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Planta

, Volume 243, Issue 6, pp 1327–1337 | Cite as

The Whats, the Wheres and the Hows of strigolactone action in the roots

  • Cedrick Matthys
  • Alan Walton
  • Sylwia Struk
  • Elisabeth Stes
  • François-Didier Boyer
  • Kris Gevaert
  • Sofie GoormachtigEmail author
Review
Part of the following topical collections:
  1. Strigolactones

Abstract

Main conclusion

Strigolactones control various aspects of plant development, including root architecture. Here, we review how strigolactones act in the root and survey the strigolactone specificity of signaling components that affect root development.

Strigolactones are a group of secondary metabolites produced in plants that have been assigned multiple roles, of which the most recent is hormonal activity. Over the last decade, these compounds have been shown to regulate various aspects of plant development, such as shoot branching and leaf senescence, but a growing body of literature suggests that these hormones play an equally important role in the root. In this review, we present all known root phenotypes linked to strigolactones. We examine the expression and presence of the main players in biosynthesis and signaling of these hormones and bring together the available information that allows us to explain how strigolactones act to modulate the root system architecture.

Keywords

rac-GR24 Root system architecture Strigolactone Strigolactone-related compounds 

Abbreviations

D

DWARF

KAI

KARRIKIN INSENSITIVE

LR

Lateral root

LRD

Lateral root density

MAX

MORE AXILLARY GROWTH

PIN

PIN-FORMED

rac-GR24

RACEMIC GR24

SCF

Skp, Cullin, F-box

SL

Strigolactone

SMAX1

SUPPRESSOR OF MAX2 1

SMXL

SUPPRESSOR OF MAX2 1 LIKE

TIR1

TRANSPORT INHIBITOR RESPONSE1

WT

Wild type

Notes

Acknowledgments

We thank Martine De Cock for help with the manuscript. This work was supported by Ghent University Hercules program for the UPLC-Synapt Q-Tof HDMS system (Grant No. AUGE/014) and European Cooperation on Science and Technology (COST action FA1206). C.M. and A.W. are the recipients of a predoctoral fellowship from the “Bijzonder Onderzoeksfonds” of the Ghent University and of a VIB International PhD program fellowship, respectively. E.S. is a Postdoctoral Fellow of the Research Foundation-Flanders.

References

  1. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827CrossRefPubMedGoogle Scholar
  2. Alder A, Holdermann I, Beyer P, Al-Babili S (2008) Carotenoid oxygenases involved in plant branching catalyse a highly specific conserved apocarotenoid cleavage reaction. Biochem J 416:289–296CrossRefPubMedGoogle Scholar
  3. Arite T, Kameoka H, Kyozuka J (2012) Strigolactone positively controls crown root elongation in rice. J Plant Growth Regul 31:165–172CrossRefGoogle Scholar
  4. Bainbridge K, Sorefan K, Ward S, Leyser O (2005) Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. Plant J 44:569–580CrossRefPubMedGoogle Scholar
  5. Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea. Action of genes Rms3 and Rms4. Plant Physiol 110:859–865PubMedPubMedCentralGoogle Scholar
  6. Beveridge CA, Dun EA, Rameau C (2009) Pea has its tendrils in branching discoveries spanning a century from auxin to stringolactones. Plant Physiol 151:985–990CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 14:1232–1238CrossRefPubMedGoogle Scholar
  8. 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 8:443–449CrossRefPubMedGoogle Scholar
  9. Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS, Cubas P (2014) Strigolactone promotes degradation of DWARF14, an α/β hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26:1134–1150CrossRefPubMedPubMedCentralGoogle Scholar
  10. Conn CE, Nelson DC (2016) Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front Plant Sci 6:1219CrossRefPubMedPubMedCentralGoogle Scholar
  11. Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, Shirasu K, Bond CS, Dyer KA, Nelson DC (2015) Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–543CrossRefPubMedGoogle Scholar
  12. 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 154:1189–1190CrossRefPubMedGoogle Scholar
  13. 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 137:2905–2913CrossRefPubMedGoogle Scholar
  14. De Cuyper C, Fromentin J, Yocgo RE, De Keyser A, Guillotin B, Kunert K, Boyer F-D, Goormachtig S (2015) From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J Exp Bot 66:137–146 [Erratum J Exp Bot 66:4091] Google Scholar
  15. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445CrossRefPubMedGoogle Scholar
  16. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221CrossRefPubMedGoogle Scholar
  17. Drummond RSM, Martínez-Sánchez NM, Janssen BJ, Templeton KR, Simons JL, Quinn BD, Karunairetnam S, Snowden KC (2009) Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE7 is involved in the production of negative and positive branching signals in petunia. Plant Physiol 151:1867–1877CrossRefPubMedPubMedCentralGoogle Scholar
  18. Drummond RSM, Sheehan H, Simons JL, Martínez-Sánchez NM, Turner RM, Putterill J, Snowden KC (2011) The expression of petunia strigolactone pathway genes is altered as part of the endogenous developmental program. Front Plant Sci 2:115PubMedPubMedCentralGoogle Scholar
  19. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17:464–474CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60CrossRefPubMedGoogle Scholar
  21. 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 455:189–194CrossRefPubMedGoogle Scholar
  22. Guo Y, Zheng Z, La Clair JJ, Chory J, Noel JP (2013) Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. Proc Natl Acad Sci USA 110:8284–8289CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG, Summers W, Carbonnel S, Mansfield C, Yang S-Y, Nadal M, Acosta I, Takano M, Jiao W-B, Schneeberger K, Kelly KA, Paszkowski U (2015) Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350:1521–1524CrossRefPubMedGoogle Scholar
  24. 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 22:2032–2036CrossRefPubMedGoogle Scholar
  25. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 46:79–86CrossRefPubMedGoogle Scholar
  27. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, Yi W, Zhao L, Ma H, He Y, Wu Z, Melcher K, Qian Q, Xu HE, Wang Y, Li J (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405CrossRefPubMedGoogle Scholar
  28. Jiang L, Matthys C, Marquez-Garcia B, De Cuyper C, Smet L, De Keyser A, Boyer F-D, Beeckman T, Depuydt S, Goormachtig S (2016) Strigolactones spatially influence lateral root development through the cytokinin signaling network. J Exp Bot 67:379–389CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 (2011a) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216CrossRefPubMedGoogle Scholar
  30. 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 62:2915–2924CrossRefPubMedGoogle Scholar
  31. 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 155:974–987CrossRefPubMedPubMedCentralGoogle Scholar
  32. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549CrossRefPubMedGoogle Scholar
  33. Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136CrossRefGoogle Scholar
  34. Kong X, Zhang M, Ding Z (2014) D53: the missing link in strigolactone signaling. Mol Plant 7:761–763CrossRefPubMedGoogle Scholar
  35. 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 198:866–874CrossRefPubMedGoogle Scholar
  36. 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 483:341–344CrossRefPubMedGoogle Scholar
  37. Kumar M, Pandya-Kumar N, Dam A, Haor H, Mayzlish-Gati E, Belausov E, Wininger S, Abu-Abied M, McErlean CSP, Bromhead LJ, Prandi C, Kapulnik Y, Koltai H (2015) Arabidopsis response to low-phosphate conditions includes active changes in actin filaments and PIN2 polarization and is dependent on strigolactone signalling. J Exp Bot 66:1499–1510CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 21:1512–1525CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 64:1967–1981CrossRefPubMedPubMedCentralGoogle Scholar
  40. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287CrossRefPubMedGoogle Scholar
  41. Mashiguchi K, Sasaki E, Shimada Y, Nagae M, Ueno K, Nakano T, Yoneyama K, Suzuki Y, Asami T (2009) Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci Biotechnol Biochem 73:2460–2465CrossRefPubMedGoogle Scholar
  42. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, Wininger S, Resnick N, Cohen M, Kapulnik Y, Koltai H (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160:1329–1341CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 108:8897–8902CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, Koltai H (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202:1184–1196CrossRefPubMedGoogle Scholar
  45. Park J-Y, Kim H-J, Kim J (2002) Mutation in domain II of IAA1 confers diverse auxin-related phenotypes and represses auxin-activated expression of Aux/IAA genes in steroid regulator-inducible system. Plant J 32:669–683CrossRefPubMedGoogle Scholar
  46. Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408CrossRefPubMedGoogle Scholar
  47. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rasmussen A, Heugebaert T, Matthys C, Van Deun R, Boyer F-D, Goormachtig S, Stevens C, Geelen D (2013) A fluorescent alternative to the synthetic strigolactone GR24. Mol Plant 6:100–112CrossRefPubMedGoogle Scholar
  49. 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, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sasse J, Simon S, Gübeli C, Liu G-W, Cheng X, Friml J, Bouwmeester H, Martinoia E, Borghi L (2015) Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr Biol 25:647–655CrossRefPubMedGoogle Scholar
  51. Scaffidi A, Waters MT, Ghisalberti EL, Dixon KW, Flematti GR, Smith SM (2013) Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J 76:1–9PubMedGoogle Scholar
  52. Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232CrossRefPubMedPubMedCentralGoogle Scholar
  53. Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111:1640–1645CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1—JAZ co-receptor. Nature 468:400–405CrossRefPubMedPubMedCentralGoogle Scholar
  55. Shen H, Luong P, Huq E (2007) The F-Box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145:1471–1483CrossRefPubMedPubMedCentralGoogle Scholar
  56. Shen H, Zhu L, Bu Q-Y, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5:750–762CrossRefPubMedGoogle Scholar
  57. 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:e1001474CrossRefPubMedPubMedCentralGoogle Scholar
  58. Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (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 17:746–759CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474CrossRefPubMedPubMedCentralGoogle Scholar
  60. Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, Leyser O, Nelson DC (2015) SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27:3143–3159CrossRefPubMedGoogle Scholar
  61. Stanga JP, Smith SM, Briggs WR, Nelson DC (2013) SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol 163:318–330CrossRefPubMedPubMedCentralGoogle Scholar
  62. Stirnberg P, Furner IJ, Leyser HMO (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94CrossRefPubMedGoogle Scholar
  63. Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate- and nitrate-deficiency–induced root development and auxin transport in rice. J Exp Bot 65:6735–6746CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sun H, Tao J, Hou M, Huang S, Chen S, Liang Z, Xie T, Wei Y, Xie X, Yoneyama K, Xu G, Zhang Y (2015) A strigolactone signal is required for adventitious root formation in rice. Ann Bot 115:1155–1162CrossRefPubMedGoogle Scholar
  65. Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Miñambres M, Walther D, Schulze WX, Paz-Ares J, Scheible W-R, Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:15025 [Erratum Nat. Plants 1:15088] Google Scholar
  66. 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 53:107–117CrossRefPubMedGoogle Scholar
  67. 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 6:741–749CrossRefPubMedGoogle Scholar
  68. Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S, Holbrook-Smith D, Zhang H, McCourt P, Itami K, Kinoshita T, Hagihara S (2015) Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–868CrossRefPubMedGoogle Scholar
  69. Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32:255–262CrossRefPubMedGoogle Scholar
  70. 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 455:195–200CrossRefPubMedGoogle Scholar
  71. Urquhart S, Foo E, Reid JB (2015) The role of strigolactones in photomorphogenesis of pea is limited to adventitious rooting. Physiol Plant 153:392–402CrossRefPubMedGoogle Scholar
  72. Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487CrossRefPubMedGoogle Scholar
  73. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397CrossRefPubMedGoogle Scholar
  74. Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311CrossRefPubMedGoogle Scholar
  75. Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z, Meng X, Wang Y, Smith SM, Li J (2015) Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:3128–3142CrossRefPubMedPubMedCentralGoogle Scholar
  76. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159:1073–1085CrossRefPubMedPubMedCentralGoogle Scholar
  77. Woo HR, Chung KM, Park J-H, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790CrossRefPubMedPubMedCentralGoogle Scholar
  78. Xie X, Yoneyama K, Kisugi T, Nomura T, Akiyama K, Asami T, Yoneyama K (2015) Strigolactones are transported from roots to shoots, although not through the xylem. J Pestic Sci 40:214–216CrossRefGoogle Scholar
  79. Yang X, Lee S, So J-h, Dharmasiri S, Dharmasiri N, Ge L, Jensen C, Hangarter R, Hobbie L, Estelle M (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J 40:772–782CrossRefPubMedGoogle Scholar
  80. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, Ma W, Gao H, Chen J, Yang C, Wang D, Tan J, Zhang X, Guo X, Wang J, Jiang L, Liu X, Chen W, Chu J, Yan C, Ueno K, Ito S, Asami T, Cheng Z, Wang J, Lei C, Zhai H, Wu C, Wang H, Zheng N, Wan J (2013) D14–SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410CrossRefPubMedPubMedCentralGoogle Scholar
  81. 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 48:687–698CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Cedrick Matthys
    • 1
    • 2
  • Alan Walton
    • 1
    • 2
    • 3
    • 4
  • Sylwia Struk
    • 1
    • 2
  • Elisabeth Stes
    • 1
    • 2
    • 3
    • 4
  • François-Didier Boyer
    • 5
    • 6
  • Kris Gevaert
    • 3
    • 4
  • Sofie Goormachtig
    • 1
    • 2
    Email author
  1. 1.Department of Plant Systems BiologyVIBGhentBelgium
  2. 2.Department of Plant Biotechnology and BioinformaticsGhent UniversityGhentBelgium
  3. 3.Department of Medical Protein ResearchVIBGhentBelgium
  4. 4.Department of BiochemistryGhent UniversityGhentBelgium
  5. 5.Institut Jean-Pierre BourginUnité Mixte de Recherche 1318, Institut National de la Recherche Agronomique-AgroParisTechVersailles CedexFrance
  6. 6.Centre de Recherche de GifInstitut de Chimie des Substances Naturelles, Unité Propre de Recherche 2301, Centre National de la Recherche ScientifiqueGif‐Sur‐YvetteFrance

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