Strigolactone Biosynthesis and Signal Transduction

  • Kun-Peng Jia
  • Changsheng Li
  • Harro J. Bouwmeester
  • Salim Al-BabiliEmail author


Strigolactones (SLs) are a group of carotenoid derivatives that act as a hormone regulating plant development and response to environmental stimuli. SLs are also released into soil as a signal indicating the presence of a host for symbiotic arbuscular mycorrhizal fungi and root parasitic weeds. In this chapter, we provide an overview on the enormous progress that has been recently made in elucidating SL biosynthesis and signal transduction. We describe the tailoring pathway from the carotenoid precursor to the central intermediate carlactone, highlighting the stereospecificity of the involved enzymes, the all-trans/9-cis-β-carotene isomerase (D27), the 9-cis-specific CAROTENOID CLEAVAGE DIOXYGENASE 7 (CCD7), as well as CCD8 and its unusual catalytic activity. We then outline the oxidation of carlactone by cytochrome P450 enzymes, such as the Arabidopsis MORE AXILLARY GROWTH 1 (MAX1), into different SLs and the role of other enzymes in generating this diversity, and discuss why plants produce many different SLs. This is followed by depicting hormonal and nutritional factors that regulate SL biosynthesis and release, and by a description of transport mechanisms. In the second part of our chapter, we focus on SL perception and signal transduction, describing the SL receptor DECREASED APICAL DOMINANCE 2 (DAD2)/DWARF14 (D14) and its unique features, the central function of protein degradation mediated by the F-box protein MAX2 and its homologs. We also discuss the latest advances in understanding how SLs regulate the transcription of target genes and the role of SMXL/D53 transcription inhibitors.


Strigolactone biosynthesis Carotenoids D27 CCD7 CCD8 Carlactone MAX1 Strigolactone signaling Strigolactone perception 



We thank Justine Braguy and Jianing Mi for assisting drawing the illustrations and their critical reading to the manuscript.


ABC transporter

ATP-binding cassette transporters, consisting of multi-subunits including transmembrane proteins and membrane-associated ATPases, with especially important roles in transport of plant secondary metabolites and hormones.

α/β-fold Hydrolase

A large, diverse superfamily of hydrolytic enzymes characterized by a core alpha-/beta-sheet, which contains eight beta strands connected by six alpha helices and a catalytic triad.


The oxidative cleavage products of carotenoids by CCDs or spontaneous oxidation.

Arbuscular mycorrhizal (AM) fungi

A class of symbiotic fungi of the phylum Glomeromycota, characterized by the formation of unique intracellular structures called arbuscules that receive organic carbon from the host and assist the plant in the acquisition of mineral nutrients through their associations with roots.


A lactone with a four-carbon heterocyclic ring structure. It is a common moiety in all SLs.

Canonical SLs

A subfamily of SLs characterized by the presence of a tricyclic lactone (ABC-ring) connected to a conserved butenolide ring (D-ring) via an enol ether bridge in R-configuration.


A core intermediate in the biosynthesis of SLs, generated by the sequential action of D27, CCD7, and CCD8 from all-trans-β-carotene.


A class of terpenoid pigments produced in plants, algae, and some bacteria. They fulfill essential functions in photosynthesis and serve as precursors of hormones and signaling molecules.

Carotenoid cleavage dioxygenases (CCDs)

A large family of non-heme iron (II)-dependent enzymes which break C=C double bonds in carotenoid or apocarotenoid backbone, leading to two carbonyl products.

Catalytic triad

A set of three coordinated amino acids comprising an acid, a base, and a nucleophile (often Asp, His, and Ser, respectively) found in the active site of hydrolases.

F-box protein

A component of the SCF-type E3 ubiquitin-protein ligase complexes, which are responsible for substrate recognition, polyubiquitination, and eventually protein degradation.


High-performance liquid chromatography, an analytical chemistry technique used to separate, identify, and quantify different compounds in a sample mixture, which relies on pumps to pass a pressurized liquid solvent containing the sample mixture through a column filled with a solid adsorbent material. Due to the slightly different interaction of each substance in the sample with the adsorbent material, different substances have different flow rates when flowing out of the column therefore leading to their separation.


Liquid chromatography-mass spectrometry, a commonly used technique in analytical chemistry to identify a chemical by combining liquid chromatography (LC) or high-performance liquid chromatography (HPLC) with the mass analysis capabilities of mass spectrometry (MS).

MEP pathway

2-C-Methyl-d-erythritol 4-phosphate pathway, a route for the biosynthesis of the isoprenoid precursor isopentenyl pyrophosphate (IPP), which starts with the condensation of pyruvate with D-glyceraldehyde phosphate. The MEP pathway is responsible for the synthesis of the isoprenoid building block IPP in bacteria and plastids.

Mevalonate pathway

A pathway for the synthesis of isopentenyl pyrophosphate (IPP) in the cytoplasm of eukaryotic cells, archaea, and some bacteria. The mevalonate pathway is initiated by the condensation of two molecules acetyl-CoA and is the source of IPP in the cytoplasm of eukaryotic cells.


Mass spectrometry, an analytical technique that ionizes chemical species by electrons, ions or photons, energetic neutral atoms, or heavy cluster ions and sorts the ions based on their mass-to-charge ratio (m/z) and to detect them qualitatively and quantitatively by their respective m/z and abundance.


The region of soil surrounding the roots, which is directly affected by root secretions and is enriched in soil microorganisms.


The lower part of the combined grafted plant.


The upper part of the combined grafted plant.


A class of terpenes formed by the condensation of three isoprene units and consisting of a C15 skeleton.

Non-canonical SLs

Subfamily of SLs that contain a variable second moiety instead of the tricyclic lactone connected to a conserved butenolide ring (D-ring) via an enol ether bridge in R-configuration.


  1. Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111:18084–18089PubMedCrossRefGoogle Scholar
  2. Abuauf H, Haider I, Jia K-P, Ablazov A, Mi J, Blilou I, Al-Babili S (2018) The Arabidopsis DWARF27 gene encodes an all-trans-/9-cis-β-carotene isomerase and is induced by auxin, abscisic acid and phosphate deficiency. Plant Sci 277:33–42PubMedCrossRefGoogle Scholar
  3. Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472PubMedPubMedCentralCrossRefGoogle Scholar
  4. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  5. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186PubMedCrossRefGoogle Scholar
  6. 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 416:289–296PubMedCrossRefGoogle Scholar
  7. 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 beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351PubMedCrossRefGoogle Scholar
  8. 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 51:1019–1029PubMedCrossRefGoogle Scholar
  9. 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 50:1416–1424PubMedCrossRefGoogle Scholar
  10. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321PubMedCrossRefGoogle Scholar
  11. Avendano-Vazquez AO, Cordoba E, Llamas E, San Roman C, Nisar N, De la Torre S, Ramos-Vega M, Gutierrez-Nava MD, Cazzonelli CI, Pogson BJ, Leon P (2014) An uncharacterized apocarotenoid-derived signal generated in zeta-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in arabidopsis. Plant Cell 26(6):2524–2537PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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 48:221Google Scholar
  13. Baz L, Mori N, Guo X, Jamil M, Kountche BA, Mi J, Jia K-P, Vermathen M, Akiyama K, Al-Babili S (2018) 3-Hydroxycarlactone, a novel product of the strigolactone biosynthesis core pathway. Mol Plant 11(10):1312–1314PubMedCrossRefGoogle Scholar
  14. Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea (action of genes Rms3 and Rms4). Plant Physiol 110:859–865PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154PubMedCrossRefGoogle Scholar
  16. Bonneau L, Huguet S, Wipf D, Pauly N, Truong HN (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytol 199:188–202PubMedCrossRefGoogle Scholar
  17. 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 14:1232–1238PubMedCrossRefGoogle Scholar
  18. 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 8:443–449PubMedCrossRefGoogle Scholar
  19. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host–parasitic plant interactions. Curr Opin Plant Biol 6:358–364PubMedCrossRefGoogle Scholar
  20. Braun N, de Saint Germain A, Pillot J-P, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158:225–238PubMedCrossRefGoogle Scholar
  21. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017PubMedCrossRefGoogle Scholar
  22. Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28PubMedCrossRefGoogle Scholar
  23. Brewer PB, Yoneyama K, Filardo F, Meyers E, Scaffidi A, Frickey T, Akiyama K, Seto Y, Dun EA, Cremer JE, Kerr SC, Waters MT, Flematti GR, Mason MG, Weiller G, Yamaguchi S, Nomura T, Smith SM, Yoneyama K, Beveridge CA (2016) LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 113:6301–6306PubMedCrossRefGoogle Scholar
  24. Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558PubMedCrossRefGoogle Scholar
  25. Bruno M, Al-Babili S (2016) On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27. Planta 243:1429–1440PubMedCrossRefGoogle Scholar
  26. Bruno M, Hofmann M, Vermathen M, Alder A, Beyer P, Al-Babili S (2014) On the substrate-and stereospecificity of the plant carotenoid cleavage dioxygenase 7. FEBS Lett 588:1802–1807PubMedCrossRefGoogle Scholar
  27. Bruno M, Beyer P, Al-Babili S (2015) The potato carotenoid cleavage dioxygenase 4 catalyzes a single cleavage of β-ionone ring-containing carotenes and non-epoxidated xanthophylls. Arch Biochem Biophys 572:126–133PubMedCrossRefGoogle Scholar
  28. Bruno M, Koschmieder J, Wuest F, Schaub P, Fehling-Kaschek M, Timmer J, Beyer P, Al-Babili S (2016) Enzymatic study on AtCCD4 and AtCCD7 and their potential to form acyclic regulatory metabolites. J Exp Bot 67:5993–6005PubMedPubMedCentralCrossRefGoogle Scholar
  29. Bruno M, Vermathen M, Alder A, Wüst F, Schaub P, Steen R, Beyer P, Ghisla S, Al-Babili S (2017) Insights into the formation of carlactone from in-depth analysis of the CCD8-catalyzed reactions. FEBS Lett 591:792–800PubMedCrossRefGoogle Scholar
  30. Butler LG (1995) Chemical communication between the parasitic weed striga and its crop host. ACS Symp Ser 582:158–168CrossRefGoogle Scholar
  31. Campbell R, Ducreux LJ, Morris WL, Morris JA, Suttle JC, Ramsay G, Bryan GJ, Hedley PE, Taylor MA (2010) The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato. Plant Physiol 154:656–664PubMedPubMedCentralCrossRefGoogle Scholar
  32. Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O (2013) A role for more axillary growth1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol 161:1885–1902PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chapple C (1998) Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu Rev Plant Biol 49:311–343CrossRefGoogle Scholar
  34. Charnikhova TV, Gaus K, Lumbroso A, Sanders M, Vincken J-P, De Mesmaeker A, Ruyter-Spira CP, Screpanti C, Bouwmeester HJ (2017) Zealactones. Novel natural strigolactones from maize. Phytochemistry 137:123–131PubMedCrossRefGoogle Scholar
  35. Charnikhova TV, Gaus K, Lumbroso A, Sanders M, Vincken J-P, De Mesmaeker A, Ruyter-Spira CP, Screpanti C, Bouwmeester HJ (2018) Zeapyranolactone − a novel strigolactone from maize. Phytochem Lett 24:172–178CrossRefGoogle Scholar
  36. Chhikara N, Kour R, Jaglan S, Gupta P, Gat Y, Panghal A (2018) Citrus medica: nutritional, phytochemical composition and health benefits–a review. Food Funct 9:1978–1992PubMedCrossRefGoogle Scholar
  37. 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 349:540–543PubMedCrossRefGoogle Scholar
  38. 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 154:1189–1190PubMedCrossRefPubMedCentralGoogle Scholar
  39. Cook C, Whichard LP, Wall M, Egley GH, Coggon P, Luhan PA, McPhail A (1972) Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J Am Chem Soc 94:6198–6199CrossRefGoogle Scholar
  40. Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b 6 f complex. Annu Rev Biochem 75:769–790PubMedCrossRefGoogle Scholar
  41. de Kraker J-W, Franssen MC, de Groot A, König WA, Bouwmeester HJ (1998) (+)-Germacrene A biosynthesis: the committed step in the biosynthesis of bitter sesquiterpene lactones in chicory. Plant Physiol 117:1381–1392PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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 (2016) An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat Chem Biol 12:787–794PubMedPubMedCentralCrossRefGoogle Scholar
  43. Decker EL, Alder A, Hunn S, Ferguson J, Lehtonen MT, Scheler B, Kerres KL, Wiedemann G, Safavi-Rizi V, Nordzieke S (2017) Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytol 216(2):455–468PubMedCrossRefPubMedCentralGoogle Scholar
  44. Delavault P, Simier P, Thoiron S, Véronési C, Fer A, Thalouarn P (2002) Isolation of mannose 6-phosphate reductase cDNA, changes in enzyme activity and mannitol content in broomrape (Orobanche ramosa) parasitic on tomato roots. Physiol Plant 115:48–55PubMedCrossRefGoogle Scholar
  45. DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738PubMedCrossRefGoogle Scholar
  46. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 26(435(7041)):441–445CrossRefGoogle Scholar
  47. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386(6624):485–488PubMedCrossRefGoogle Scholar
  48. Drummond RS, 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 151:1867–1877PubMedPubMedCentralCrossRefGoogle Scholar
  49. Drummond RS, 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 10(2):115Google Scholar
  50. Estrada AF, Maier D, Scherzinger D, Avalos J, Al-Babili S (2008) Novel apocarotenoid intermediates in Neurospora crassa mutants imply a new biosynthetic reaction sequence leading to neurosporaxanthin formation. Fungal Genet Biol 45:1497–1505PubMedCrossRefGoogle Scholar
  51. Flematti GR, Dixon KW, Smith SM (2015) What are karrikins and how were they ‘discovered’ by plants? BMC Biol 13:108PubMedPubMedCentralCrossRefGoogle Scholar
  52. Floss DS, Schliemann W, Schmidt J, Strack D, Walter MH (2008) RNA interference-mediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C27 apocarotenoids, shedding light on the functional role of CCD1. Plant Physiol 148:1267–1282PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 17:464–474PubMedPubMedCentralCrossRefGoogle Scholar
  54. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265PubMedCrossRefGoogle Scholar
  55. 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 21:4905–4908PubMedCrossRefGoogle Scholar
  56. Giuliano G, Al-Babili S, Von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149PubMedCrossRefGoogle Scholar
  57. Gobena D, Shimels M, Rich PJ, Ruyter-Spira C, Bouwmeester H, Kanuganti S, Mengiste T, Ejeta G (2017) Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. Proc Natl Acad Sci USA 114:4471–4476PubMedCrossRefGoogle Scholar
  58. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedCrossRefGoogle Scholar
  59. Gonzalez-Jorge S, Ha S-H, Magallanes-Lundback M, Gilliland LU, Zhou A, Lipka AE, Nguyen Y-N, Angelovici R, Lin H, Cepela J (2013) Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in Arabidopsis seeds. Plant Cell 25:4812–4826PubMedPubMedCentralCrossRefGoogle Scholar
  60. Goodwin TW (1988) Plant pigments. Academic Press, LondonGoogle Scholar
  61. Guan JC, Koch KE, Suzuki M, Wu S, Latshaw S, Petruff T, Goulet C, Klee HJ, McCarty DR (2012) Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork. Plant Physiol 160:1303–1317PubMedPubMedCentralCrossRefGoogle Scholar
  62. Guillotin B, Etemadi M, Audran C, Bouzayen M, Bécard G, Combier JP (2017) Sl-IAA27 regulates strigolactone biosynthesis and mycorrhization in tomato (var. MicroTom). New Phytol 213:1124–1132PubMedCrossRefGoogle Scholar
  63. 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 110:8284–8289PubMedCrossRefGoogle Scholar
  64. Gutjahr C (2014) Phytohormone signaling in arbuscular mycorrhiza development. Curr Opin Plant Biol 20:26–34PubMedCrossRefGoogle Scholar
  65. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617PubMedCrossRefGoogle Scholar
  66. Haider I, Andreo-Jimenez B, Bruno M, Bimbo A, Floková K, Abuauf H, Ntui VO, Guo X, Charnikhova T, Al-Babili S (2018) The interaction of strigolactones with abscisic acid during the drought response in rice. J Exp Bot 69:2403–2414PubMedGoogle Scholar
  67. 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 22:2032–2036PubMedCrossRefGoogle Scholar
  68. Hashimot H, Uragami C, Cogdell RJ (2016) Carotenoids and photosynthesis. In: Stange C (ed) Carotenoids in nature, Subcellular biochemistry, vol 79. Springer, ChamGoogle Scholar
  69. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412PubMedPubMedCentralCrossRefGoogle Scholar
  70. Hershko A, Ciechanover A (1998) The ubiquitin system. Ann Rev 67:425–479Google Scholar
  71. Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445PubMedCrossRefGoogle Scholar
  72. Huang F-C, Horváth G, Molnár P, Turcsi E, Deli J, Schrader J, Sandmann G, Schmidt H, Schwab W (2009) Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena. Phytochemistry 70:457–464PubMedCrossRefGoogle Scholar
  73. Ilg A, Yu Q, Schaub P, Beyer P, Al-Babili S (2010) Overexpression of the rice carotenoid cleavage dioxygenase 1 gene in Golden Rice endosperm suggests apocarotenoids as substrates in planta. Planta 232:691–699PubMedCrossRefGoogle Scholar
  74. Iseki M, Shida K, Kuwabara K, Wakabayashi T, Mizutani M, Takikawa H, Sugimoto Y (2018) Evidence for species-dependent biosynthetic pathways for converting carlactone to strigolactones in plants. J Exp Bot 69:2305–2318PubMedCrossRefGoogle Scholar
  75. 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 46:79–86PubMedCrossRefGoogle Scholar
  76. Isin EM, Guengerich FP (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim Biophys Acta Gen Subj 1770:314–329CrossRefGoogle Scholar
  77. Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, Yajima S, Kyozuka J, Ueguchi-Tanaka M, Matsuoka M (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol 174:1250–1259PubMedPubMedCentralCrossRefGoogle Scholar
  78. Jamil M, Rodenburg J, Charnikhova T, Bouwmeester HJ (2011) Pre-attachment Striga hermonthica resistance of New Rice for Africa (NERICA) cultivars based on low strigolactone production. New Phytol 192:964–975PubMedCrossRefGoogle Scholar
  79. Jamil M, Kanampiu F, Karaya H, Charnikhova T, Bouwmeester H (2012) Striga hermonthica parasitism in maize in response to N and P fertilisers. Field Crop Res 134:1–10CrossRefGoogle Scholar
  80. Jamil M, Van Mourik T, Charnikhova T, Bouwmeester H (2013) Effect of diammonium phosphate application on strigolactone production and Striga hermonthica infection in three sorghum cultivars. Weed Res 53:121–130CrossRefGoogle Scholar
  81. Jamil M, Kountche BA, Haider I, Guo X, Ntui VO, Jia K-P, Ali S, Hameed US, Nakamura H, Lyu Y (2017) Methyl phenlactonoates are efficient strigolactone analogs with simple structure. J Exp Bot 69(9):2319–2331PubMedCentralPubMedGoogle Scholar
  82. Jia KP, Kountche BA, Jamil M, Guo X, Ntui VO, Rüfenacht A, Rochange S, Al-Babili S (2016) Nitro-phenlactone, a carlactone analog with pleiotropic strigolactone activities. Mol Plant 9:1341–1344PubMedCrossRefGoogle Scholar
  83. Jia KP, Baz L, Al-Babili S (2018) From carotenoids to strigolactones. J Exp Bot 69(9):2189–2204PubMedCrossRefGoogle Scholar
  84. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401PubMedPubMedCentralCrossRefGoogle Scholar
  85. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541PubMedCrossRefGoogle Scholar
  86. 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 142:1014–1026PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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 18:147–160PubMedCrossRefGoogle Scholar
  88. Katsir L, Chung HS, Koo AJ, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ke J, Ma H, Gu X, Thelen A, Brunzelle JS, Li J, Xu HE, Melcher K (2015) Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Sci Adv 1:e1500107PubMedPubMedCentralCrossRefGoogle Scholar
  90. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446PubMedCrossRefGoogle Scholar
  91. Khosla A, Nelson DC (2016) Strigolactones, super hormones in the fight against Striga. Curr Opin Plant Biol 33:57–63PubMedCrossRefGoogle Scholar
  92. Kim HI, Kisugi T, Khetkam P, Xie X, Yoneyama K, Uchida K, Yokota T, Nomura T, McErlean CS, Yoneyama K (2014) Avenaol, a germination stimulant for root parasitic plants from Avena strigosa. Phytochemistry 103:85–88PubMedCrossRefGoogle Scholar
  93. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester HJ, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in non-AM host Arabidopsis thaliana. Plant Physiol 110:164640Google Scholar
  94. Kohlen W, Charnikhova T, Bours R, López-Ráez JA, Bouwmeester H (2013) Tomato strigolactones: a more detailed look. Proc Natl Acad Sci USA 8:e22785Google Scholar
  95. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549PubMedCrossRefGoogle Scholar
  96. 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 483:341–344PubMedCrossRefGoogle Scholar
  97. Lakshminarayana R, Raju M, Krishnakantha TP, Baskaran V (2005) Determination of major carotenoids in a few Indian leafy vegetables by high-performance liquid chromatography. J Agric Food Chem 53:2838–2842PubMedCrossRefGoogle Scholar
  98. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525PubMedPubMedCentralCrossRefGoogle Scholar
  99. Liu J, He H, Vitali M, Visentin I, Charnikhova T, Haider I, Schubert A, Ruyter-Spira C, Bouwmeester HJ, Lovisolo C (2015) Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241:1435–1451PubMedCrossRefGoogle Scholar
  100. Lopez-Raez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TD, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187:343–354PubMedCrossRefGoogle Scholar
  101. Ma G, Zhang L, Matsuta A, Matsutani K, Yamawaki K, Yahata M, Wahyudi A, Motohashi R, Kato M (2013) Enzymatic formation of β-citraurin from β-cryptoxanthin and zeaxanthin by carotenoid cleavage dioxygenase4 in the flavedo of citrus fruit. Plant Physiol 163:682–695PubMedPubMedCentralCrossRefGoogle Scholar
  102. Maass D, Arango J, Wüst F, Beyer P, Welsch R (2009) Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS One 4:e6373PubMedPubMedCentralCrossRefGoogle Scholar
  103. 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 73:2460–2465PubMedCrossRefGoogle Scholar
  104. Matusova R, Rani K, Verstappen FW, Franssen MC, 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 139:920–934PubMedPubMedCentralCrossRefGoogle Scholar
  105. Medina HR, Cerdá-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82:199–208PubMedCrossRefGoogle Scholar
  106. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135PubMedPubMedCentralCrossRefGoogle Scholar
  107. Miura K, Ikeda M, Matsubara A, Song X-J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545PubMedCrossRefGoogle Scholar
  108. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80PubMedCrossRefGoogle Scholar
  109. Moise AR, Von Lintig J, Palczewski K (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci 10:178–186PubMedCrossRefGoogle Scholar
  110. Moise AR, Al-Babili S, Wurtzel ET (2014) Mechanistic aspects of carotenoid biosynthesis. Chem Rev 114:164–193PubMedCrossRefGoogle Scholar
  111. Morris SE, Turnbull CG, Murfet IC, Beveridge CA (2001) Mutational analysis of branching in pea. Evidence ThatRms1 and Rms5 regulate the same novel signal. Plant Physiol 126:1205–1213PubMedPubMedCentralCrossRefGoogle Scholar
  112. Motonami N, Ueno K, Nakashima H, Nomura S, Mizutani M, Takikawa H, Sugimoto Y (2013) The bioconversion of 5-deoxystrigol to sorgomol by the sorghum, Sorghum bicolor (L.) Moench. Phytochemistry 93:41–48PubMedCrossRefGoogle Scholar
  113. Nakamura H, Xue Y-L, Miyakawa T, Hou F, Qin H-M, Fukui K, Shi X, Ito E, Ito S, Park S-H (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613PubMedCrossRefGoogle Scholar
  114. Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, Smith SM (2009) Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol 149:863–873PubMedPubMedCentralCrossRefGoogle Scholar
  115. Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:7095–7100PubMedCrossRefGoogle Scholar
  116. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82PubMedCrossRefGoogle Scholar
  117. Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201PubMedPubMedCentralCrossRefGoogle Scholar
  118. Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459PubMedCrossRefGoogle Scholar
  119. Parry AD, Horgan R (1992) Abscisic acid biosynthesis in roots. Planta 187:185–191PubMedCrossRefGoogle Scholar
  120. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788PubMedPubMedCentralCrossRefGoogle Scholar
  121. Rodrigo MJ, Alquézar B, Alós E, Medina V, Carmona L, Bruno M, Al-Babili S, Zacarías L (2013) A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments. J Exp Bot 64:4461–4478PubMedPubMedCentralCrossRefGoogle Scholar
  122. Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158PubMedPubMedCentralCrossRefGoogle Scholar
  123. Ruyter-Spira C, Al-Babili S, Van Der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83PubMedCrossRefGoogle Scholar
  124. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 4(7):571Google Scholar
  125. Samodelov SL, Beyer HM, Guo X, Augustin M, Jia K-P, Baz L, Ebenhöh O, Beyer P, Weber W, Al-Babili S (2016) StrigoQuant: a genetically encoded biosensor for quantifying strigolactone activity and specificity. Sci Adv 2.:e1601266:1–8CrossRefGoogle Scholar
  126. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071PubMedCrossRefGoogle Scholar
  127. Sasse J, Simon S, Gubeli C, Liu GW, 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 25:647–655PubMedCrossRefGoogle Scholar
  128. 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 165:1221–1232PubMedPubMedCentralCrossRefGoogle Scholar
  129. Scherzinger D, Al-Babili S (2008) In vitro characterization of a carotenoid cleavage dioxygenase from Nostoc sp. PCC 7120 reveals a novel cleavage pattern, cytosolic localization and induction by highlight. Mol Microbiol 69:231–244PubMedCrossRefGoogle Scholar
  130. Schlicht M, Šamajová O, Schachtschabel D, Mancuso S, Menzel D, Boland W, Baluška F (2008) D’orenone blocks polarized tip growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex. Plant J 55:709–717PubMedCrossRefGoogle Scholar
  131. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874PubMedCrossRefGoogle Scholar
  132. 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 279:46940–46945PubMedCrossRefGoogle Scholar
  133. 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 111:1640–1645PubMedCrossRefGoogle Scholar
  134. Shen H, Zhu L, Bu QY, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5:750–762PubMedCrossRefGoogle Scholar
  135. Shu K, Yang W (2017) E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol 58:1461–1476PubMedPubMedCentralCrossRefGoogle Scholar
  136. Siame BA, 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 41:1486–1491CrossRefGoogle Scholar
  137. Simons JL, Napoli CA, Janssen BJ, Plummer KM, Snowden KC (2007) Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol 143:697–706PubMedPubMedCentralCrossRefGoogle Scholar
  138. 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 17:746–759PubMedPubMedCentralCrossRefGoogle Scholar
  139. Song X, Lu Z, Yu H, Shao G, Xiong J, Meng X, Jing Y, Liu G, Xiong G, Duan J (2017) IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 27:1128PubMedPubMedCentralCrossRefGoogle Scholar
  140. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474PubMedPubMedCentralCrossRefGoogle Scholar
  141. 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 27:3143–3159PubMedPubMedCentralCrossRefGoogle Scholar
  142. 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 163:318–330PubMedPubMedCentralCrossRefGoogle Scholar
  143. Stauder R, Welsch R, Camagna M, Kohlen W, Balcke GU, Tissier A, Walter MH (2018) Strigolactone levels in dicot roots are determined by an ancestral symbiosis-regulated clade of the PHYTOENE SYNTHASE Gene Family. Front Plant Sci 9:255PubMedPubMedCentralCrossRefGoogle Scholar
  144. Stirnberg P, van De Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141PubMedGoogle Scholar
  145. Stirnberg P, Furner IJ, Ottoline Leyser H (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94PubMedCrossRefGoogle Scholar
  146. 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(22):6735–6746PubMedPubMedCentralCrossRefGoogle Scholar
  147. Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520PubMedCrossRefGoogle Scholar
  148. Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240PubMedCrossRefGoogle Scholar
  149. Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15:211–216PubMedCrossRefGoogle Scholar
  150. Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S, Holbrook-Smith D, Zhang H, McCourt P, Itami K, Kinoshita T (2015) Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–868PubMedCrossRefGoogle Scholar
  151. Ueguchi-Tanaka M, Matsuoka M (2010) The perception of gibberellins: clues from receptor structure. Curr Opin Plant Biol 13:503–508PubMedCrossRefGoogle Scholar
  152. 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 59:10485–10490PubMedCrossRefGoogle Scholar
  153. Ueno K, Furumoto T, Umeda S, Mizutani M, Takikawa H, Batchvarova R, Sugimoto Y (2014) Heliolactone, a non-sesquiterpene lactone germination stimulant for root parasitic weeds from sunflower. Phytochemistry 108:122–128PubMedCrossRefGoogle Scholar
  154. 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 455:195–200PubMedCrossRefPubMedCentralGoogle Scholar
  155. 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 51:1118–1126PubMedPubMedCentralCrossRefGoogle Scholar
  156. Van Ha C, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA 111:851–856PubMedCrossRefGoogle Scholar
  157. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay R, Pandey M (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161PubMedPubMedCentralGoogle Scholar
  158. Wallner E-S, López-Salmerón V, Belevich I, Poschet G, Jung I, Grünwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y (2017) Strigolactone-and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr Biol 27:1241–1247PubMedPubMedCentralCrossRefGoogle Scholar
  159. Walter MH (2013) Role of carotenoid metabolism in the arbuscular mycorrhizal symbiosis. In: Molecular microbial ecology of the rhizosphere, vol 1 & 2. Wiley, Hoboken, NJ, pp 513–524CrossRefGoogle Scholar
  160. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692PubMedCrossRefPubMedCentralGoogle Scholar
  161. Wang Y, Bouwmeester HJ (2018) Structural diversity in the strigolactones. J Exp Bot 69:2219–2230PubMedCrossRefGoogle Scholar
  162. Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8:677–688PubMedCrossRefGoogle Scholar
  163. 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 27:3128–3142PubMedPubMedCentralCrossRefGoogle Scholar
  164. 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 159:1073–1085PubMedPubMedCentralCrossRefGoogle Scholar
  165. 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 139:1285–1295PubMedCrossRefPubMedCentralGoogle Scholar
  166. Waters MT, Scaffidi A, Flematti GR, Smith SM (2013) The origins and mechanisms of karrikin signalling. Curr Opin Plant Biol 16:667–673PubMedCrossRefGoogle Scholar
  167. Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (2014) The karrikin response system of Arabidopsis. Plant J 79:623–631PubMedCrossRefGoogle Scholar
  168. Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322PubMedCrossRefPubMedCentralGoogle Scholar
  169. Wen C, Zhao Q, Nie J, Liu G, Shen L, Cheng C, Xi L, Ma N, Zhao L (2016) Physiological controls of chrysanthemum DgD27 gene expression in regulation of shoot branching. Plant Cell Rep 35:1053–1070PubMedCrossRefGoogle Scholar
  170. Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1:Reviews3003. 3001CrossRefGoogle Scholar
  171. Xie X (2016) Structural diversity of strigolactones and their distribution in the plant kingdom. J Pestic Sci 41:175–180PubMedPubMedCentralCrossRefGoogle Scholar
  172. 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 Agri Food Chem 55:8067–8072CrossRefGoogle Scholar
  173. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Takeuchi Y, Sugimoto Y, Yoneyama K (2008) Sorgomol, germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Lett 49:2066–2068CrossRefGoogle Scholar
  174. 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 70:211–215PubMedCrossRefGoogle Scholar
  175. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117PubMedCrossRefGoogle Scholar
  176. 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
  177. Xie X, Kisugi T, Yoneyama K, Nomura T, Akiyama K, Uchida K, Yokota T, McErlean CS, Yoneyama K (2017) Methyl zealactonoate, a novel germination stimulant for root parasitic weeds produced by maize. J Pestic Sci 42:58–61PubMedPubMedCentralCrossRefGoogle Scholar
  178. 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 536:469–473PubMedCrossRefGoogle Scholar
  179. Yao R, Wang F, Ming Z, Du X, Chen L, Wang Y, Zhang W, Deng H, Xie D (2017) ShHTL7 is a non-canonical receptor for strigolactones in root parasitic weeds. Cell Res 27(6):838–841PubMedPubMedCentralCrossRefGoogle Scholar
  180. Yasuda N, Sugimoto Y, Kato M, Inanaga S, Yoneyama K (2003) (+)-Strigol, a witchweed seed germination stimulant, from Menispermum dauricum root culture. Phytochemistry 62:1115–1119PubMedCrossRefGoogle Scholar
  181. 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 49:1967–1973CrossRefGoogle Scholar
  182. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) 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 227:125–132PubMedCrossRefGoogle Scholar
  183. Yoneyama K, Kisugi T, Xie X, Yoneyama K (2013) Chemistry of strigolactones: why and how do plants produce so many strigolactones? In: Molecular microbial ecology of the rhizosphere, vol 1 & 2. Wiley, Hoboken, NJ, pp 373–379CrossRefGoogle Scholar
  184. Yoneyama K, Arakawa R, Ishimoto K, Kim HI, Kisugi T, Xie X, Nomura T, Kanampiu F, Yokota T, Ezawa T (2015) Difference in striga-susceptibility is reflected in strigolactone secretion profile, but not in compatibility and host preference in arbuscular mycorrhizal symbiosis in two maize cultivars. New Phytol 206:983–989PubMedCrossRefGoogle Scholar
  185. Yoneyama K, Mori N, Sato T, Yoda A, Xie X, Okamoto M, Iwanaga M, Ohnishi T, Nishiwaki H, Asami T (2018) Conversion of carlactone to carlactonoic acid is a conserved function of MAX 1 homologs in strigolactone biosynthesis. New Phytol 218:1522–1533PubMedCrossRefGoogle Scholar
  186. Zhang Y, van Dijk AD, Scaffidi A, Flematti GR, Hofmann M, Charnikhova T, Verstappen F, Hepworth J, van der Krol S, Leyser O, Smith SM, Zwanenburg B, Al-Babili S, Ruyter-Spira C, Bouwmeester HJ (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033PubMedCrossRefGoogle Scholar
  187. Zhang Y, Cheng X, Wang Y, Diez-Simon C, Flokova K, Bimbo A, Bouwmeester HJ, Ruyter-Spira C (2018) The tomato MAX1 homolog, SlMAX1, is involved in the biosynthesis of tomato strigolactones from carlactone. New Phytol 219(1):297–309PubMedCrossRefGoogle Scholar
  188. 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 alpha/beta hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439PubMedPubMedCentralCrossRefGoogle Scholar
  189. 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-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kun-Peng Jia
    • 1
  • Changsheng Li
    • 2
  • Harro J. Bouwmeester
    • 2
  • Salim Al-Babili
    • 1
    Email author
  1. 1.The BioActives LabThe King Abdullah University of Science and Technology (KAUST)ThuwalSaudi Arabia
  2. 2.Plant Hormone Biology Group, Swammerdam Institute for Life SciencesUniversity of AmsterdamAmsterdamThe Netherlands

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