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Role of cAMP in Gibberellin Promotion of Seed Germination in Orobanche minor Smith

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Abstract

Adenosine 3′,5′-cyclic monophosphate (cAMP) is known as a key second messenger in many living organisms, regulating a wide range of cellular responses. In higher plants the function of cAMP is poorly understood. In this study, we examined the role of cAMP in seed germination of the root parasitic plant Orobanche minor whose seeds require preincubation in warm moist environments for several days, termed conditioning, prior to exposure to germination stimulants released from roots of host plants. Accumulation of endogenous cAMP was observed in the conditioned O. minor seeds. When the seeds were exposed to light or supraoptimal temperature during the conditioning period, cAMP did not accumulate and the seeds showed low germination rates after stimulation with strigol, a germination stimulant. Addition of membrane-permeable cAMP to the medium restored the germination rates of the seeds treated with light or supraoptimal temperature during the conditioning period, suggesting that cAMP functions during the conditioning period. The endogenous cAMP levels of the seeds conditioned in the light or at a supraoptimal temperature were elevated by treatment of the seeds with gibberellin (GA) during the conditioning period. Uniconazole, a potent inhibitor of GA biosynthesis, blocked elevation of the cAMP level. Furthermore, a correlation between the endogenous cAMP level and GA level was observed during the conditioning period. These results suggest that GAs elevate the cAMP level, which is required for the germination of O. minor seeds.

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References

  • Arazi T, Sunkar R, Kaplan B, Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J 20:171–182

    Article  PubMed  CAS  Google Scholar 

  • Balague C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379

    Article  PubMed  CAS  Google Scholar 

  • Bindschedler LV, Minibayeva F, Gardner SL, Gerrish C, Davies DR, Bolwell GP (2001) Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+. New Phytol 151:185–194

    Article  CAS  Google Scholar 

  • Brooks DW, Bevinakatti HS, Kennedy E, Hathaway J (1985) Practical total synthesis of (±)-strigol. J Org Chem 50:628–638

    Article  CAS  Google Scholar 

  • Brown EG, Newton RP (1992) Analytical procedures for cyclic nucleotides and their associated enzymes in plant tissues. Phytochem Anal 3:1–13

    Article  CAS  Google Scholar 

  • Carricarte VC, Bianchini GM, Muschietti JP, Tellez-Inon MT, Perticari A, Torres N, Flawia MM (1988) Adenylate cyclase activity in a higher plant, alfalfa (Medicago sativa). Biochem J 249:807–811

    PubMed  CAS  Google Scholar 

  • Chae SH, Yomeyama K, Takeuchi Y, Joel DM (2003) Fluridone and norflurazon, carotenoid-biosynthesis inhibitors, promote seed conditioning and germination of the holoparasite Orobanche minor. Physiol Plant 120:1–10

    Google Scholar 

  • Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97:9323–9328

    Article  PubMed  CAS  Google Scholar 

  • Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190

    Article  PubMed  CAS  Google Scholar 

  • Cooke CJ, Newton RP, Smith CJ, Walton TJ (1989) Pathogenic elicitation of phytoalexin in lucerne tissues; involvement of cyclic AMP in intracellular mechanisms. Biochem Soc Trans 17:915–916

    CAS  Google Scholar 

  • Cooke CJ, Smith CJ, Walton TJ, Newton RP (1994) Evidence that cyclic AMP is involved in the hypersensitive response of Medicago sativa to a fungal elicitor. Phytochemistry 35:889–895

    Article  CAS  Google Scholar 

  • Dailey OD Jr (1987) A new synthetic route to (±)-strigol. J Org Chem 52:1984–1989

    Article  CAS  Google Scholar 

  • Duffus CM, Duffus JH (1969) A possible role for cyclic AMP in gibberellic acid triggered release of alpha-amylase in barley endosperm slices. Experientia 25:581

    Article  PubMed  CAS  Google Scholar 

  • Ehsan H, Reichheld JP, Roef L, Witters E, Lardon F, Van Bockstaele D, Van Montagu M, Inze D, Van Onckelen H (1998) Effect of indomethacin on cell cycle dependent cyclic AMP fluxes in tobacco BY-2 cells. FEBS Lett 422:165–169

    Article  PubMed  CAS  Google Scholar 

  • Estabrook EM, Yoder JI (1998) Plant-plant communications: Rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7

    Article  CAS  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  PubMed  CAS  Google Scholar 

  • Foy CL, Jain R, Jacobsohn R (1989) Recent approaches for chemical control of broomrape (Orobanche spp.). Rev Weed Sci 4:123–152

    CAS  Google Scholar 

  • Galsky AG, Lippincott JA (1969) Promotion and inhibition of α-amylase production in barley endosperm by cyclic 3′, 5′-adenosine monophosphate and adenosine diphosphate. Plant Cell Physiol 10:607–620

    CAS  Google Scholar 

  • Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJ (2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot 57:791–800

    Article  PubMed  CAS  Google Scholar 

  • Gomi K, Matsuoka M (2003) Gibberellin signalling pathway. Curr Opin Plant Biol 6:489–493

    Article  PubMed  CAS  Google Scholar 

  • Hall KA, Galsky AG (1973) The action of cyclic-AMP on GA3 controlled responses IV. Characteristics of the promotion of seed germination in Lactuca sative variety ‘Spartan Lake’ by gibberellic acid and cyclic 3′, 5′-adenosine monophosphate. Plant Cell Phisiol 14:565–571

    CAS  Google Scholar 

  • Hauck C, Müller S, Schildknecht H (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J Plant Physiol 139:474–478

    CAS  Google Scholar 

  • Holms RE, Miller MR (1972) Hormonal control of weed seed germination. Weed Sci 20:209–211

    Google Scholar 

  • Joel DM, Back A, Kleifeld Y, Gepstein S (1989) Seed conditioning and its role in Orobanche seed germination: inhibition by paclobutrazol. In: Wegmann K, Musselman LJ (eds), Progress in Orobanche Research. Proceedings of the 1989 International Workshop on Orobanche Research. Eberhard-Karls-University, Tubingen, FRG, pp 147–156

  • Kamisaka S, Masuda Y (1971) Stimulation of gibberellin-induced germination in lettuce seeds by cyclic 3′, 5′-adenosine monophosphate. Plant Cell Physiol 12:1003–1005

    CAS  Google Scholar 

  • Kurosaki F, Nishi A (1993) Stimulation of calcium influx and calcium cascade by cyclic AMP in cultured carrot cells. Arch Biochem Biophys 302:144–151

    Article  PubMed  CAS  Google Scholar 

  • Kurosaki F, Tsurusawa Y, Nishi A (1987) The elicitation of phytoalexins by Ca2+ and cyclic AMP in cultured carrot cells. Phytochemistry 26:1919–1923

    Article  CAS  Google Scholar 

  • Lusini P, Trabalzini L, Franchi GG, Bovalini L, Martelli P (1991) Adenylate cyclase in roots of Ricinus communis stimulation by GTP and manganese. Phytochemistry 30:109–110

    Article  CAS  Google Scholar 

  • Moutinho A, Hussey PJ, Trewavas AJ, Malho R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci U S A 98:10481–10486

    Article  PubMed  CAS  Google Scholar 

  • Müller S, Hauck C, Schildknecht H (1992) Germination stimulants produced by Vigna unguiculata Walp cv Saunders Upright. J Plant Growth Regul 11:77–84

    Article  Google Scholar 

  • Nakajima M, Yamaguchi I, Kizawa S, Murofushi N, Takahashi N (1991) Preparation and validation of an antiserum specific for non-derivatized gibberellins. Plant Cell Physiol 32:505–510

    CAS  Google Scholar 

  • Newton RP, Smith CJ (2004) Cyclic nucleotides. Phytochemistry 65:2423–2437

    Article  PubMed  CAS  Google Scholar 

  • Newton RP, Roef L, Witters E, Van Onckelen H (1999) Cyclic nucleotides in higher plants: the enduring paradox. New Phytol 143:427–455

    Article  CAS  Google Scholar 

  • Nun NB, Mayer AM (1993) Preconditioning and germination of Orobanche seeds: respiration and protein synthesis. Phytochemistry 34:39–45

    Article  CAS  Google Scholar 

  • Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14 Suppl:S61–80

    PubMed  CAS  Google Scholar 

  • Pacini B, Petrigliano A, Diffley P, Paffetti A, Brown EG, Martelli P, Trabalzini L, Bovalini L, Lusini P, Newton RP (1993) Adenyl cyclase activity in roots of Pisum sativum. Phytochemistry 34:899–903

    Article  CAS  Google Scholar 

  • Peng J, Harberd NP (2002) The role of GA-mediated signalling in the control of seed germination. Curr Opin Plant Biol 5:376–381

    Article  PubMed  CAS  Google Scholar 

  • Richards H, Das S, Smith CJ, Pereira L, Geisbrecht A, Devitt NJ, Games DE, van Geyschem J, Gareth Brenton A, Newton RP (2002) Cyclic nucleotide content of tobacco BY-2 cells. Phytochemistry 61:531–537

    Article  PubMed  CAS  Google Scholar 

  • Sato S, Tabata S, Hotta Y (1992) Changes in intracellular cAMP level and activities of adenylcyclase and phosphodiesterase during meiosis of lily microsporocytes. Cell Struct Funct 17:335–339

    Article  PubMed  CAS  Google Scholar 

  • Siame BA, Weerasuriya Y, Wood K, Ejeta G, Butler LG (1993) Isolation of strigol, a germination stimulant for Striga asiatica, from natural host plants. J Agric Food Chem 41:1486–1491

    Article  CAS  Google Scholar 

  • Song WJ, Zhou WJ, Jin ZL, Cao DD, Joel DM, Takeuchi Y, Yoneyama K (2005) Germination response of Orobanche seeds subjected to conditioning temperature, water potential and growth regulator treatments. Weed Res 45:467–476

    Article  Google Scholar 

  • Stewart GR, Press MC (1990) The physiology and biochemistry of parasitic angiosperms. Annu Rev Plant Physiol Plant Mol Biol 41:127–151

    Article  CAS  Google Scholar 

  • Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–342

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Omigawa Y, Ogasawara M, Yomeyama K, Konnai M, Worsham AD (1995) Effects of brassinosteroids on conditioning and germination of clover broomrape (Orobanche minor) seeds. Plant Growth Regul 16:153–160

    Article  CAS  Google Scholar 

  • Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293

    Article  PubMed  CAS  Google Scholar 

  • Zehhar N, Ingouff M, Bouya D, Fer A (2002) Possible involvement of gibberellins and ethylene in Orobanche ramosa germination. Weed Res 42:464–469

    Article  CAS  Google Scholar 

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Correspondence to Yasuhisa Fukui.

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Uematsu, K., Nakajima, M., Yamaguchi, I. et al. Role of cAMP in Gibberellin Promotion of Seed Germination in Orobanche minor Smith. J Plant Growth Regul 26, 245–254 (2007). https://doi.org/10.1007/s00344-007-9012-9

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  • DOI: https://doi.org/10.1007/s00344-007-9012-9

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