|
THE PLANT CELL, Vol 8, Issue 7 1137-1148, Copyright © 1996 by American Society of Plant Biologists
Evolution of Floral Scent in Clarkia: Novel Patterns of S-Linalool Synthase Gene Expression in the C. breweri Flower
N. Dudareva, L. Cseke, V. M. Blanc and E. Pichersky
Biology Department, University of Michigan, Ann Arbor, Michigan 48109
Flowers of Clarkia breweri, an annual plant from the coastal range of
California, emit a strong sweet scent of which S-linalool, an acyclic
monoterpene, is a major component. Chromosomal, chemical, and morphological
data, and the species' geographic distribution, suggest that C. breweri
evolved from an extant nonscented species, C. concinna. A cDNA of Lis, the
gene encoding S-linalool synthase, was isolated from C. breweri. We show
that in C. breweri, Lis is highly expressed in cells of the transmitting
tract of the stigma and style and in the epidermal cells of petals, as well
as in stamens, whereas in the nonscented C. concinna, Lis is expressed only
in the stigma and at a relatively low level. In both species, changes in
protein levels parallel changes in mRNA levels, and changes in enzyme
activity levels parallel changes in protein levels. The results indicate
that in C. breweri, the expression of Lis has been upregulated and its
range enlarged to include cells not expressing this gene in C. concinna.
These results show how scent can evolve in a relatively simple way without
the evolution of highly specialized "scent glands" and other specialized
structures. Lis encodes a protein that is structurally related to the
family of proteins termed terpene synthases. The protein encoded by Lis is
the first member of this family found to catalyze the formation of an
acyclic monoterpene.
This article has been cited by other articles:

|
 |

|
 |
 
S. Lee and J. Chappell
Biochemical and Genomic Characterization of Terpene Synthases in Magnolia grandiflora
Plant Physiology,
July 1, 2008;
147(3):
1017 - 1033.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Scalliet, F. Piola, C. J. Douady, S. Rety, O. Raymond, S. Baudino, K. Bordji, M. Bendahmane, C. Dumas, J. M. Cock, et al.
From the Cover: Scent evolution in Chinese roses
PNAS,
April 15, 2008;
105(15):
5927 - 5932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Herde, K. Gartner, T. G. Kollner, B. Fode, W. Boland, J. Gershenzon, C. Gatz, and D. Tholl
Identification and Regulation of TPS04/GES, an Arabidopsis Geranyllinalool Synthase Catalyzing the First Step in the Formation of the Insect-Induced Volatile C16-Homoterpene TMTT
PLANT CELL,
April 1, 2008;
20(4):
1152 - 1168.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q. Cronk and I. Ojeda
Bird-pollinated flowers in an evolutionary and molecular context
J. Exp. Bot.,
March 7, 2008;
(2008)
ern009v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Hernandez, D. Molenaar, J. Beekwilder, H. Bouwmeester, and J. E. T. van Hylckama Vlieg
Expression of Plant Flavor Genes in Lactococcus lactis
Appl. Envir. Microbiol.,
March 1, 2007;
73(5):
1544 - 1552.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Orlova, A. Marshall-Colon, J. Schnepp, B. Wood, M. Varbanova, E. Fridman, J. J. Blakeslee, W. A. Peer, A. S. Murphy, D. Rhodes, et al.
Reduction of Benzenoid Synthesis in Petunia Flowers Reveals Multiple Pathways to Benzoic Acid and Enhancement in Auxin Transport
PLANT CELL,
December 1, 2006;
18(12):
3458 - 3475.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Ulland, E. Ian, A.-K. Borg-Karlson, and H. Mustaparta
Discrimination between Enantiomers of Linalool by Olfactory Receptor Neurons in the Cabbage Moth Mamestra brassicae (L.)
Chem Senses,
May 1, 2006;
31(4):
325 - 334.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Scalliet, C. Lionnet, M. Le Bechec, L. Dutron, J.-L. Magnard, S. Baudino, V. Bergougnoux, F. Jullien, P. Chambrier, P. Vergne, et al.
Role of Petal-Specific Orcinol O-Methyltransferases in the Evolution of Rose Scent
Plant Physiology,
January 1, 2006;
140(1):
18 - 29.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Fridman, J. Wang, Y. Iijima, J. E. Froehlich, D. R. Gang, J. Ohlrogge, and E. Pichersky
Metabolic, Genomic, and Biochemical Analyses of Glandular Trichomes from the Wild Tomato Species Lycopersicon hirsutum Identify a Key Enzyme in the Biosynthesis of Methylketones
PLANT CELL,
April 1, 2005;
17(4):
1252 - 1267.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Stuurman, M. E. Hoballah, L. Broger, J. Moore, C. Basten, and C. Kuhlemeier
Dissection of Floral Pollination Syndromes in Petunia
Genetics,
November 1, 2004;
168(3):
1585 - 1599.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Aharoni, A. P. Giri, F. W.A. Verstappen, C. M. Bertea, R. Sevenier, Z. Sun, M. A. Jongsma, W. Schwab, and H. J. Bouwmeester
Gain and Loss of Fruit Flavor Compounds Produced by Wild and Cultivated Strawberry Species
PLANT CELL,
November 1, 2004;
16(11):
3110 - 3131.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-C. Caissard, A. Meekijjironenroj, S. Baudino, and M.-C. Anstett
Localization of production and emission of pollinator attractant on whole leaves of Chamaerops humilis (Arecaceae)
Am. J. Botany,
August 1, 2004;
91(8):
1190 - 1199.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Dudareva, E. Pichersky, and J. Gershenzon
Biochemistry of Plant Volatiles
Plant Physiology,
August 1, 2004;
135(4):
1893 - 1902.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Boatright, F. Negre, X. Chen, C. M. Kish, B. Wood, G. Peel, I. Orlova, D. Gang, D. Rhodes, and N. Dudareva
Understanding in Vivo Benzenoid Metabolism in Petunia Petal Tissue
Plant Physiology,
August 1, 2004;
135(4):
1993 - 2011.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. R. Wilderman, M. Xu, Y. Jin, R. M. Coates, and R. J. Peters
Identification of Syn-Pimara-7,15-Diene Synthase Reveals Functional Clustering of Terpene Synthases Involved in Rice Phytoalexin/Allelochemical Biosynthesis
Plant Physiology,
August 1, 2004;
135(4):
2098 - 2105.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. M. Martin, J. Faldt, and J. Bohlmann
Functional Characterization of Nine Norway Spruce TPS Genes and Evolution of Gymnosperm Terpene Synthases of the TPS-d Subfamily
Plant Physiology,
August 1, 2004;
135(4):
1908 - 1927.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Tholl, C. M. Kish, I. Orlova, D. Sherman, J. Gershenzon, E. Pichersky, and N. Dudareva
Formation of Monoterpenes in Antirrhinum majus and Clarkia breweri Flowers Involves Heterodimeric Geranyl Diphosphate Synthases
PLANT CELL,
April 1, 2004;
16(4):
977 - 992.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Iijima, D. R. Gang, E. Fridman, E. Lewinsohn, and E. Pichersky
Characterization of Geraniol Synthase from the Peltate Glands of Sweet Basil
Plant Physiology,
January 1, 2004;
134(1):
370 - 379.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Lucker, W. Schwab, B. van Hautum, J. Blaas, L. H. W. van der Plas, H. J. Bouwmeester, and H. A. Verhoeven
Increased and Altered Fragrance of Tobacco Plants after Metabolic Engineering Using Three Monoterpene Synthases from Lemon
Plant Physiology,
January 1, 2004;
134(1):
510 - 519.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Aharoni, A. P. Giri, S. Deuerlein, F. Griepink, W.-J. de Kogel, F. W. A. Verstappen, H. A. Verhoeven, M. A. Jongsma, W. Schwab, and H. J. Bouwmeester
Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants
PLANT CELL,
December 1, 2003;
15(12):
2866 - 2884.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Negre, C. M. Kish, J. Boatright, B. Underwood, K. Shibuya, C. Wagner, D. G. Clark, and N. Dudareva
Regulation of Methylbenzoate Emission after Pollination in Snapdragon and Petunia Flowers
PLANT CELL,
December 1, 2003;
15(12):
2992 - 3006.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Romano and G. A. Wray
Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation
Development,
September 1, 2003;
130(17):
4187 - 4199.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Wray, M. W. Hahn, E. Abouheif, J. P. Balhoff, M. Pizer, M. V. Rockman, and L. A. Romano
The Evolution of Transcriptional Regulation in Eukaryotes
Mol. Biol. Evol.,
September 1, 2003;
20(9):
1377 - 1419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Dudareva, D. Martin, C. M. Kish, N. Kolosova, N. Gorenstein, J. Faldt, B. Miller, and J. Bohlmann
(E)-{beta}-Ocimene and Myrcene Synthase Genes of Floral Scent Biosynthesis in Snapdragon: Function and Expression of Three Terpene Synthase Genes of a New Terpene Synthase Subfamily
PLANT CELL,
May 1, 2003;
15(5):
1227 - 1241.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Perret, A. Chautems, R. Spichiger, G. Kite, and V. Savolainen
Systematics and evolution of tribe Sinningieae (Gesneriaceae): evidence from phylogenetic analyses of six plastid DNA regions and nuclear ncpGS
Am. J. Botany,
March 1, 2003;
90(3):
445 - 460.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Chen, D. Tholl, J. C. D'Auria, A. Farooq, E. Pichersky, and J. Gershenzon
Biosynthesis and Emission of Terpenoid Volatiles from Arabidopsis Flowers
PLANT CELL,
February 1, 2003;
15(2):
481 - 494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Schnee, T. G. Kollner, J. Gershenzon, and J. Degenhardt
The Maize Gene terpene synthase 1 Encodes a Sesquiterpene Synthase Catalyzing the Formation of (E)-beta -Farnesene, (E)-Nerolidol, and (E,E)-Farnesol after Herbivore Damage
Plant Physiology,
December 1, 2002;
130(4):
2049 - 2060.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Eckardt
A Rose by Any Other Name?
PLANT CELL,
October 1, 2002;
14(10):
2315 - 2317.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Guterman, M. Shalit, N. Menda, D. Piestun, M. Dafny-Yelin, G. Shalev, E. Bar, O. Davydov, M. Ovadis, M. Emanuel, et al.
Rose Scent: Genomics Approach to Discovering Novel Floral Fragrance-Related Genes
PLANT CELL,
October 1, 2002;
14(10):
2325 - 2338.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. D'Auria, F. Chen, and E. Pichersky
Characterization of an Acyltransferase Capable of Synthesizing Benzylbenzoate and Other Volatile Esters in Flowers and Damaged Leaves of Clarkia breweri
Plant Physiology,
September 1, 2002;
130(1):
466 - 476.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Martin, D. Tholl, J. Gershenzon, and J. Bohlmann
Methyl Jasmonate Induces Traumatic Resin Ducts, Terpenoid Resin Biosynthesis, and Terpenoid Accumulation in Developing Xylem of Norway Spruce Stems
Plant Physiology,
July 1, 2002;
129(3):
1003 - 1018.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Vainstein, E. Lewinsohn, E. Pichersky, and D. Weiss
Floral Fragrance. New Inroads into an Old Commodity
Plant Physiology,
December 1, 2001;
127(4):
1383 - 1389.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Lewinsohn, F. Schalechet, J. Wilkinson, K. Matsui, Y. Tadmor, K.-H. Nam, O. Amar, E. Lastochkin, O. Larkov, U. Ravid, et al.
Enhanced Levels of the Aroma and Flavor Compound S-Linalool by Metabolic Engineering of the Terpenoid Pathway in Tomato Fruits
Plant Physiology,
November 1, 2001;
127(3):
1256 - 1265.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Kolosova, N. Gorenstein, C. M. Kish, and N. Dudareva
Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants
PLANT CELL,
October 1, 2001;
13(10):
2333 - 2347.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Kolosova, D. Sherman, D. Karlson, and N. Dudareva
Cellular and Subcellular Localization of S-Adenosyl-L-Methionine:Benzoic Acid Carboxyl Methyltransferase, the Enzyme Responsible for Biosynthesis of the Volatile Ester Methylbenzoate in Snapdragon Flowers
Plant Physiology,
July 1, 2001;
126(3):
956 - 964.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Dudareva, L. M. Murfitt, C. J. Mann, N. Gorenstein, N. Kolosova, C. M. Kish, C. Bonham, and K. Wood
Developmental Regulation of Methyl Benzoate Biosynthesis and Emission in Snapdragon Flowers
PLANT CELL,
June 1, 2000;
12(6):
949 - 961.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
N. Dudareva and E. Pichersky
Biochemical and Molecular Genetic Aspects of Floral Scents
Plant Physiology,
March 1, 2000;
122(3):
627 - 634.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. J. Bouwmeester, F. W.A. Verstappen, M. A. Posthumus, and M. Dicke
Spider Mite-Induced (3S)-(E)-Nerolidol Synthase Activity in Cucumber and Lima Bean. The First Dedicated Step in Acyclic C11-Homoterpene Biosynthesis
Plant Physiology,
September 1, 1999;
121(1):
173 - 180.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. Doebley and L. Lukens
Transcriptional Regulators and the Evolution of Plant Form
PLANT CELL,
July 1, 1998;
10(7):
1075 - 1082.
[Full Text]
|
 |
|

|
 |

|
 |
 
M. L. Wise, T. J. Savage, E. Katahira, and R. Croteau
Monoterpene Synthases from Common Sage (Salvia officinalis). cDNA ISOLATION, CHARACTERIZATION, AND FUNCTIONAL EXPRESSION OF (+)-SABINENE SYNTHASE, 1,8-CINEOLE SYNTHASE, AND (+)-BORNYL DIPHOSPHATE SYNTHASE
J. Biol. Chem.,
June 12, 1998;
273(24):
14891 - 14899.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Bohlmann, G. Meyer-Gauen, and R. Croteau
Plant terpenoid synthases: Molecular biology and phylogenetic analysis
PNAS,
April 14, 1998;
95(8):
4126 - 4133.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Dudareva, R. A. Raguso, J. Wang, J. R. Ross, and E. Pichersky
Floral Scent Production in Clarkia breweri . III. Enzymatic Synthesis and Emission of Benzenoid Esters
Plant Physiology,
February 1, 1998;
116(2):
599 - 604.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Bohlmann, C. L. Steele, and R. Croteau
Monoterpene Synthases from Grand Fir (Abies grandis). cDNA ISOLATION, CHARACTERIZATION, AND FUNCTIONAL EXPRESSION OF MYRCENE SYNTHASE, (-)-(4S)-LIMONENE SYNTHASE, AND (-)-(1S,5S)-PINENE SYNTHASE
J. Biol. Chem.,
August 29, 1997;
272(35):
21784 - 21792.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|