Strigolactone and Karrikin Signaling Proteins

  • Toshio HakoshimaEmail author


Strigolactones (SLs) are plant hormones that inhibit shoot branching. DWARF14 (D14), which inhibits rice tillering, is an SL receptor involved in the branching inhibition pathway. Close homologs, rice DWARF14-LIKE (D14L) or Arabidopsis KARRIKIN-INSENSITIVE 2 (KAI2), are the receptors of karrikins (KARs), which are derived from burnt vegetation and act as smoke stimulants of seed germination. Enormous progress has been made in the last decade with respect to molecular studies of the SL and KAR signaling pathways. The main axis of the signaling pathway is D14-D3/MAX2-D53/SMXL678 for SL and KAR-KAI2-D3/MAX2-SMAX1,2 for KAR. In these pathways, the main switch molecules are the hormone receptors, D14 and KAI2, which act as the input device of the pathway. The output device is the ubiquitylation substrate, being D53/SMXL678 for SL and SMAX1,2 for KAR signaling. Since D14 and KAI2 are not canonical hormone receptors but also are enzymes, an understanding of these proteins requires the acquisition and investigation of three-dimensional structures of higher-order complexes. The recent structure of the CLIM-D14-D3 complex has succeeded in shedding light on the mechanisms by which the chemical conversion of SL is able to switch on the signaling pathway. However, several fundamental issues remain to be solved in terms of molecular structures and chemistry.


  1. 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 50:1416–1424CrossRefPubMedGoogle Scholar
  2. 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 148:402–413CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39CrossRefPubMedGoogle Scholar
  4. 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
  5. Bythell-Douglas R, Waters MT, Scaffidi A, Flematti GR, Smith SM, Bond CS (2013) The structure of the karrikin-insensitive protein (KAI2) in Arabidopsis thaliana. PLoS One 8(1):e54758CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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
  7. 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
  8. de Saint Germain A, Clavé G, Badet-Denisot M-A, Pillot J-P, Cornu D, Le Caer J-P, Burger M, Pelissier F, Retailleau P, Turnbull C, Bonhomme S, Chory J, Rameau C, Boyer FD (2016) An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat Chem Biol 12:787–794CrossRefPubMedPubMedCentralGoogle Scholar
  9. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977–977CrossRefPubMedGoogle Scholar
  10. Flematti GR, Goddard-Borger ED, Merritt DJ, Ghisalberti EL, Dixon KW, Trengove RD (2007) Preparation of 2H-furo[2.3-c]pyran-2-one derivatives and evaluation of their germination-promoting activity. J Agric Food Chem 55:2189–2194CrossRefPubMedGoogle Scholar
  11. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2009) Identification of alkyl substituted 2H-furo[2.3-c]pyran-2-ones as germination stimulants present in smoke. J Agric Food Chem 57:9475–9480CrossRefPubMedGoogle Scholar
  12. Flematti GR, Scaffidi A, Goddard-Borger ED, Heath CH, Nelson DC, Commander LE, Stick RV, Dixon KW, Smith SM, Ghisalberti EL (2010) Structure-activity relationship of karrikin germination stimulants. J Agric Food Chem 58:8612–8617CrossRefPubMedGoogle Scholar
  13. Flematti GR, Scaffidi A, Dixon KW, Smith SM, Ghisalbert EL (2011) Production of the seed germination stimulant karrikinolide from combustion of simple carbohydrates. J Agric Food Chem 59:1195–1198CrossRefPubMedGoogle Scholar
  14. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194CrossRefPubMedGoogle Scholar
  15. Guo Y, Zheng Z, La Clair JJ, Chory J, Noel JP (2013) Smoke-derived karrikin perception by the alpha/beta-hydrolase KAI2 from Arabidopsis. Proc Natl Acad Sci U S A 110:8284–8289CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hamiaux C, Drummond RS, 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
  17. Heikinheimo P, Goldman A, Jeffries C, Ollis DL (1999) Of barn owls and bankers: a lush variety of α/β hydrolases. Struct Fold Des 7:R141–R146CrossRefGoogle Scholar
  18. 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
  19. 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) DWARF53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kagiyama M, Hirano Y, Mor 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 18:147–160CrossRefPubMedGoogle Scholar
  21. 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 139:920–934CrossRefPubMedPubMedCentralGoogle Scholar
  22. Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463CrossRefPubMedGoogle Scholar
  23. Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park SH, Miyauchi Y, Asano A, Totsuka N, Ueda T, Tanokura M, Asami T (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613CrossRefPubMedGoogle Scholar
  24. Nardini M, Dijkstra BW (1999) α/β hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9:732–737CrossRefPubMedGoogle Scholar
  25. Rittinger K, Walker PA, Eccleston JF, Smerdon SJ, Gamblin SJ (1997a) Structure at 1.65 a of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389:758–762CrossRefPubMedGoogle Scholar
  26. Rittinger K, Walker PA, Eccleston JF, Nurmahomed K, Owen D, Laue E, Gamblin SJ, Smerdon SJ (1997b) Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP. Nature 388:693–697CrossRefPubMedGoogle Scholar
  27. Sorefan K, Booker J, Haurogne 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
  28. 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 27:3143–3159CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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
  30. Stanga JP, Morffy N, Nelson DC (2016) Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta 243:1397–1406CrossRefPubMedGoogle Scholar
  31. Stirnberg P, van de Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141PubMedGoogle Scholar
  32. Tokunaga T, Hayashi H, Akiyama K (2015) Medicaol, a strigolactone identified as a putative didehydro-orobanchol isomer from Medicago truncatula. Phytochemistry 111:91–97CrossRefPubMedGoogle Scholar
  33. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698CrossRefPubMedGoogle Scholar
  34. 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
  35. Waters MT, Scaffidi A, Flematti G, Smith SM (2015a) Substrate-induced degradation of the α/β-fold hydrolase KARRIKIN INSENSITIVE2 requires a functional catalytic triad but is independent of MAX2. Mol Plant 8:814–817CrossRefPubMedGoogle Scholar
  36. Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015b) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:1925–1944CrossRefPubMedPubMedCentralGoogle Scholar
  37. Yamaguchi S, Kyozuka J (2010) Branching hormone is busy both underground and overground. Plant Cell Physiol 51:1091–1094CrossRefPubMedGoogle Scholar
  38. Yao R, Ming Z, Yan L, Li S, Wang F, Ma S, Yu C, Yang M, Chen L, Chen L, Li Y, Yan C, Miao D, Sun Z, Yan J, Sun Y, Wang L, Chu J, Fan S, He W, Deng H, Nan F, Li J, Rao Z, Lou Z, Xie D (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536:469–473CrossRefPubMedGoogle Scholar
  39. Yoneyama K, Awad AA, Xie X, Yoneyama K, Takeuchi Y (2010) Strigolactones as germination stimulants for root parasitic plants. Plant Cell Physiol 51:1095–1103CrossRefPubMedPubMedCentralGoogle Scholar
  40. Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH, Liu Y, Chen RZ, Kovach A, Kang Y, Hou L, He Y, Xie C, Song W, Zhong D, Xu Y, Wang Y, Li J, Zhang C, Melcher K, Xu HE (2013) Crystal structures of two phytohormone signal transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhao J, Wang T, Wang M, Liu Y, Yuan S, Gao Y, Yin L, Sun W, Peng L, Zhang W, Wan J, Li X (2014) DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol 55:1096–1109CrossRefPubMedGoogle Scholar
  42. Zhao LH, Zhou XE, Yi W, Wu Z, Liu Y, et al, Kang Y, Hou L, de Waal PW, Li S, Jiang Y, Scaffidi A, Flematti GR, Smith SM, Lam VQ, Griffin PR, Wang Y, Li J, Melcher K, Xu HE (2015) Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res 25:1219–1236Google Scholar
  43. 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
  44. Zwanenburg B, Pospíšil T (2013) Structure and activity of strigolactones: new plant hormones with a rich future. Mol Plant 6:38–62CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Structural Biology Laboratory, Nara Institute of Science and TechnologyTakayamaJapan

Personalised recommendations