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Strigolactone Biosynthesis and Signal Transduction

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Book cover Strigolactones - Biology and Applications

Abstract

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.

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References

  • 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 111:18084–18089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 277:33–42

    Article  CAS  PubMed  Google Scholar 

  • Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186

    Article  CAS  PubMed  Google Scholar 

  • 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 416:289–296

    Article  CAS  PubMed  Google Scholar 

  • 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 335:1348–1351

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1019–1029

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321

    Article  CAS  PubMed  Google Scholar 

  • 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):2524–2537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Awad AA, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48:221

    CAS  Google Scholar 

  • 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):1312–1314

    Article  CAS  PubMed  Google Scholar 

  • Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea (action of genes Rms3 and Rms4). Plant Physiol 110:859–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154

    Article  CAS  PubMed  Google Scholar 

  • 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 199:188–202

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host–parasitic plant interactions. Curr Opin Plant Biol 6:358–364

    Article  CAS  PubMed  Google Scholar 

  • 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 158:225–238

    Article  CAS  PubMed  Google Scholar 

  • 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 64:1002–1017

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28

    Article  CAS  PubMed  Google Scholar 

  • 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 113:6301–6306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558

    Article  CAS  PubMed  Google Scholar 

  • Bruno M, Al-Babili S (2016) On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27. Planta 243:1429–1440

    Article  CAS  PubMed  Google Scholar 

  • 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 588:1802–1807

    Article  CAS  PubMed  Google Scholar 

  • 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 572:126–133

    Article  CAS  PubMed  Google Scholar 

  • 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 67:5993–6005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 591:792–800

    Article  CAS  PubMed  Google Scholar 

  • Butler LG (1995) Chemical communication between the parasitic weed striga and its crop host. ACS Symp Ser 582:158–168

    Article  CAS  Google Scholar 

  • 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 154:656–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 161:1885–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapple C (1998) Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu Rev Plant Biol 49:311–343

    Article  CAS  Google Scholar 

  • 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 137:123–131

    Article  CAS  PubMed  Google Scholar 

  • 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 24:172–178

    Article  CAS  Google Scholar 

  • 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 9:1978–1992

    Article  CAS  PubMed  Google Scholar 

  • 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 349:540–543

    Article  CAS  PubMed  Google Scholar 

  • 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 154:1189–1190

    Article  CAS  PubMed  Google Scholar 

  • 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 94:6198–6199

    Article  CAS  Google Scholar 

  • Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b 6 f complex. Annu Rev Biochem 75:769–790

    Article  CAS  PubMed  Google Scholar 

  • 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 117:1381–1392

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 12:787–794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):455–468

    Article  CAS  PubMed  Google Scholar 

  • 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 115:48–55

    Article  CAS  PubMed  Google Scholar 

  • DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 26(435(7041)):441–445

    Article  CAS  Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386(6624):485–488

    Article  CAS  PubMed  Google Scholar 

  • 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 151:1867–1877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):115

    Google Scholar 

  • 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 45:1497–1505

    Article  CAS  PubMed  Google Scholar 

  • Flematti GR, Dixon KW, Smith SM (2015) What are karrikins and how were they ‘discovered’ by plants? BMC Biol 13:108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 148:1267–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:464–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Giuliano G, Al-Babili S, Von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149

    Article  CAS  PubMed  Google Scholar 

  • 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 114:4471–4476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 455:189–194

    Article  CAS  PubMed  Google Scholar 

  • 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 25:4812–4826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodwin TW (1988) Plant pigments. Academic Press, London

    Google Scholar 

  • 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 160:1303–1317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 213:1124–1132

    Article  CAS  PubMed  Google Scholar 

  • 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 110:8284–8289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutjahr C (2014) Phytohormone signaling in arbuscular mycorrhiza development. Curr Opin Plant Biol 20:26–34

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    Article  CAS  PubMed  Google Scholar 

  • 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 69:2403–2414

    CAS  PubMed  Google Scholar 

  • 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 22:2032–2036

    Article  CAS  PubMed  Google Scholar 

  • Hashimot H, Uragami C, Cogdell RJ (2016) Carotenoids and photosynthesis. In: Stange C (ed) Carotenoids in nature, Subcellular biochemistry, vol 79. Springer, Cham

    Google Scholar 

  • Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Ann Rev 67:425–479

    CAS  Google Scholar 

  • Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445

    Article  CAS  PubMed  Google Scholar 

  • 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 70:457–464

    Article  CAS  PubMed  Google Scholar 

  • 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 232:691–699

    Article  CAS  PubMed  Google Scholar 

  • 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 69:2305–2318

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Isin EM, Guengerich FP (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim Biophys Acta Gen Subj 1770:314–329

    Article  CAS  Google Scholar 

  • 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 174:1250–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 192:964–975

    Article  CAS  PubMed  Google Scholar 

  • 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 134:1–10

    Article  Google Scholar 

  • 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 53:121–130

    Article  CAS  Google Scholar 

  • 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):2319–2331

    PubMed Central  Google Scholar 

  • 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 9:1341–1344

    Article  CAS  PubMed  Google Scholar 

  • Jia KP, Baz L, Al-Babili S (2018) From carotenoids to strigolactones. J Exp Bot 69(9):2189–2204

    Article  CAS  PubMed  Google Scholar 

  • 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 504:401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 42:541

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Katsir L, Chung HS, Koo AJ, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1500107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446

    Article  CAS  PubMed  Google Scholar 

  • Khosla A, Nelson DC (2016) Strigolactones, super hormones in the fight against Striga. Curr Opin Plant Biol 33:57–63

    Article  CAS  PubMed  Google Scholar 

  • 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 103:85–88

    Article  CAS  PubMed  Google Scholar 

  • 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 110:164640

    Google Scholar 

  • Kohlen W, Charnikhova T, Bours R, López-Ráez JA, Bouwmeester H (2013) Tomato strigolactones: a more detailed look. Proc Natl Acad Sci USA 8:e22785

    Google Scholar 

  • Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190:545–549

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 53:2838–2842

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1512–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 241:1435–1451

    Article  CAS  PubMed  Google Scholar 

  • 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 187:343–354

    Article  CAS  PubMed  Google Scholar 

  • 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 163:682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e6373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 73:2460–2465

    Article  CAS  PubMed  Google Scholar 

  • 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 139:920–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina HR, Cerdá-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82:199–208

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1127–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 42:545

    Article  CAS  PubMed  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    Article  CAS  PubMed  Google Scholar 

  • Moise AR, Von Lintig J, Palczewski K (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci 10:178–186

    Article  CAS  PubMed  Google Scholar 

  • Moise AR, Al-Babili S, Wurtzel ET (2014) Mechanistic aspects of carotenoid biosynthesis. Chem Rev 114:164–193

    Article  CAS  PubMed  Google Scholar 

  • 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 126:1205–1213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 93:41–48

    Article  CAS  PubMed  Google Scholar 

  • 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 4:2613

    Article  PubMed  CAS  Google Scholar 

  • 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 149:863–873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107:7095–7100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82

    Article  CAS  PubMed  Google Scholar 

  • 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 142:1193–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459

    Article  CAS  PubMed  Google Scholar 

  • Parry AD, Horgan R (1992) Abscisic acid biosynthesis in roots. Planta 187:185–191

    Article  CAS  PubMed  Google Scholar 

  • 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 464:788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 64:4461–4478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruyter-Spira C, Al-Babili S, Van Der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83

    Article  CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 4(7):571

    Google Scholar 

  • 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.:e1601266:1–8

    Article  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071

    Article  CAS  PubMed  Google Scholar 

  • 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 25:647–655

    Article  CAS  PubMed  Google Scholar 

  • 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 165:1221–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 69:231–244

    Article  CAS  PubMed  Google Scholar 

  • 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 55:709–717

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 111:1640–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen H, Zhu L, Bu QY, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5:750–762

    Article  PubMed  CAS  Google Scholar 

  • Shu K, Yang W (2017) E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol 58:1461–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 41:1486–1491

    Article  CAS  Google Scholar 

  • 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 143:697–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:746–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 27:1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:1469–1474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 27:3143–3159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 163:318–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:255

    Article  PubMed  PubMed Central  Google Scholar 

  • Stirnberg P, van De Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141

    CAS  PubMed  Google Scholar 

  • 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 50:80–94

    Article  CAS  PubMed  Google Scholar 

  • 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):6735–6746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:513–520

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15:211–216

    Article  CAS  PubMed  Google Scholar 

  • 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 349:864–868

    Article  CAS  PubMed  Google Scholar 

  • Ueguchi-Tanaka M, Matsuoka M (2010) The perception of gibberellins: clues from receptor structure. Curr Opin Plant Biol 13:503–508

    Article  CAS  PubMed  Google Scholar 

  • 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 59:10485–10490

    Article  CAS  PubMed  Google Scholar 

  • 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 108:122–128

    Article  CAS  PubMed  Google Scholar 

  • 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 455:195–200

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1118–1126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 111:851–856

    Article  PubMed  CAS  Google Scholar 

  • 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 8:161

    PubMed  PubMed Central  Google Scholar 

  • 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 27:1241–1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 513–524

    Chapter  Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Bouwmeester HJ (2018) Structural diversity in the strigolactones. J Exp Bot 69:2219–2230

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Wang H (2015) The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8:677–688

    Article  CAS  PubMed  Google Scholar 

  • 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 27:3128–3142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Scaffidi A, Flematti GR, Smith SM (2013) The origins and mechanisms of karrikin signalling. Curr Opin Plant Biol 16:667–673

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (2014) The karrikin response system of Arabidopsis. Plant J 79:623–631

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322

    Article  CAS  PubMed  Google Scholar 

  • 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 35:1053–1070

    Article  CAS  PubMed  Google Scholar 

  • Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1:Reviews3003. 3001

    Article  Google Scholar 

  • Xie X (2016) Structural diversity of strigolactones and their distribution in the plant kingdom. J Pestic Sci 41:175–180

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 55:8067–8072

    Article  CAS  Google Scholar 

  • 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 49:2066–2068

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117

    Article  CAS  PubMed  Google Scholar 

  • 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 40:214–216

    Article  CAS  Google Scholar 

  • 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 42:58–61

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 536:469–473

    Article  CAS  PubMed  Google Scholar 

  • 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):838–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuda N, Sugimoto Y, Kato M, Inanaga S, Yoneyama K (2003) (+)-Strigol, a witchweed seed germination stimulant, from Menispermum dauricum root culture. Phytochemistry 62:1115–1119

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 227:125–132

    Article  CAS  PubMed  Google Scholar 

  • 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 373–379

    Chapter  Google Scholar 

  • 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 206:983–989

    Article  CAS  PubMed  Google Scholar 

  • 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 218:1522–1533

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1028–1033

    Article  PubMed  CAS  Google Scholar 

  • 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):297–309

    Article  CAS  PubMed  Google Scholar 

  • 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 23:436–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 504:406–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgment

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

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Correspondence to Salim Al-Babili .

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Glossary

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.

Apocarotenoids

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.

Butenolide

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.

Carlactone

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

Carotenoids

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.

HPLC

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.

LC-MS

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.

MS

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.

Rhizosphere

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

Rootstock

The lower part of the combined grafted plant.

Scion

The upper part of the combined grafted plant.

Sesquiterpenes

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.

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Jia, KP., Li, C., Bouwmeester, H.J., Al-Babili, S. (2019). Strigolactone Biosynthesis and Signal Transduction. In: Koltai, H., Prandi, C. (eds) Strigolactones - Biology and Applications. Springer, Cham. https://doi.org/10.1007/978-3-030-12153-2_1

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