volumn 158, Issue 4, 2012, Pages 2053-2067

  Teper Bamnolker, Paula ^a   Buskila, Yossi ^a   Lopesco, Yael ^a   Ben Dor, Shifra ^b   Saad, Inbal ^a   Holdengreber, Vered ^a   Belausov, Eduard ^a   Zemach, Hanita ^a   Ori, Naomi ^c   Lers, Amnon ^a   Eshel, Dani ^a  

^a Department of Postharvest Science ^*  (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

SOLANUM TUBEROSUM;

EID: 84859336037     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.194076     Document Type: Article

References (103)

1. Alexopoulos AA, Aivalakis G, Akoumianakis KA, Passam HC (2009) Bromoethane induces dormancy breakage and metabolic changes in tubers derived from true potato seed. Postharvest Biol Technol 54: 165-171
2. Antão CM, Malcata FX (2005) Plant serine proteases: biochemical, physiological and molecular features. Plant Physiol Biochem 43: 637-650
3. Aoyagi S, Sugiyama M, Fukuda H (1998) BEN1 and ZEN1 cDNAs encoding S1-type DNases that are associated with programmed cell death in plants. FEBS Lett 429: 134-138
4. Bajji M, M'Hamdi M, Gastiny F, Rojas-Beltran J, du Jardin P (2007) Catalase inhibition accelerates dormancy release and sprouting in potato (Solanum tuberosum L.) tubers. Biotech Agron Soc Environ 11: 121-131
5. Birch P, Avrova A, Duncan J, Lyon G, Toth R (1999) Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol Plant Microbe Interact 12: 356-361
6. Bonneau L, Ge Y, Drury GE, Gallois P (2008) What happened to plant caspases? J Exp Bot 59: 491-499
7. Bozhkov PV, Filonova LH, Suarez MF (2005) Programmed cell death in plant embryogenesis. Curr Top Dev Biol 67: 135-179
8. Callis J (1995) Regulation of protein degradation. Plant Cell 7: 845-857
9. Campbell M, Segear E, Beers L, Knauber D, Suttle J (2008) Dormancy in potato tuber meristems: chemically induced cessation in dormancy matches the natural process based on transcript profiles. Funct Integr Genomics 8: 317-328
10. Campbell MA, Gleichsner A, Alsbury R, Horvath D, Suttle J (2010) The sprout inhibitors chlorpropham and 1,4-dimethylnaphthalene elicit different transcriptional profiles and do not suppress growth through a prolongation of the dormant state. Plant Mol Biol 73: 181-189
11. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19: 2430-2439
12. Coffeen WC, Wolpert TJ (2004) Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16: 857-873
13. Coleman WK (1984) Large scale application of bromoethane for breaking potato tuber dormancy. Am J Potato Res 61: 587-589
14. Coleman WK (2000) Physiological ageing of potato tubers: a review. Ann Appl Biol 137: 189-199
15. Coupe SA, Watson LM, Ryan DJ, Pinkney TT, Eason JR (2004) Molecular analysis of programmed cell death during senescence in Arabidopsis thaliana and Brassica oleracea: cloning broccoli LSD1, Bax inhibitor and serine palmitoyltransferase homologues. J Exp Bot 55: 59-68
16. Delaplace P, Rojas-Beltran J, Frettinger P, du Jardin P, Fauconnier ML (2008) Oxylipin profile and antioxidant status of potato tubers during extended storage at room temperature. Plant Physiol Biochem 46: 1077-1084
17. DellaMea M, De Filippis F, Genovesi V, Serafini Fracassini D, Del Duca S (2007) The acropetal wave of developmental cell death of tobacco corolla is preceded by activation of transglutaminase in different cell compartments. Plant Physiol 144: 1211-1222
18. Destefano-Beltrán L, Knauber D, Huckle L, Suttle J (2006a) Chemically forced dormancy termination mimics natural dormancy progression in potato tuber meristems by reducing ABA content and modifying expression of genes involved in regulating ABA synthesis and metabolism. J Exp Bot 57: 2879-2886
19. Destefano-Beltrán L, Knauber D, Huckle L, Suttle JC (2006b) Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 61: 687-697
20. Dun EA, Ferguson BJ, Beveridge CA (2006) Apical dominance and shoot branching: divergent opinions or divergent mechanisms? Plant Physiol 142: 812-819
21. Erez A (1987) Chemical control of bud break. Hortic Sci 22: 1240-1243
22. Ewing EE, Simko I, Omer EA, Davies PJ (2004) Polygene mapping as a tool to study the physiology of potato tuberization and dormancy. Am J Potato Res 81: 281-289
23. Faivre-Rampant O, Cardle L, Marshall D, Viola R, Taylor MA (2004) Changes in gene expression during meristem activation processes in Solanum tuberosum with a focus on the regulation of an auxin response factor gene. J Exp Bot 55: 613-622
24. Fauconnier ML, Rojas Beltrán J, Delcarte J, Dejaeghere F, Marlier M, Jardin P (2002) Lipoxygenase pathway and membrane permeability and composition during storage of potato tubers (Solanum tuberosum L. cv Bintje and Desiree) in different conditions. Plant Biol 4: 77-85
25. Fauconnier ML, Welti R, Blée E, Marlier M (2003) Lipid and oxylipin profiles during aging and sprout development in potato tubers (Solanum tuberosum L.). Biochim Biophys Acta 1633: 118-126
26. Filonova LH, Bozhkov PV, Brukhin VB, Daniel G, Zhivotovsky B, von Arnold S (2000) Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J Cell Sci 113: 4399-4411
27. Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5: 379-391
28. Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119: 375-384
29. Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8: 404-408
30. Hartmann A, Senning M, Hedden P, Sonnewald U, Sonnewald S (2011) Reactivation of meristem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol 155: 776-796
31. Hartmans KJ, Van Loon C (1987) Effect of physiological age on growth vigour of seed potatoes of two cultivars. I. Influence of storage period and temperature on sprouting characteristics. Potato Res 30: 397-410
32. Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11: 905-911
33. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305: 855-858
34. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29: 649-659
35. Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21: 2284-2297
36. Ito J, Fukuda H (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14: 3201-3211
37. Ji ZL, Wang SY (1988) Reduction of abscisic acid content and induction of sprouting in potato, Solanum tuberosum L., by thidiazuron. J Plant Growth Regul 7: 37-44
38. Katsuhara M, Shibasaka M (2000) Cell death and growth recovery of barley after transient salt stress. J Plant Res 113: 239-243
39. Kloosterman B, Vorst O, Hall RD, Visser RGF, Bachem CW (2005) Tuber on a chip: differential gene expression during potato tuber development. Plant Biotechnol J 3: 505-519
40. Krijthe N (1962) Observations on the sprouting of seed potatoes. Potato Res 5: 316-333
41. Kumar GNM, Knowles NR (1993a) Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed tubers. Plant Physiol 102: 115-124
42. Kumar GNM, Knowles NR (1993b) Involvement of auxin in the loss of apical dominance and plant growth potential accompanying aging of potato seed tubers. Can J Bot 71: 541-550
43. Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5: 568-573
44. Kuroda H, Maliga P (2003) The plastid clpP1 protease gene is essential for plant development. Nature 425: 86-89
45. Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol 43: 143-151
46. Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I (2005) Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem280: 32914-32920
47. Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5: 305-315
48. Lam E (2008) Programmed cell death in plants: orchestrating an intrinsic suicide program within walls. Crit Rev Plant Sci 27: 413-423
49. Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. Hortic Sci 22: 371-377
50. Law RD, Suttle JC (2003) Transient decreases in methylation at 5#-cCGG-3# sequences in potato (Solanum tuberosum L.) meristem DNA during progression of tubers through dormancy precede the resumption of sprout growth. Plant Mol Biol 51: 437-447
51. Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant Cell Environ 32: 694-703
52. Li J, Wang DY, Li Q, Xu YJ, Cui KM, Zhu YX (2004) PPF1 inhibits programmed cell death in apical meristems of both G2 pea and transgenic Arabidopsis plants possibly by delaying cytosolic Ca2+ elevation. Cell Calcium 35: 71-77
53. Li W, Dickman MB (2004) Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnol Lett 26: 87-95
54. Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16-20
55. Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R, et al (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58: 1035-1045
56. Meijers CP (1972) Effect of carbon-disulphide on the dormancy and sprouting of seed-potatoes. Potato Res 15: 160-165
57. Mino M, Murata N, Date S, Inoue M (2007) Cell death in seedlings of the interspecific hybrid of Nicotiana gossei and N. tabacum: possible role of knob-like bodies formed on tonoplast in vacuolar-collapse-mediated cell death. Plant Cell Rep 26: 407-419
58. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410
59. Mizuno M, Tada Y, Uchii K, Kawakami S, Mayama S (2005) Catalase and alternative oxidase cooperatively regulate programmed cell death induced by beta-glucan elicitor in potato suspension cultures. Planta 220: 849-853
60. Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Ann Bot (Lond) 107: 1203-1212
61. Ophir R, Pang X, Halaly T, Venkateswari J, Lavee S, Galbraith D, Or E (2009) Gene-expression profiling of grape bud response to two alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement. Plant Mol Biol 71: 403-423
62. Piszczek E, Gutman W (2007) Caspase-like proteases and their role in programmed cell death in plants. Acta Physiol Plant 29: 391-398
63. Rappaport L, Lippert LF, Timm H (1957) Sprouting, plant growth, and tuber production as affected by chemical treatment of white potato seed pieces. Am J Potato Res 34: 254-260
64. Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180: 13-26
65. Rehman F, Lee SK, Kim HS, Jeon JH, Park J, Joung H (2001) Dormancy breaking and effects on tuber yield of potato subjected to various chemicals and growth regulators under greenhouse conditions. J Biol Sci 1: 818-820
66. Rentzsch S, Podzimska D, Voegele A, Imbeck M, Müller K, Linkies A, Leubner-Metzger G (2011) Dose-and tissue-specific interaction of monoterpenes with the gibberellin-mediated release of potato tuber bud dormancy, sprout growth and induction of a-amylases and b-amylases. Planta 235: 137-151
67. Ronning CM, Stegalkina SS, Ascenzi RA, Bougri O, Hart AL, Utterbach TR, Vanaken SE, Riedmuller SB, White JA, Cho J, et al (2003) Comparative analyses of potato expressed sequence tag libraries. Plant Physiol 131: 419-429
68. Rotari VI, He R, Gallois P (2005) Death by proteases in plants: whodunit. Physiol Plant 123: 376-385
69. Salimi K, Tavakkol Afshari R, Hosseini MB, Struik PC (2010) Effects of gibberellic acid and carbon disulphide on sprouting of potato minitubers. Sci Hortic (Amsterdam) 124: 14-18
70. Sanmartín M, Jaroszewski L, Raikhel NV, Rojo E (2005) Caspases: regulating death since the origin of life. Plant Physiol 137: 841-847
71. Sasabe M, Takeuchi K, Kamoun S, Ichinose Y, Govers F, Toyoda K, Shiraishi T, Yamada T (2000) Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur J Biochem 267: 5005-5013
72. Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220: 183-197
73. Shi Y (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9: 459-470
74. Simko I, McMurry S, Yang HM, Manschot A, Davies PJ, Ewing EE (1997) Evidence from polygene mapping for a causal relationship between potato tuber dormancy and abscisic acid content. Plant Physiol 115: 1453-1459
75. Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431-444
76. Sonnewald U (2001) Control of potato tuber sprouting. Trends Plant Sci 6: 333-335
77. Sorce C, Lombardi L, Giorgetti L, Parisi B, Ranalli P, Lorenzi R (2009) Indoleacetic acid concentration and metabolism changes during bud development in tubers of two potato (Solanum tuberosum) cultivars. J Plant Physiol 166: 1023-1033
78. Sorce C, Lorenzi R, Ceccarelli N, Ranalli P (2000) Changes in free and conjugated IAA during dormancy and sprouting of potato tubers. Funct Plant Biol 27: 371-377
79. Struik PC, Wiersema SG (1999) Seed Potato Technology. CSIRO, Wageningen, The Netherlands
80. Sukhova LS, Macháčková I, Eder J, Bibik ND, Korableva NP (1993) Changes in the levels of free IAA and cytokinins in potato tubers during dormancy and sprouting. Biol Plant 35: 387-391
81. Suttle JC (1998) Involvement of ethylene in potato microtuber dormancy. Plant Physiol 118: 843-848
82. Suttle JC (2004a) Involvement of endogenous gibberellins in potato tuber dormancy and early sprout growth: a critical assessment. J Plant Physiol 161: 157-164
83. Suttle JC (2004b) Physiological regulation of potato tuber dormancy. Am J Potato Res 81: 253-262
84. Suttle JC (2009) Ethylene is not involved in hormone-and bromoethaneinduced dormancy break in Russet Burbank minitubers. Am J Potato Res 86: 278-285
85. Suttle JC, Hultstrand JF (1994) Role of endogenous abscisic acid in potato microtuber dormancy. Plant Physiol 105: 891-896
86. Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C, Machida Y (2001) A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 128: 4681-4689
87. Teper-Bamnolker P, Dudai N, Fischer R, Belausov E, Zemach H, Shoseyov O, Eshel D (2010) Mint essential oil can induce or inhibit potato sprouting by differential alteration of apical meristem. Planta 232: 179-186
88. Turk B, Stoka V (2007) Protease signalling in cell death: caspases versus cysteine cathepsins. FEBS Lett 581: 2761-2767
89. Turnbull CGN, Hanke DE (1985) The control of bud dormancy in potato tubers. Planta 165: 359-365
90. Turner S, Gallois P, Brown D (2007) Tracheary element differentiation. Annu Rev Plant Biol 58: 407-433
91. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141: 384-390
92. van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trends Plant Sci 10: 117-122
93. VercammenD, van de Cotte B, De JaegerG, Eeckhout D, Casteels P, Vandepoele K, Vandenberghe I, Van Beeumen J, Inzé D, Van Breusegem F (2004) Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 279: 45329-45336
94. Wagner D, Przybyla D, Opden Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, et al (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306: 1183-1185
95. Watanabe N, Lam E (2004) Recent advance in the study of caspase-like proteases and Bax inhibitor-1 in plants: their possible roles as regulator of programmed cell death. Mol Plant Pathol 5: 65-70
96. Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45: 884-894
97. Williams B, Dickman M (2008) Plant programmed cell death: can't live with it, can't live without it. Mol Plant Pathol 9: 531-544
98. Wiltshire JJJ, Cobb AH (1996) A review of the physiology of potato tuber dormancy. Ann Appl Biol 129: 553-569
99. Woltering EJ (2010) Death proteases: alive and kicking. Trends Plant Sci 15: 185-188
100. Woltering EJ, van der Bent A, Hoeberichts FA (2002) Do plant caspases exist? Plant Physiol 130: 1764-1769
101. Yano A, Suzuki K, Shinshi H (1999) A signaling pathway, independent of the oxidative burst, that leads to hypersensitive cell death in cultured tobacco cells includes a serine protease. Plant J 18: 105-109
102. Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18: 397-411
103. Zhang H, Dong S, Wang M, Wang W, Song W, Dou X, Zheng X, Zhang Z (2010) The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. J Exp Bot 61: 3799-3812