Strigolactone involvement in root development, response to abiotic stress, and interactions with the biotic soil environment

Plant Physiology

Volumn 166, Issue 2, 2014, Pages 560-569

  Kapulnik, Yoram ^a   Koltai, Hinanit ^a  

^a VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

LACTONE; SOIL;

GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT ROOT; SIGNAL TRANSDUCTION; SOIL;

LACTONES; PLANT ROOTS; SIGNAL TRANSDUCTION; SOIL; STRESS, PHYSIOLOGICAL;

EID: 84907801212     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.244939     Document Type: Article

References (131)

1. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, et al (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108: 20242–20247
2. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot (Lond) 97: 925–931
3. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827
4. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from b-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348–1351
5. 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: 1416–1424
6. Bates TR, Lynch JP (2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87: 964–970
7. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16: 553–563
8. Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148: 402–413
9. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4: e226
10. Beveridge CA, Symons GM, Murfet IC, Ross JJ, Rameau C (1997) The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol 115: 1251–1258
11. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24: 225–252
12. 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 signaling molecule. Curr Biol 14: 1232–1238
13. 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: 443–449
14. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6: 358–364
15. Boyer FD, de Saint Germain A, Pouvreau JB, Clavé G, Pillot JP, Roux A, Rasmussen A, Depuydt S, Lauressergues D, Frei Dit Frey N, et al (2014) New strigolactone analogs as plant hormones with low activities in the rhizosphere. Mol Plant 7: 675–690
16. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150: 482–493
17. Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The presymbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13: 693–698
18. Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C, Wright MH, Liu J, Meng X, et al (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA 111: 2379–2384
19. Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS, Cubas P (2014) Strigolactone promotes degradation of DWARF14, an a/b hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26: 1134–1150
20. Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M (2003) Effects of phosphate availability on the root system architecture: large-scale analysis of the natural variation between Arabidopsis accessions. Plant Cell Environ 26: 1839–1850
21. Cohen M, Prandi C, Occhiato EG, Tabasso S, Wininger S, Resnick N, Steinberger Y, Koltai H, Kapulnik Y (2013) Structure-function relations of strigolactone analogs: activity as plant hormones and plant interactions. Mol Plant 6: 141–152
22. Cook CE, Whichard LP, Wall M, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J Am Chem Soc 94: 6198–6199
23. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905–2913
24. de Saint Germain A, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163: 1012–1025
25. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195: 857–871
26. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12: 211–221
27. Douds DD Jr, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In Kapulnik Y, Douds DD Jr, eds, Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 107–130
28. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158: 487–498
29. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2013) Dynamics of strigolactone function and shoot branching responses in Pisum sativum. Mol Plant 6: 128–140
30. Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149: 1929–1944
31. 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: 262–268
32. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305: 977
33. Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234: 1073–1081
34. Foo E, Ferguson BJ, Reid JB (2014) The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway. Ann Bot (Lond) 113: 1037–1045
35. Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB (2013a) Strigolactones: internal and external signals in plant symbioses? Plant Signal Behav 8: e23168
36. Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013b) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6: 76–87
37. Fukui K, Ito S, Asami T (2013) Selective mimics of strigolactone actions and their potential use for controlling damage caused by root parasitic weeds. Mol Plant 6: 88–99
38. Fukui K, Ito S, Ueno K, Yamaguchi S, Kyozuka J, Asami T (2011) New branching inhibitors and their potential as strigolactone mimics in rice. Bioorg Med Chem Lett 21: 4905–4908
39. Gianinazzi-Pearson V, Gianinazzi S (1989) Cellular and genetical aspects of interactions between hosts and fungal symbionts in mycorrhizae. Genome 31: 336–341
40. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5: 56–60
41. Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol 133: 65–71
42. Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of Strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55: 21–28
43. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, et al (2008) Strigolactone inhibition of shoot branching. Nature 455: 189–194
44. Gressel J, Joel DM (2013) Weedy orobanchaceae: the problem. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 309–312
45. Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an a/b hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22: 2032–2036
46. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151: 400–412
47. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46: 79–86
48. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, et al (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401–405
49. Joel DM (2000) The long-term approach to parasitic weeds control: manipulation of specific developmental mechanisms of the parasite. Crop Prot 19: 753–758
50. Joel DM (2013) The haustorium and the life cycles of parasitic orobanchaceae. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 21–23
51. Joel DM, Bar H (2013) The seed and the seedling. In Joel DM, Gressel J, Musselman LJ, eds, Parasitic Orobanchaceae. Springer, Berlin, pp 147–165
52. Johnson AW, Rosebery G, Parker C (1976) A novel approach to Striga and Orobanche control using synthetic germination stimulants. Weed Res 16: 223–227
53. Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species: Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142: 1014–1026
54. Jones D, Hinsinger P (2008) The rhizosphere: complex by design. Plant Soil 312: 1–6
55. Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18: 147–160
56. Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier JP, Bécard G, Belausov E, et al (2011a) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233: 209–216
57. Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H (2011b) Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J Exp Bot 62: 2915–2924
58. 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: 344–347
59. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) 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: 974–987
60. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190: 545–549
61. Koltai H, Beveridge CA (2013) Strigolactones and the coordinated development of shoot and root. In Baluka F, ed, Long-Distance Systemic Signaling and Communication in Plants. Springer, Berlin, pp 189–204
62. Koltai H, Dor E, Hershenhorn J, Joel D, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, et al (2010a) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29: 129–136
63. Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, et al (2010b) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61: 1739–1749
64. Koren D, Resnick N, Mayzlish Gati E, Belausov E, Weininger S, Kapulnik Y, Koltai H (2013) Strigolactone signaling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198: 866–874
65. Koske RE, Gemma JN (1992) Fungal reactions to plants prior to mycorrhizal formation. In Allen MF, ed, Mycorrhizal Functioning: An Integrative Plant-Fungal Process. Chapman & Hall, New York, pp 3–36
66. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483: 341–344
67. Lendzemo V, Kuyper TW, Vierheilig H (2009) Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19: 287–294
68. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, et al (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512–1525
69. Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F (2013) Carotenoid cleavage dioxygenase 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64: 1967–1981
70. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280–287
71. López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168: 294–297
72. Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12: 250–258
73. Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14: 77–86
74. 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: 920–934
75. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, et al (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160: 1329–1341
76. McCain S, Davies MS (1983) Effects of pretreatment with phosphate in natural populations of Agrostis capillaris L. New Phytol 94: 367–379
77. Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16: 3181–3195
78. Moscatiello R, Squartini A, Mariani P, Navazio L (2010) Flavonoidinduced calcium signalling in Rhizobium leguminosarum bv. viciae. New Phytol 188: 814–823
79. Mosse B, Hepper C (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5: 215–223
80. Mouchel CF, Leyser O (2007) Novel phytohormones involved in longrange signaling. Curr Opin Plant Biol 10: 473–476
81. 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. PlantPhysiol 138: 2061–2074
82. Nagahashi G, Douds DD Jr (2000) Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi. Mycol Res 104: 1453–1464
83. Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park SH, et al (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4: 2613
84. 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 signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108: 8897–8902
85. Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59: 67–74
86. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58: 93–113
87. Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, et al (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202: 1184–1196
88. Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65: 453–459
89. Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442–450
90. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez 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: 3258–3272
91. Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto I (2011) New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur J Org Chem 2011: 3781–3793
92. 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: 1531–1539
93. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, et al (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976–1987
94. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216: 23–37
95. Redecker D, Raab P (2006) Phylogeny of the glomeromycota (arbuscular mycorrhizal fungi): recent developments and new gene markers. Mycologia 98: 885–895
96. Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68: 33–40
97. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18: 72–83
98. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, 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: 721–734
99. Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17: 354–358
100. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez 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: 174–184
101. Sato D, Awad AA, Chae SH, Yokota T, Sugimoto Y, Takeuchi Y, Yoneyama K (2003) Analysis of strigolactones, germination stimulants for striga and orobanche, by high-performance liquid chromatography/ tandem mass spectrometry. J Agric Food Chem 51: 1162–1168
102. Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279: 46940–46945
103. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediary carbon metabolism in vesiculararbuscular mycorrhizal leek. Plant Physiol 108: 7–15
104. Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474
105. Smith S, Read D, editors (2008) Mycorrhizal Symbiosis, Ed 3. Academic Press Elsevier, New York
106. Solaiman MZ, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol 136: 533–538
107. Soto MJ, Fernandez-Aparicio MN, Castellanos-Morales V, Garcia-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42: 383–385
108. Stirnberg P, van De Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131–1141
109. Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (March 4, 2014) Strigolactones are involved in phosphateand nitratedeficiency-induced root development and auxin transport in rice. J Exp Bot
110. Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139: 3997–4006
111. Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR, Symonova O, Zheng Y, Bucksch A, Mileyko Y, Galkovskyi T, et al (2013) 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc Natl Acad Sci USA 110: E1695–E1704
112. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200
113. Vurro M, Yoneyama K (2012) Strigolactones—intriguing biologically active compounds: perspectives for deciphering their biological role and for proposing practical application. Pest Manag Sci 68: 664–668
114. Waldie T, McCulloch H, Leyser O (February 25, 2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 10.1111/tpj.12488
115. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012a) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159: 1073–1085
116. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012b) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285–1295
117. Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (January 16, 2014) The karrikin response system of Arabidopsis. Plant J 10.1111/tpj.12488
118. Xie X, Kusumoto D, Takeuchi Y, Yoneyama K, Yamada Y, Yoneyama K (2007) 29-epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. J Agric Food Chem 55: 8067–8072
119. Xie X, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y, Yoneyama K (2009) Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum. Phytochemistry 70: 211–215
120. 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: 2066–2068
121. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K (2008b) Isolation and identification of alectrol as (+)-orobanchyl acetate, a germination stimulant for root parasitic plants. Phytochemistry 69: 427–431
122. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48: 93–117
123. 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: 1967–1973
124. Yoneyama K, Kisugi T, Xie X, Yoneyama K (2013) Chemistry of strigolactones: why and how do plants produce so many strigolactones? In de Bruijn FJ, ed, Molecular Microbial Ecology of the Rhizosphere: Two Volume Set, John Wiley & Sons, Inc., Hoboken, NJ, pp 373–379
125. 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: 1197–1207
126. 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: 125–132
127. 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: 484–494
128. 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: 1031–1038
129. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, et al (2013) D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406–410
130. 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: 478–491
131. Zwanenburg B, Nayak SK, Charnikhova TV, Bouwmeester HJ (2013) New strigolactone mimics: structure-activity relationship and mode of action as germinating stimulants for parasitic weeds. Bioorg Med Chem Lett 23: 5182–5186