Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense

被引:89
作者
Fatouros, Nina E. [1 ]
Broekgaarden, Colette [1 ,2 ]
Bukovinszkine'Kiss, Gabriella [1 ]
van Loon, Joop J. A. [1 ]
Mumm, Roland [1 ]
Huigens, Martinus E. [1 ]
Dicke, Marcel [1 ]
Hilker, Monika [3 ]
机构
[1] Wageningen Univ, Dept Plant Sci, Entomol Lab, NL-6700 EH Wageningen, Netherlands
[2] Univ Wageningen & Res Ctr, NL-6708 PB Wageningen, Netherlands
[3] Free Univ Berlin, Inst Biol, D-12163 Berlin, Germany
关键词
egg parasitoid; elicitor; Trichogramma brassicae; Pieris brassicae; Brussels sprouts;
D O I
10.1073/pnas.0707809105
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Plants can recruit parasitic wasps in response to egg deposition by herbivorous insects-a sophisticated. indirect plant defense mechanism. Oviposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprout plants induces phytochemical changes that arrest the egg parasitoid Trichogramma brassicae. Here, we report the identification of an elicitor of such an oviposition-induced plant response. Eliciting activity was present in accessory gland secretions released by mated female butterflies during egg deposition. In contrast, gland secretions from virgin female butterflies were inactive. In the male ejaculate, P. brassicae females receive the anti-aphrodisiac benzyl cyanide (BC) that reduces the females' attractiveness for subsequent mating. We detected this pheromone in the accessory gland secretion released by mated female butterflies. When applied onto leaves, BC alone induced phytochemical changes that arrested females of the egg parasitoid. Microarray analyses revealed a similarity in induced plant responses that may explain the arrest of T. brassicae to egg-laden and BC-treated plants. Thus, a male-derived compound endangers the offspring of the butterfly by inducing plant defense. Recently, BC was shown to play a role in foraging behavior of T. brassicae, by acting as a cue to facilitate phoretic transport by mated female butterflies to oviposition sites. Our results suggest that the anti-aphrodisiac pheromone incurs fitness costs for the butterfly by both mediating phoretic behavior and inducing plant defense.
引用
收藏
页码:10033 / 10038
页数:6
相关论文
共 46 条
[1]   Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles [J].
Alborn, Hans T. ;
Hansen, Trond V. ;
Jones, Tappey H. ;
Bennett, Derrick C. ;
Tumlinson, James H. ;
Schmelz, Eric A. ;
Teal, Peter E. A. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (32) :12976-12981
[2]   An elicitor of plant volatiles from beet armyworm oral secretion [J].
Alborn, HT ;
Turlings, TCJ ;
Jones, TH ;
Stenhagen, G ;
Loughrin, JH ;
Tumlinson, JH .
SCIENCE, 1997, 276 (5314) :945-949
[3]   Identification and synthesis of volicitin and related components from beet armyworm oral secretions [J].
Alborn, HT ;
Jones, TH ;
Stenhagen, GS ;
Tumlinson, JH .
JOURNAL OF CHEMICAL ECOLOGY, 2000, 26 (01) :203-220
[4]   Differential activity and degradation of plant volatile elicitors in regurgitant of tobacco hornworm (Manduca sexta) larvae [J].
Alborn, HT ;
Brennan, MM ;
Tumlinson, JH .
JOURNAL OF CHEMICAL ECOLOGY, 2003, 29 (06) :1357-1372
[5]   Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females [J].
Andersson, J ;
Borg-Karlson, AK ;
Wiklund, C .
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2000, 267 (1450) :1271-1275
[6]   Antiaphrodisiacs in pierid butterflies: A theme with variation! [J].
Andersson, J ;
Borg-Karlson, AK ;
Wiklund, C .
JOURNAL OF CHEMICAL ECOLOGY, 2003, 29 (06) :1489-1499
[7]   Functional annotation of the Arabidopsis genome using controlled vocabularies [J].
Berardini, TZ ;
Mundodi, S ;
Reiser, L ;
Huala, E ;
Garcia-Hernandez, M ;
Zhang, PF ;
Mueller, LA ;
Yoon, J ;
Doyle, A ;
Lander, G ;
Moseyko, N ;
Yoo, D ;
Xu, I ;
Zoeckler, B ;
Montoya, M ;
Miller, N ;
Weems, D ;
Rhee, SY .
PLANT PHYSIOLOGY, 2004, 135 (02) :745-755
[8]   Male butterfly investment in successive ejaculates in relation to mating system [J].
Bissoondath, CJ ;
Wiklund, C .
BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 1996, 39 (05) :285-292
[9]   Genotypic variation in genome-wide transcription profiles induced by insect feeding:: Brassica oleracea-Pieris rapae interactions [J].
Broekgaarden, Colette ;
Poelman, Erik H. ;
Steenhuis, Greet ;
Voorrips, Roeland E. ;
Dicke, Marcel ;
Vosman, Ben .
BMC GENOMICS, 2007, 8 (1)
[10]   Oviposition-Induced Changes in Arabidopsis Genome Expression Anticipating Your Enemy? [J].
Bruessow, Friederike ;
Reymond, Philippe .
PLANT SIGNALING & BEHAVIOR, 2007, 2 (03) :165-167