Plant carotenoid cleavage oxygenases and their apocarotenoid products.

The oxidative cleavage of carotenoids leads to the production of apocarotenoids and is catalyzed by a family of carotenoid cleavage dioxygenases (CCDs). CCDs often exhibit substrate promiscuity, which probably contributes to the diversity of apocarotenoids found in nature. Biologically and commercially important apocarotenoids include the phytohormone abscisic acid, the visual and signaling molecules retinal and retinoic acid, and the aromatic volatile beta-ionone. Unexpected properties associated with the CCD catalytic products emphasize their role in many aspects of plant growth and development. For instance, CCD7 and CCD8 produce a novel, graft-transmissible hormone that controls axillary shoot growth in plants. Here, CCDs are discussed according to their roles in the biosynthesis of these products. Recent studies regarding their mechanism of action are also addressed.

[1]  H. Leyser,et al.  MAX1 and MAX2 control shoot lateral branching in Arabidopsis. , 2002, Development.

[2]  P. Beyer,et al.  Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803 , 2004, Molecular microbiology.

[3]  N. Terrier,et al.  A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. , 2005, Journal of experimental botany.

[4]  B. Camara,et al.  Biosynthesis of the Food and Cosmetic Plant Pigment Bixin (Annatto) , 2003, Science.

[5]  N. Watanabe,et al.  Enzymatic carotenoid cleavage in star fruit (Averrhoa carambola). , 2003, Phytochemistry.

[6]  C. Beveridge,et al.  The Branching Gene RAMOSUS1 Mediates Interactions among Two Novel Signals and Auxin in Pea , 2005, The Plant Cell Online.

[7]  S. Andersson,et al.  Biochemical Properties of Purified Recombinant Human β-Carotene 15,15′-Monooxygenase* , 2002, The Journal of Biological Chemistry.

[8]  C. Beveridge,et al.  MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. , 2003, Genes & development.

[9]  J. Bu’lock,et al.  Trisporic acid biosynthesis and carotenogenesis in Blakesleea trispora. , 1969, The Biochemical journal.

[10]  H. Klee,et al.  The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. , 2004, The Plant journal : for cell and molecular biology.

[11]  S. Schwartz,et al.  The Biochemical Characterization of Two Carotenoid Cleavage Enzymes from Arabidopsis Indicates That a Carotenoid-derived Compound Inhibits Lateral Branching* , 2004, Journal of Biological Chemistry.

[12]  R. Rouseff,et al.  Carotenoid-derived aroma compounds , 2001 .

[13]  S. Hessel,et al.  Identification and Characterization of a Mammalian Enzyme Catalyzing the Asymmetric Oxidative Cleavage of Provitamin A* , 2001, The Journal of Biological Chemistry.

[14]  W. Eisenreich,et al.  The Carotenase AtCCD1 from Arabidopsis thaliana Is a Dioxygenase* , 2006, Journal of Biological Chemistry.

[15]  S. Hessel,et al.  Towards a better understanding of carotenoid metabolism in animals. , 2005, Biochimica et biophysica acta.

[16]  T. Moore Vitamin A and carotene: The absence of the liver oil vitamin A from carotene. VI. The conversion of carotene to vitamin A in vivo. , 1930, The Biochemical journal.

[17]  O. Hayaishi,et al.  The enzymatic cleavage of beta-carotene into vitamin A by soluble enzymes of rat liver and intestine. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. Akiyama,et al.  Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi , 2005, Nature.

[19]  C. Beveridge,et al.  Long-distance signaling and the control of branching in the rms1 mutant of pea. , 2001, Plant physiology.

[20]  Ottoline Leyser,et al.  Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. , 2005, The Plant journal : for cell and molecular biology.

[21]  C. Turnbull,et al.  Micrografting techniques for testing long-distance signalling in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[22]  W. Woggon Oxidative cleavage of carotenoids catalyzed by enzyme models and beta-carotene 15,15´-monooxygenase , 2002 .

[23]  O. Leyser,et al.  MAX3/CCD7 Is a Carotenoid Cleavage Dioxygenase Required for the Synthesis of a Novel Plant Signaling Molecule , 2004, Current Biology.

[24]  Beverly A. Underwood,et al.  Circadian Regulation of the PhCCD1 Carotenoid Cleavage Dioxygenase Controls Emission of β-Ionone, a Fragrance Volatile of Petunia Flowers1 , 2004, Plant Physiology.

[25]  D. Goodman,et al.  Biosynthesis of Vitamin A with Rat Intestinal Enzymes , 1965, Science.

[26]  Y. Saburi,et al.  Cloning, expression, and sequence analysis of a lignostilbene-α,β-dioxygenase gene from Pseudomonas paucimobilis TMY1009 , 1993 .

[27]  H. Klee,et al.  Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. , 2006, The Plant journal : for cell and molecular biology.

[28]  C. Napoli,et al.  Highly Branched Phenotype of the Petunia dad1-1 Mutant Is Reversed by Grafting , 1996, Plant physiology.

[29]  Joanne L. Simons,et al.  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 , 2005, The Plant Cell Online.

[30]  C. M. Karssen,et al.  Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. , 1983, Planta.

[31]  J. Mutterer,et al.  Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. , 2003, The Plant cell.

[32]  C. Hamel,et al.  Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated in vitro. , 1993, The Journal of biological chemistry.

[33]  C. Beveridge Axillary bud outgrowth: sending a message. , 2006, Current opinion in plant biology.

[34]  D. Zamir,et al.  Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analyses. , 2005, Journal of agricultural and food chemistry.

[35]  D. McCarty,et al.  Genetic control of abscisic acid biosynthesis in maize. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Leuenberger,et al.  The Reaction Mechanism of the Enzyme-Catalyzed Central Cleavage of β-Carotene to Retinal. , 2001, Angewandte Chemie.

[37]  R. Bressan,et al.  Uncoupling the Effects of Abscisic Acid on Plant Growth and Water Relations. Analysis of sto1/nced3, an Abscisic Acid-Deficient but Salt Stress-Tolerant Mutant in Arabidopsis1 , 2004, Plant Physiology.

[38]  Xianwu Zheng,et al.  HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E. L. Arumingtyas Branching in Pisum: inheritance and allelism tests with 17 ramosus mutants , 1992 .

[40]  V. Wray,et al.  Is stimulation of carotenoid biosynthesis in arbuscular mycorrhizal roots a general phenomenon? , 2005, Phytochemistry.

[41]  K. Shinozaki,et al.  Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. , 2001, The Plant journal : for cell and molecular biology.

[42]  H. Bouwmeester,et al.  The Strigolactone Germination Stimulants of the Plant-Parasitic Striga and Orobanche spp. Are Derived from the Carotenoid Pathway1 , 2005, Plant Physiology.

[43]  S. Baldermann,et al.  Enzymatic carotenoid degradation and aroma formation in nectarines (Prunus persica) , 2005 .

[44]  R. Creelman,et al.  Incorporation of oxygen into abscisic Acid and phaseic Acid from molecular oxygen. , 1984, Plant physiology.

[45]  C. Turnbull,et al.  MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. , 2005, Developmental cell.

[46]  G. Travis,et al.  Rpe65 Is the Retinoid Isomerase in Bovine Retinal Pigment Epithelium , 2005, Cell.

[47]  G. Schulz,et al.  The Structure of a Retinal-Forming Carotenoid Oxygenase , 2005, Science.

[48]  D. McCarty,et al.  Specific oxidative cleavage of carotenoids by VP14 of maize. , 1997, Science.

[49]  J. von Lintig,et al.  Filling the Gap in Vitamin A Research , 2000, The Journal of Biological Chemistry.

[50]  D. McCarty,et al.  Substrate specificity and kinetics for VP14, a carotenoid cleavage dioxygenase in the ABA biosynthetic pathway. , 2003, Biochimica et biophysica acta.

[51]  P. Bliss,et al.  Identification of loci affecting flavour volatile emissions in tomato fruits. , 2006, Journal of experimental botany.

[52]  S. Schwartz,et al.  Characterization of a Novel Carotenoid Cleavage Dioxygenase from Plants* , 2001, The Journal of Biological Chemistry.

[53]  K. Cline,et al.  Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. , 2003, The Plant journal : for cell and molecular biology.

[54]  W. Zhai,et al.  Characterizations and fine mapping of a mutant gene for high tillering and dwarf in rice (Oryza sativa L.) , 2005, Planta.

[55]  K. Cline,et al.  Localization and targeting of the VP14 epoxy-carotenoid dioxygenase to chloroplast membranes. , 2001, The Plant journal : for cell and molecular biology.

[56]  S. Yu,et al.  Identification, Expression, and Substrate Specificity of a Mammalian β-Carotene 15,15′-Dioxygenase* , 2001, The Journal of Biological Chemistry.