Advertisement

Induction of Germination

  • Koichi YoneyamaEmail author
  • Carolien Ruyter-Spira
  • Harro Bouwmeester
Chapter

Abstract

Germination is the first crucial step in the life cycle of obligate root parasitic Orobanchaceae, which cannot survive on their own. Therefore, germination of the tiny seeds with minimal reserves should occur only near host roots. These parasites detect the presence of hosts by using root-derived signalling molecules belonging to several distinct classes of metabolites. Strigolactones, the most important germination stimulants, are derived from carotenoids through the action of carotenoid isomerase, carotenoid cleavage dioxygenases, and possibly a cytochrome P450 enzyme. Strigolactone production is increased under phosphate and nitrogen deficiencies. Strigolactones also attract arbuscular mycorrhizal fungi and act as plant hormones that decrease shoot and increase root branching. Various strigolactones have been identified, and the biological processes have differential sensitivity to different strigolactones. Germination stimulants may be a target for the control of parasitic weeds, but considering their other biological functions, such strategies need to be carefully analyzed for unwanted side effects.

Keywords

Arbuscular Mycorrhizal Root Exudate Phosphate Starvation Parasitic Weed Germination Stimulant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

KY acknowledges grants from KAKENHI (18208010, 23338006) and Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry. HB acknowledges funding by the Netherlands Organization for Scientific Research (NWO; VICI grant, 865.06.002 and Equipment grant, 834.08.001). He was co-financed by the Centre for BioSystems Genomics (CBSG) which is part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research.

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedGoogle Scholar
  2. Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117PubMedGoogle Scholar
  3. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester HJ, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351PubMedGoogle Scholar
  4. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26:1053–1066Google Scholar
  5. Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029PubMedGoogle Scholar
  6. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) D14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424PubMedGoogle Scholar
  7. Auger B, Pouvreau J-B, Pouponneau K, Yoneyama K, Montiel G et al (2012) Germination stimulants of Phelipanche ramosa in the rhizosphere of Brassica napus are derived from the glucosinolate pathway. Mol Plant Microbe Interact 25:993–1004PubMedGoogle Scholar
  8. Awad AA, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48:221–227Google Scholar
  9. Ayongwa GC, Stomph TJ, Emechebe AM, Kuyper TW (2006) Root nitrogen concentration of sorghum above 2% produces least Striga hermonthica seed stimulation. Ann Appl Biol 149:255–262Google Scholar
  10. Babalola OO, Osir EO, Sanni AI (2002) Characterization of potential ethylene-producing rhizosphere bacteria of Striga-infested maize and sorghum. Afr J Biotechnol 1:67–69Google Scholar
  11. Babiker AG, Ejeta G, Butler LG, Woodson WR (1993a) Ethylene biosynthesis and strigol-induced germination of Striga asiatica. Physiol Plant 88:359–365Google Scholar
  12. Babiker AGT, Butler KG, Ejeta G, Woodson WR (1993b) Enhancement of ethylene biosynthesis and germination by cytokinins and 1-aminocyclopropane-1-carboxylic acid in Striga asiatica seeds. Physiol Plant 89:21–26Google Scholar
  13. Baldwin IT, Staszak-Kozinski L, Davidson R (1994) Up in smoke: smoke-derived germination cues for postfire annual, Nicotiana attenuata Torr. ex. Watson. J Chem Ecol 20:2345–2371Google Scholar
  14. Balzergue C, Puech-Pags V, Bécard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 62:1049–1060PubMedGoogle Scholar
  15. Bar Nun N, Mayer AM (2005) Smoke chemicals and coumarin promote the germination of the parasitic weed Orobanche aegyptiaca. Isr J Plant Sci 53:97–101Google Scholar
  16. Berner DK, Schaad NW, Völksch B (1999) Use of ethylene-producing bacteria for stimulation of Striga spp. seed germination. Biol Control 15:274–282Google Scholar
  17. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J-C, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247Google Scholar
  18. Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132:281–288PubMedGoogle Scholar
  19. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signalling molecule. Curr Biol 14:1232–1238PubMedGoogle Scholar
  20. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 Encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449PubMedGoogle Scholar
  21. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364PubMedGoogle Scholar
  22. Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230PubMedGoogle Scholar
  23. Brown NAC, van Staden J (1997) Smoke as a germination cue: a review. Plant Growth Regul 22:115–124Google Scholar
  24. Brown R, Johnson AW, Robinson E, Todd AR (1949) The stimulant involved in the germination of Striga hermonthica. Proc R Soc Lond B Biol Sci 136:395–404Google Scholar
  25. Brown R, Greenwood AD, Johnson AW, Long AG (1951a) The stimulant involved in the germination of Orobanche minor Sm. 1. Assay technique and bulk preparation of the stimulant. Biochem J 48:559–564PubMedGoogle Scholar
  26. Brown R, Greenwood AD, Johnson AW, Long AG, Tyler GL (1951b) The stimulant involved in the germination of Orobanche minor Sm. 2. Chromatographic purification of crude concentrates. Biochem J 48:564–568PubMedGoogle Scholar
  27. Brown R, Greenwood AD, Johnson AW, Lansdown AR, Long AG, Suderland N (1952a) The Orobanche germination factor. III. Concentration of the factor by counter current distribution. Biochem J 52:571–574PubMedGoogle Scholar
  28. Brown R, Johnson AW, Robinson E, Tyler GL (1952b) The Striga germination factor. II. Chromatographic purification of crude concentrates. Biochem J 50:596–600PubMedGoogle Scholar
  29. Butler LG (1995) Chemical communication between the parasitic weed Striga and its crop host. A new dimension in allelochemistry. In: Inderjit KM, Dakshini M, Enhelling FA (eds) Allelopathy, organisms, processes and applications. American Chemical Society, Washington, DC, pp 158–166Google Scholar
  30. Cardoso C, Ruyter-Spira C, Bouwmeester HJ (2011) Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci 180:414–420PubMedGoogle Scholar
  31. Chae HS, Yoneyama K, Takeuchi Y, Joel DM (2004) Fluridone and norflurazon, carotenoid-biosynthesis inhibitors, promote seed conditioning and germination of the holoparasite Orobanche minor. Physiol Plant 120:328–337PubMedGoogle Scholar
  32. Chang M, Netzly DG, Butler LG, Lynn DG (1986) Chemical regulation of distance: characterization of the first natural host germination stimulant for Striga asiatica. J Am Chem Soc 108:7858–7860PubMedGoogle Scholar
  33. Chen VX, Boyer FD, Rameau C, Retailleau P, Vors JP, Beau JM (2010) Stereochemistry, total synthesis, and biological evaluation of the new plant hormone solanacol. Chem Eur J 16:13941–13945PubMedGoogle Scholar
  34. Chittapur BM, Hunshal CS, Shenoy H (2001) Allelopathy in parasitic weed management: role of catch and trap crops. Allelopathy J 8:147–160Google Scholar
  35. Chiwocha SDS, Dixon KW, Flematti GR, Ghisalbert EL, Merritt DJ, Nelson DC, Riseborough J-AM, Smith SM, Stevens JC (2009) Karrikins: a new family of plant growth regulators in smoke. Plant Sci 177:252–256Google Scholar
  36. Cline M (1997) Concepts and terminology of apical dominance. Am J Bot 84:1064PubMedGoogle Scholar
  37. 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 154:1189–1190PubMedGoogle Scholar
  38. Cook CE, Whichard LP, Wall ME, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. II. The structure of strigol – a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199Google Scholar
  39. Daws MI, Pritchard HW, Van Staden J (2008) Butenolide from plant-derived smoke functions as a strigolactone analogue: evidence from parasitic weed seed germination. S Afr J Bot 74:116–120Google Scholar
  40. Dayan FE, Howell JL, Weidenhamer JD (2009) Dynamic root exudation of sorgoleone and its in planta mechanism of action. J Exp Bot 60:2107–2117PubMedGoogle Scholar
  41. Delaux P-M, Xie X, Timme RE, Puech-Pages V, Dunand C et al (2012) Origin of strigolactones in the green lineage. New Phytol 195:857–871PubMedGoogle Scholar
  42. Dixon KW, Roche S, Pate JS (1995) The promotive effect of smoke derived from burnt native vegetation on seed germination of Western Australian plants. Oecologia 101:185–192Google Scholar
  43. Dor E, Alperin B, Wininger S, Ben-Dor B, Somvanshi VS, Koltai H, Kapulnik Y, Hershenhorn J (2010) Characterization of a novel tomato mutant resistant to the weedy parasites Orobanche and Phelipanche spp. Euphytica 171:371–380Google Scholar
  44. Ejeta G (2007) Breeding for Striga resistance in sorghum: exploitation of an intricate host-parasite biology. Crop Sci 47:S216–S227Google Scholar
  45. El-Halmouch Y, Benharrat H, Thalouarn P (2006) Effect of root exudates from different tomato genotypes on broomrape (O. aegyptiaca) seed germination and tubercle development. Crop Prot 25:501–507Google Scholar
  46. Evidente A, Andolfi A, Fiore M, Boari A, Vurro M (2006) Stimulation of Orobanche ramosa seed germination by fusicoccin derivatives: a structure–activity relationship study. Phytochemistry 67:19–26PubMedGoogle Scholar
  47. Evidente A, Fernández-Aparicio M, Cimmino A, Rubiales D, Andolfi A, Motta A (2009) Peagol and peagoldione, two new strigolactone-like metabolites isolated from pea root exudates. Tetrahedron Lett 50:6955–6958Google Scholar
  48. Evidente A, Cimmino A, Fernández-Aparicio M, Andolfi A, Rubiales D, Motta A (2010) Polyphenols, including the new peapolyphenols A-C, from pea root exudates stimulate Orobanche foetida seed germination. J Agric Food Chem 58:2902–2907PubMedGoogle Scholar
  49. Evidente A, Cimmino A, Fernández-Aparicio M, Rubiales D, Andolfi A, Melck D (2011) Soyasapogenol B and trans-22-dehydrocampesterol from common vetch (Vicia sativa L.) root exudates stimulate broomrape seed germination. Pest Manag Sci 67:1015–1022PubMedGoogle Scholar
  50. Fernández-Aparicio M, García-Garrido JM, Ocampo JA, Rubiales D (2010) Colonisation of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 50:262–268Google Scholar
  51. Fernández-Aparicio M, Yoneyama K, Rubiales D (2011) The role of strigolactones in host specificity of Orobanche and Phelipanche seed germination. Seed Sci Res 21:55–61Google Scholar
  52. Flematti GR, Ghisalberti EL, Dixon KW, Trengrove RD (2004) A compound from smoke that promotes seed germination. Science 305:977PubMedGoogle Scholar
  53. Foo E, Turnbull CGN, Beveridge CA (2001) Long-distance signalling and the control of branching in the rms1 mutant of pea. Plant Physiol 126:203–209PubMedGoogle Scholar
  54. Fukui K, Ito S, Ueno K, Yamaguchi S, Kyozuka J, Asami T (2011) Inhibition of rice branching and promotion of Striga germination by debranone derivatives mimicking strigolactone function. Bioorg Med Chem Lett 21:4905–4908PubMedGoogle Scholar
  55. Goldwasser Y, Yoder JI (2001) Differential induction of Orobanche seed germination by Arabidopsis thaliana. Plant Sci 160:951–959PubMedGoogle Scholar
  56. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedGoogle Scholar
  57. Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22:2032–2036PubMedGoogle Scholar
  58. Harrison MJ (2005) Signalling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedGoogle Scholar
  59. Hauck C, Müller S, Schildknecht H (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. J Plant Physiol 139:474–478Google Scholar
  60. Hess DE, Ejeta G, Butler LG (1992) Selecting sorghum genotypes expressing a quantitative biosynthetic trait that confers resistance to Striga. Phytochemistry 31:493–497Google Scholar
  61. Höniges A, Ardelean A, Xie X, Yoneyama K, Yoneyama K, Wegmann K (2012) Towards understanding Orobanche host-specificity. Rom Agric Res 29:313–322Google Scholar
  62. Humphrey AJ, Beale MH (2006) Strigol: biogenesis and physiological activity. Phytochemistry 67:636–640PubMedGoogle Scholar
  63. Ito S, Kitahata N, Umehara M, Hanada A, Kato A, Ueno K, Mashiguchi K, Kyozuka J, Yoneyama K, Yamaguchi S, Asami T (2010) A new lead chemical for strigolactone biosynthesis inhibitors. Plant Cell Physiol 51:1143–1150PubMedGoogle Scholar
  64. Jain R, Foy CL (1992) Nutrient effects on parasitism and germination of Egyptian broomrape (Orobanche aegyptiaca). Weed Technol 6:269–275Google Scholar
  65. Jamil M, Charnikhova T, Verstappen F, Bouwmeester H (2010) Carotenoid inhibitors reduce strigolactone production and Striga hermonthica infection in rice. Arch Biochem Biophys 504:123–131PubMedGoogle Scholar
  66. Jamil M, Charnikhova T, Cardoso C, Jamil T, Ueno K, Verstappen F, Asami T, Bouwmeester HJ (2011a) Quantification of the relationship between strigolactones and Striga hermonthica infection in rice under varying levels of nitrogen and phosphorus. Weed Res 51:373–385Google Scholar
  67. Jamil M, Rodenburg J, Charnikhova T, Bouwmeester HJ (2011b) Pre-attachment Striga hermonthica resistance of NERICA cultivars based on low strigolactone production. New Phytol 192:964–975PubMedGoogle Scholar
  68. Joel DM, Hershenhorn J, Eizenburg H, Aly R, Ejeta G, Rich PJ, Ransom JK, Sauerborn J, Rubiales D (2007) Biology and management of weedy root parasites. In: Janick J (ed) Horticultural reviews. Wiley, London, pp 267–349Google Scholar
  69. Joel DM, Chaudhuri SK, Plakhine D, Ziadna H, Steffens JC (2011) Dehydrocostus lactone is exuded from sunflower roots and stimulates germination of the root parasite Orobanche cumana. Phytochemistry 72:624–634PubMedGoogle Scholar
  70. Kapulnik Y, Delaux P-M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier J-P, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216PubMedGoogle Scholar
  71. Keeley JE, Fotheringham CJ (1997) Trace gas emissions and smoke-induced seed germination. Science 276:1248–1250Google Scholar
  72. Kim HI, Xie X, Kim HS, Chun JC, Yoneyama K, Nomura T, Takeuchi Y, Yoneyama K (2010) Structure-activity relationship of naturally occurring strigolactones in Orobanche minor seed germination stimulation. J Pestic Sci 35:344–347Google Scholar
  73. Kisugi T, Xie X, Kim HI, Yoneyama K, Sado A, Akiyama K, Hayashi H, Uchida K, Yokota T, Nomura T, Yoneyama K (2013) Strigone, the first isolation and identification as a natural strigolactone from Houttuynia cordata. Phytochemistry 87:60–64PubMedGoogle Scholar
  74. Kitahata N, Ito S, Kato A, Ueno K, Nakano T, Yoneyama K, Asami T (2011) Abamine as a basis for new designs of regulators of strigolactone production. J Pestic Sci 36:53–57Google Scholar
  75. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011a) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987PubMedGoogle Scholar
  76. Kohlen W, Ruyter-Spira C, Bouwmeester HJ (2011b) Strigolactones. A new musician in the orchestra of plant hormones. Botany 89:827–840Google Scholar
  77. Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P, Haider I, Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ, López-Ráez JA (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signalling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547PubMedGoogle Scholar
  78. Koltai H, Dor E, Hershenhorn J, Joel D, Weininger S, Lekalla S, Shealtiel H, Bahattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010a) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136Google Scholar
  79. Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, Joel DM, Kapulnik Y (2010b) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61:1739–1749PubMedGoogle Scholar
  80. Koltai H, Cohen M, Chesin O, Mayzlish-Gati E, Bécard G, Puech-Pagès V, Dor BB, Resnick N, Wininger S, Kapulnik Y (2011) Light is a positive regulator of strigolactone levels in tomato roots. J Plant Physiol 168:1993–1996PubMedGoogle Scholar
  81. Kondo Y, Tadokoro E, Matsuura M, Iwasaki K, Sugimoto Y, Miyake H, Takikawa H, Sasaki M (2007) Synthesis and seed germination stimulating activity of some imino analogs of strigolactones. Biosci Biotechnol Biochem 71:2781–2786PubMedGoogle Scholar
  82. Kusumoto D, Chae SH, Mukaida K, Yoneyama K, Joel DM, Takeuchi Y (2006) Effects of fluridone and norflurazon on conditioning and germination of Striga asiatica seeds. Plant Growth Regul 48:73–78Google Scholar
  83. Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC (2010) Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytol 188:803–813PubMedGoogle Scholar
  84. Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ, Van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal Behav 2:58–62PubMedGoogle Scholar
  85. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525PubMedGoogle Scholar
  86. Logan DC, Stewart GR (1991) Role of ethylene in the germination of the hemiparasite Striga hermonthica. Plant Physiol 97:1435–1438PubMedGoogle Scholar
  87. López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256PubMedGoogle Scholar
  88. López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008a) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874PubMedGoogle Scholar
  89. López-Ráez JA, Charnikhova T, Mulder P, Kohlen W, Bino R, Levin I, Bouwmeester H (2008b) Susceptibility of the tomato mutant high pigment-2dg (hp-2 dg) to Orobanche spp. infection. J Agric Food Chem 56:6326–6332PubMedGoogle Scholar
  90. López-Ráez JA, Matusova R, Cardoso C, Jamil M, Charnikhova T, Kohlen W, Ruyter-Spira C, Verstappen F, Bouwmeester H (2008c) Strigolactones: ecological significance and use as a target for parasitic plant control. Pest Manag Sci 64:471–477Google Scholar
  91. López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TDH, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187:343–354PubMedGoogle Scholar
  92. López-Ráez JA, Charnikhova T, Fernandez I, Bouwmeester HJ, Pozo MJ (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297PubMedGoogle Scholar
  93. Lynn DG, Chang M (1990) Phenolic signals in cohabitation: implications for plant development. Annu Rev Plant Physiol Plant Mol Biol 41:497–526Google Scholar
  94. Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390PubMedGoogle Scholar
  95. Macías FA, García-Díaz MD, Pérez-de-Luque A, Rubiales D, Galindo JCG (2009) New chemical clues for broomrape-sunflower host–parasite interactions: synthesis of guaianestrigolactones. J Agric Food Chem 57:5853–5864PubMedGoogle Scholar
  96. Matsuura H, Ohashi K, Sasako H, Tagawa N, Takano Y, Ioka Y, Nabeta K, Yoshihara T (2008) Germination stimulant from root exudates of Vigna unguiculata. Plant Growth Regul 54:31–36Google Scholar
  97. Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934PubMedGoogle Scholar
  98. Mori K, Matsui J, Bando M, Kido M, Takeuchi Y (1998) Synthetic disproof against the structure proposed for alectrol, the germination stimulant from Vigna unguiculata. Tetrahedron Lett 39:6023–6026Google Scholar
  99. Müller S, Hauck C, Schildknecht H (1992) Germination stimulants produced by Vigna unguiculata Walp cv Saunders Upright. J Plant Growth Regul 11:77–84Google Scholar
  100. Mwakaboko AS, Zwanenburg B (2011) Strigolactone analogs derived from ketones using a working model for germination stimulants as a blueprint. Plant Cell Physiol 52:699–715PubMedGoogle Scholar
  101. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074PubMedGoogle Scholar
  102. Nefkens GHL, Thuring JWJF, Beenakkers MFM, Zwanenburg B (1997) Synthesis of a phthaloylglycine-derived strigol analogue and its germination stimulatory activity towards seeds of the parasitic weeds Striga hermonthica and Orobanche crenata. J Agric Food Chem 45:2273–2277Google Scholar
  103. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signalling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:8897–8902PubMedGoogle Scholar
  104. Pérez de Luque AP, Galindo JCG, Macías FA, Jorrín J (2000) Sunflower sesquiterpene lactone models induce Orobanche cumana seed germination. Phytochemistry 53:45–50PubMedGoogle Scholar
  105. Pérez-Torres C-A, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272PubMedGoogle Scholar
  106. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedGoogle Scholar
  107. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539PubMedGoogle Scholar
  108. Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626PubMedGoogle Scholar
  109. Rubiales D, Verkleij J, Vurro M, Murdoch AJ, Joel DM (2009) Parasitic plant management in sustainable agriculture. Weed Res 49:1–5Google Scholar
  110. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734PubMedGoogle Scholar
  111. Sánchez-Calderón L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184PubMedGoogle Scholar
  112. Sergeant MJ, Li J-J, Fox C, Brookbank N, Rea D, Bugg TD, Thompson AJ (2009) Selective inhibition of carotenoid cleavage dioxygenases: phenotypic effects on shoot branching. J Biol Chem 284:5257–5264PubMedGoogle Scholar
  113. Shen H, Luong P, Huq E (2007) The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145:1471–1483PubMedGoogle Scholar
  114. Siame BP, Weerasuriya Y, Wood K, Ejeta G, Butler LG (1993) Isolation of strigol, a germination stimulant for Striga asiatica, from host plants. J Agric Food Chem 41:1486–1491Google Scholar
  115. Sliwinska E, Bassel GW, Bewley JD (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. J Exp Bot 60:3587–3594PubMedGoogle Scholar
  116. Snowden KC, Simkin AJ, Janssen BJ et al (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759PubMedGoogle Scholar
  117. Sorefan K, Booker J, Haurogné K et al (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474PubMedGoogle Scholar
  118. Stirnberg P, van de Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141PubMedGoogle Scholar
  119. Sugimoto Y, Ali AM, Yabuta S, Kinoshita H, Inanaga S, Itai A (2003) Germination strategy of Striga hermonthica involves regulation of ethylene biosynthesis. Physiol Plant 119:1–9Google Scholar
  120. Sun Z, Matusova R, Bouwmeester HJ (2007) Germination of Striga and chemical signalling involved: a target for control methods. In: Gressel J, Ejeta G (eds) Integrating new technologies for Striga control: towards ending the witch-hunt. World Scientific, Singapore, pp 47–60Google Scholar
  121. Sun Z, Has J, Walter MH et al (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801PubMedGoogle Scholar
  122. Taylor J, Harrier LA (2003) Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Mol Biol 51:619–629PubMedGoogle Scholar
  123. Toh S, Kamiya Y, Kawakami N, Nambara E, McCourt P, Tsuchiya Y (2012) Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol 53:107–117PubMedGoogle Scholar
  124. Troughton A (1977) The effect of phosphorus nutrition upon the growth and morphology of young plants of Lolium perenne L. Ann Bot 41:85–92Google Scholar
  125. Tsuchiya Y, McCourt P (2009) Strigolactones: a new hormone with a past. Curr Opin Plant Biol 12:556–561PubMedGoogle Scholar
  126. Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741–749PubMedGoogle Scholar
  127. Ueno K, Nomura S, Muranaka S, Mizutani M, Takikawa H, Sugimoto Y (2011) Ent-2′-epi-orobanchol and its acetate, as germination stimulants for Striga gesnerioides seeds isolated from cowpea and red clover. J Agric Food Chem 59:10485–10490PubMedGoogle Scholar
  128. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedGoogle Scholar
  129. Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126PubMedGoogle Scholar
  130. Vaucher JP (1823) Mémoire sur la germination des orobanches. Mém Mus Hist nat Paris 10:261–273Google Scholar
  131. Virtue JG, DeDear C, Potter MJ, Rieger M (2006) Potential use of isothiocyanates in branched broomrape eradication. In: Preston C, Watts JHW, Crossman ND (eds) 15th Australian weeds conference, Adelaide. pp 629–632Google Scholar
  132. Vogel JT, Walter MH, Giavalisco P et al (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311PubMedGoogle Scholar
  133. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295PubMedGoogle Scholar
  134. Weerasuriya Y, Siame BA, Hess D, Ejets G, Butler LG (1993) Influence of conditions and genotype on the amount of Striga germination stimulants exuded by root of several host crops. J Agric Food Chem 41:1492–1496Google Scholar
  135. Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235PubMedGoogle Scholar
  136. Wigchert SCM, Kuiper E, Boelhouwer GJ, Nefkens GHL, Verkleij JAC, Zwanenburg B (1999) Dose–response of seeds of the parasitic weeds Striga and Orobanche toward the synthetic germination stimulants GR 24 and Nijmegen 1. J Agric Food Chem 47:1705–1710PubMedGoogle Scholar
  137. Xie X, Kusumoto D, Takeuchi Y, Yoneyama K, Yamada Y, Yoneyama K (2007) 2′-Epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. J Agric Food Chem 55:8067–8072PubMedGoogle Scholar
  138. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K (2008a) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Lett 49:2066–2068Google Scholar
  139. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K (2008b) Isolation and identification of alectrol as (+)-orobanchyl acetate, a novel germination stimulant for root parasitic plants. Phytochemistry 69:427–431PubMedGoogle Scholar
  140. Xie X, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y, Yoneyama K (2009a) Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum. Phytochemistry 70:211–215PubMedGoogle Scholar
  141. Xie X, Yoneyama K, Kurita J-Y, Harada Y, Yamada Y, Takeuchi Y, Yoneyama K (2009b) 7-Oxoorobanchyl acetate and 7-oxoorobanchol as germination stimulants for root parasitic plants from flax (Linum usitatissimum). Biosci Biotechnol Biochem 73:1367–1370PubMedGoogle Scholar
  142. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117PubMedGoogle Scholar
  143. Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S, Akiyama K, Hayashi H, Yokota T, Nomura T, Yoneyama K (2012) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol Plant 6:153–163PubMedGoogle Scholar
  144. Yasuda N, Sugimoto Y, Kato M, Inanaga S, Yoneyama K (2003) (+)-Strigol, a witchweed seed germination stimulant, from Menispermum dauricum root culture. Phytochemistry 62:1115–1119PubMedGoogle Scholar
  145. Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y (1998) Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49:1967–1973Google Scholar
  146. Yoneyama K, Ogasawara M, Takeuchi Y, Konnai M, Sugimoto Y, Seto H, Yoshida S (1998a) Effect of jasmonates and related compounds on seed germination of Orobanche minor Smith and Striga hermonthica (Del.) Benth. Biosci Biotechnol Biochem 62:1448–1450Google Scholar
  147. Yoneyama K, Takeuchi Y, Ogasawara M, Konnai M, Sugimoto Y, Sassa T (1998b) Cotylenins and fusicoccins stimulate seed germination of Striga hermonthica (Del.) Benth and Orobanche minor Smith. J Agric Food Chem 46:1583–1586Google Scholar
  148. Yoneyama K, Takeuchi Y, Yokota T (2001) Production of clover broomrape seed germination stimulants by red clover root requires nitrate but is inhibited by phosphate and ammonium. Physiol Plant 112:25–30PubMedGoogle Scholar
  149. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132PubMedGoogle Scholar
  150. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038PubMedGoogle Scholar
  151. Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494PubMedGoogle Scholar
  152. Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones; structures and biological activities. Pest Manag Sci 65:467–470PubMedGoogle Scholar
  153. Yoneyama K, Awad AA, Xie X, Yoneyama K, Takeuchi Y (2010) Strigolactones as germination stimulants for root parasitic plants. Plant Cell Physiol 51:1095–1103PubMedGoogle Scholar
  154. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207PubMedGoogle Scholar
  155. Zehhar N, Ingouff M, Bouya D, Fer A (2002) Possible involvement of gibberellins and ethylene in Orobanche ramosa germination. Weed Res 42:464–469Google Scholar
  156. Zhelev N (1987) The biological role of exogenic factors in broomrape germination. Rastenievudni Nauki 26:36–43 (in Bulgarian)Google Scholar
  157. Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48:687–698PubMedGoogle Scholar
  158. Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65:478–491PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Koichi Yoneyama
    • 1
    Email author
  • Carolien Ruyter-Spira
    • 2
    • 3
  • Harro Bouwmeester
    • 2
    • 4
  1. 1.Weed Science CenterUtsunomiya UniversityUtsunomiyaJapan
  2. 2.Laboratory of Plant PhysiologyWageningen UniversityWageningenThe Netherlands
  3. 3.Plant Research InternationalWageningenThe Netherlands
  4. 4.Centre for BioSystems GenomicsWageningenThe Netherlands

Personalised recommendations