Abstract
Apocarotenoids are tailored from carotenoids by oxidative enzymes [carotenoid cleavage oxygenases (CCOs)], cleaving specific double bonds of the polyene chain. The cleavage products can act as hormones, signaling compounds, chromophores and scent/aroma constituents. Recent advances were the identification of strigolactones as apocarotenoids and the description of their novel role as shoot branching inhibitor hormones. Strigolactones are also involved in plant signaling to both harmful (parasitic weeds) and beneficial [arbuscular mycorrhizal (AM) fungi] rhizosphere residents. This review describes the progress in the characterization of CCOs, termed CCDs and NCEDs, in plants. It highlights the importance of sequential cleavage reactions of C40 carotenoid precursors, the apocarotenoid cleavage oxygenase (ACO) nature of several CCOs and the topic of compartmentation. Work on the biosynthesis of abundant C13 cyclohexenone and C14 mycorradicin apocarotenoids in mycorrhizal roots has revealed a new role of CCD1 as an ACO of C27 apocarotenoid intermediates, following their predicted export from plastid to cytosol. Manipulation of the AM-induced apocarotenoid pathway further suggests novel roles of C13 apocarotenoids in controlling arbuscule turnover in the AM symbiosis. CCD7 has been established as a biosynthetic crosspoint, controlling both strigolactone and AM-induced C13 apocarotenoid biosynthesis. Interdependence of the two apocarotenoid pathways may thus play a role in AM-mediated reduction of parasitic weed infestations. Potential scenarios of C13 scent/aroma volatile biogenesis are discussed, including the novel mechanism revealed from mycorrhizal roots. The recent progress in apocarotenoid research opens up new perspectives for fundamental work, but has also great application potential for the horticulture, food and fragrance industries.
Similar content being viewed by others
Abbreviations
- ACO:
-
Apocarotenoid cleavage oxygenase
- AM:
-
Arbuscular mycorrhiza(l)
- CCD:
-
Carotenoid cleavage dioxygenase
- CCO:
-
Carotenoid cleavage oxygenase
- MEP:
-
Methylerythritol phosphate
- DXS:
-
1-Deoxy-d-xylulose 5-phosphate synthase
- NCED:
-
Nine-cis-epoxycarotenoid dioxygenase
References
Ahrazem O, Rubio-Moraga A, Lopez RC, Gomez-Gomez L (2010) The expression of a chromoplast-specific lycopene beta cyclase gene is involved in the high production of saffron’s apocarotenoid precursors. J Exp Bot 61:105–119
Akiyama K (2007) Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis. Biosci Biotechnol Biochem 71:1405–1414
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
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
Alder A, Bigler P, Werck-Reichhart D, Al-Babili S (2009) In vitro characterization of Synechocystis CYP120A1 revealed the first nonanimal retinoic acid hydroxylase. FEBS J 276:5416–5431
Alexander T, Meier R, Toth R, Weber HC (1988) Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L. New Phytol 110:363–370
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
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
Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006a) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993
Auldridge ME, McCarty DR, Klee HJ (2006b) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321
Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39
Beveridge CA, Dun EA, Rameau C (2009) Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol 151:985–990
Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser C (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238
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
Bouvier F, Dogbo O, Camara B (2003a) Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science 300:2089–2091
Bouvier F, Suire C, Mutterer J, Camara B (2003b) Oxidative remodeling of chromoplast carotenoids: Identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in crocus secondary metabolite biogenesis. Plant Cell 15:47–62
Bouvier F, Isner JC, Dogbo O, Camara B (2005) Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci 10:187–194
Bouwmeester HJ, Matusova R, Sun ZK, Beale MH (2003) Secondary metabolite signalling in host–parasitic plant interactions. Curr Opin Plant Biol 6:358–364
Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304
Burmester A, Richter M, Schultze K, Voelz K, Schachtschabel D, Boland W, Wostemeyer J, Schimek C (2007) Cleavage of beta-carotene as the first step in sexual hormone synthesis in zygomycetes is mediated by a trisporic acid regulated beta-carotene oxygenase. Fungal Genet Biol 44:1096–1108
Chandler JW (2009) Auxin as compère in plant hormone crosstalk. Planta 231:1–12
Cook CE, Whichard LP, Turner B, Wall ME (1966) Germination of witchweed (Striga lutea Lour)—isolation and properties of a potent stimulant. Science 154:1189–1190
Cook CE, Coggon P, McPhail AT, Wall ME, Whichard LP, Egley GH, Luhan PA (1972) Germination stimulants. 2. Structure of strigol—potent seed-germination stimulant for witchweed (Striga lutea Lour). J Am Chem Soc 94:6198–6199
Cooper CM, Davies NW, Menary RC (2003) C-27 apocarotenoids in the flowers of Boronia megastigma (Nees). J Agric Food Chem 51:2384–2389
Cooper CM, Davies NW, Menary RC (2009) Changes in some carotenoids and apocarotenoids during flower development in Boronia megastigma (Nees). J Agric Food Chem 57:1513–1520
Cox G, Sanders F (1974) Ultrastructure of host–fungus interface in a vesicular-arbuscular mycorrhiza. New Phytol 73:901–912
Drummond RSM, Martinez-Sanchez 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
Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14:364–372
Estrada AF, Brefort T, Mengel C, Diaz-Sanchez V, Alder A, Al-Babili S, Avalos J (2009) Ustilago maydis accumulates beta-carotene at levels determined by a retinal-forming carotenoid oxygenase. Fungal Genet Biol 46:803–813
Eugster CH, Märki-Fischer E (1991) The chemistry of rose pigments. Angew Chem Int Edit 30:654–672
Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hanse G, Strack D (2002) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43:256–265
Floss DS, Walter MH (2009) Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Sign Behav 4:172–175
Floss DS, Hause B, Lange PR, Kuster H, Strack D, Walter MH (2008a) Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 56:86–100
Floss DS, Schliemann W, Schmidt J, Strack D, Walter MH (2008b) RNA interference-mediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C-27 apocarotenoids, shedding light on the functional role of CCD1. Plant Physiol 148:1267–1282
Foo E, Buillier 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
Gao ZY, Qian Q, Liu XH, Yan MX, Feng Q, Dong GJ, Liu J, Han B (2009) Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71:265–276
Garcia-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459
Garcia-Limones C, Schnabele K, Blanco-Portales R, Bellido ML, Caballero JL, Schwab W, Munoz-Blanco J (2008) Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. J Agric Food Chem 56:9277–9285
Giuliano G, Al-Babili S, von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149
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
Hans J, Hause B, Strack D, Walter MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134:614–624
Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412
Hessel S, Eichinger A, Isken A, Amengual J, Hunzelmann S, Hoeller U, Elste V, Hunziker W, Goralczyk R, Oberhauser V, von Lintig J, Wyss A (2007) CMO1 deficiency abolishes vitamin A production from beta-carotene and alters lipid metabolism in mice. J Biol Chem 282:33553–33561
Huang FC, Horvath G, Molnar P, Turcsi E, Deli J, Schrader J, Sandmann G, Schmidt H, Schwab W (2009a) Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena. Phytochemistry 70:457–464
Huang FC, Molnar P, Schwab W (2009b) Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J Exp Bot 60:3011–3022
Humphrey AJ, Beale MH (2006) Strigol: Biogenesis and physiological activity. Phytochemistry 67:636–640
Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N, Tadmor Y, Lewinsohn E (2006) Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67:1579–1589
Ilg A, Beyer P, Al-Babili S (2009) Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial biosynthesis. FEBS J 276:736–747
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
Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725
Johnson X, Brcich T, Dun EA, Goussot M, Haurogne 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
Kang YW, Kim RN, Cho HS, Kim WT, Choi D, Pai HS (2008) Silencing of a BYPASS1 homolog results in root-independent pleiotrophic developmental defects in Nicotiana benthamiana. Plant Mol Biol 68:423–437
Kato M, Matsumoto H, Ikoma Y, Okuda H, Yano M (2006) The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit. J Exp Bot 57:2153–2164
Kiefer C, Hessel S, Lampert JM, Vogt K, Lederer MO, Breithaupt DE, von Lintig J (2001) Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J Biol Chem 276:14110–14116
Kinden DA, Brown MF (1976) Electron-microscopy of vesicular-arbuscular mycorrhizae of yellow poplar. 4. Host–endophyte interactions during arbuscular deterioration. Can J Microbiol 22:64–75
Klingner A, Bothe H, Wray V, Marner FJ (1995) Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38:53–55
Kloer DP, Schulz GE (2006) Structural and biological aspects of carotenoid cleavage. Cell Mol Life Sci 63:2291–2303
Kloer DP, Ruch S, Al-Babili S, Beyer P, Schulz GE (2005) The structure of a retinal-forming carotenoid oxygenase. Science 308:267–269
Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul (in press). doi:10.1007/s00344-009-9122-7
Lendzemo VW, Kuypers TW, Matusova R, Bouwmeester HJ, van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Sign Behav 2:58–62
Lendzemo V, Kuyper TW, Vierheilig H (2009) Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19:287–294
Leyser O (2008) Strigolactones and shoot branching: a new trick for a young dog. Dev Cell 15:337–338
Lin H, Wang RX, Qian Q, Yan MX, Meng XB, Fu ZM, Yan CY, Jiang B, Su Z, Li JY, Wang YH (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525
Liu WZ, Wu C, Fu YP, Hu GC, Si HM, Zhu L, Luan WJ, He ZQ, Sun ZX (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230:649–658
Lohse S, Hause B, Hause G, Fester T (2006) FtsZ characterization and immunolocalization in the two phases of plastid reorganization in arbuscular mycorrhizal roots of Medicago truncatula. Plant Cell Physiol 47:1124–1134
Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874
Macias FA, Varela RM, Torres A, Oliva RM, Molinillo JMG (1998) Bioactive norsesquiterpenes from Helianthus annuus: potential allelopathic activity. Phytochemistry 48:631–636
Macias FA, Lopez A, Varela RM, Torres A, Molinillo JMG (2004) Bioactive apocarotenoids annuionones F and G: structural revision of annuionones A, B and E. Phytochemistry 65:3057–3063
Maicas S, Mateo JJ (2005) Hydrolysis of terpenyl glycosides in grape juice and other fruit juices: a review. Appl Microbiol Biotechnol 67:322–335
Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 109:465–470
Marasco EK, Schmidt-Dannert C (2008) Identification of bacterial carotenoid cleavage dioxygenase homologues that cleave the interphenyl alpha, beta double bond of stilbene derivatives via a monooxygenase reaction. Chem Biochem 9:1450–1461
Marasco EK, Vay K, Schmidt-Dannert C (2006) Identification of carotenoid cleavage dioxygenases from Nostoc sp PCC 7120 with different cleavage activities. J Biol Chem 281:31583–31593
Mathieu S, Terrier N, Procureur J, Bigey F, Gunata Z (2005) A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C-13-norisoprenoid accumulation. J Exp Bot 56:2721–2731
Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934
Mendes-Pinto MM (2009) Carotenoid breakdown products: the “norisoprenoids” in wine aroma. Arch Biochem Biophys 483:236–245
Moraga AR, Rambla JL, Ahrazem O, Granell A, Gomez-Gomez L (2009) Metabolite and target transcript analyses during Crocus sativus stigma development. Phytochemistry 70:1009–1016
Mouchel CF, Leyser O (2007) Novel phytohormones involved in long-range signaling. Curr Opin Plant Biol 10:473–476
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol 56:165–185
North HM, De Almeida A, Boutin JP, Frey A, To A, Botran L, Sotta B, Marion-Poll A (2007) The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. Plant J 50:810–824
Ohmiya A (2009) Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 26:351–358
Ohmiya A, Kishimoto S, Yoshioka S, Sumitomo K (2005) Cloning of a carotenoid cleavage dioxygenase gene (CmCCD1) differentially expressed in white petals of chrysanthemum. Plant Cell Physiol 46:S241–S241
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
Ohmiya A, Sumitomo K, Aida R (2009) “Yellow Jimba”: suppression of carotenoid cleavage dioxygenase (CmCCD4a) expression turns white chrysanthemum petals yellow. J Jpn Soc Hortic Sci 78:450–455
Park S, Takano Y, Matsuura H, Yoshihara T (2004) Antifungal compounds from the root and root exudate of Zea mays. Biosci Biotechnol Biochem 68:1366–1368
Poliakov E, Gentleman S, Cunningham FX, Miller-Ihli NJ, Redmond TM (2005) Key role of conserved histidines in recombinant mouse beta-carotene 15, 15′-monooxygenase-1 activity. J Biol Chem 280:29217–29223
Prado-Cabrero A, Scherzinger D, Avalos J, Al-Babili S (2007) Retinal biosynthesis in fungi: Characterization of the carotenoid oxygenase CarX from Fusarium fujikuroi. Eukaryot Cell 6:650–657
Redmond TM, Gentleman S, Duncan T, Yu S, Wiggert B, Gantt E, Cunningham FX (2001) Identification, expression, and substrate specificity of a mammalian beta-carotene 15, 15′-dioxygenase. J Biol Chem 276:6560–6565
Rubio A, Rambla JL, Santaella M, Gomez MD, Orzaez D, Granell A, Gomez-Gomez L (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem 283:24816–24825
Ruch S, Beyer P, Ernst H, Al-Babili S (2005) Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol Microbiol 55:1015–1024
Ryle MJ, Hausinger RP (2002) Non-heme iron oxygenases. Curr Opin Chem Biol 6:193–201
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
Schimek C, Wöstemeyer J (2009) Carotene derivatives in sexual communication of zygomycete fungi. Phytochemistry 70:1867–1875
Schlicht M, Samajova O, Schachtschabel D, Mancuso S, Menzel D, Boland W, Baluska 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
Schmidt H, Kurtzer R, Eisenreich W, Schwab W (2006) The carotenase AtCCD1 from Arabidopsis thaliana is a dioxygenase. J Biol Chem 281:9845–9851
Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874
Schwartz SH, Qin XQ, Zeevaart JAD (2001) Characterization of a novel carotenoid cleavage dioxygenase from plants. J Biol Chem 276:25208–25211
Schwartz SH, Qin XQ, Zeevaart JAD (2003) Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131:1591–1601
Schwartz SH, Qin XQ, 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
Sheard LB, Zheng N (2009) Signal advance for abscisic acid. Nature 462:575–576
Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004a) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892
Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E, Clark DG, Klee HJ (2004b) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of beta-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136:3504–3514
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
Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance 1/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
Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Gene Dev 17:1469–1474
Stirnberg P, van de Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141
Stirnberg P, Furner IJ, Leyser HMO (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94
Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34
Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FWA, Ming Z, van Echtelt E, Strack D, Bisseling T, Bouwmeester HJ (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801
Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240
Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56
Tsuchiya Y, McCourt P (2009) Strigolactones: a new hormone with a past. Curr Opin Plant Biol 12:556–561
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
Van Norman JM, Sieburth LE (2007) Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J 49:619–628
Van Norman JM, Frederick RL, Sieburth LE (2004) BYPASS1 negatively regulates a root-derived signal that controls plant architecture. Curr Biol 14:1739–1746
Vogel JT, Tan BC, McCarty DR, Klee HJ (2008) The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem 283:11364–11373
Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311
von Lintig J, Vogt K (2000) Filling the gap in vitamin A research—molecular identification of an enzyme cleaving beta-carotene to retinal. J Biol Chem 275:11915–11920
von Lintig J, Vogt K (2004) Vitamin A formation in animals: molecular identification and functional characterization of carotene cleaving enzymes. J Nutr 134:251S–256S
von Lintig J, Dreher A, Kiefer C, Wernet MF, Vogt K (2001) Analysis of the blind Drosophila mutant ninaB identifies the gene encoding the key enzyme for vitamin A formation in vivo. Proc Natl Acad Sci USA 98:1130–1135
Walter MH, Fester T, Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant J 21:571–578
Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254
Walter MH, Floss DS, Hans J, Fester T, Strack D (2007) Apocarotenold biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry 68:130–138
Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984–997
Acknowledgments
The research in the author’s laboratory has been supported in part by the Deutsche Forschungsgemeinschaft. The authors are indebted to Catherine Rameau (INRA Versailles, France) for providing seeds of the pea rms mutants currently under study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Walter, M.H., Floss, D.S. & Strack, D. Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232, 1–17 (2010). https://doi.org/10.1007/s00425-010-1156-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-010-1156-3