Summary• Flowers have a high risk of pathogen attack because of their rich nutrient and moisture content, and high frequency of insect visitors. We investigated the role of (E)-b-caryophyllene in floral defense against a microbial pathogen. This sesquiterpene is a common volatile compound emitted from flowers, and is a major volatile released from the stigma of Arabidopsis thaliana flowers.• Arabidopsis thaliana lines lacking a functional (E)-b-caryophyllene synthase or constitutively overexpressing this gene were challenged with Pseudomonas syringae pv. tomato DC3000, which is a bacterial pathogen of brassicaceous plants.• Flowers of plant lines lacking (E)-b-caryophyllene emission showed greater bacterial growth on their stigmas than did wild-type flowers, and their seeds were lighter and misshapen. By contrast, plant lines with ectopic (E)-b-caryophyllene emission from vegetative parts were more resistant than wild-type plants to pathogen infection of leaves, and showed reduced cell damage and higher seed production. Based on in vitro experiments, (E)-b-caryophyllene seems to act by direct inhibition of bacterial growth, rather than by triggering defense signaling pathways.• (E)-b-Caryophyllene thus appears to serve as a defense against pathogens that invade floral tissues and, like other floral volatiles, may play multiple roles in defense and pollinator attraction.
When attacked by insects, plants release mixtures of volatile compounds that are beneficial for direct or indirect defense. Natural variation of volatile emissions frequently occurs between and within plant species, but knowledge of the underlying molecular mechanisms is limited. We investigated intraspecific differences of volatile emissions induced from rosette leaves of 27 accessions of Arabidopsis (Arabidopsis thaliana) upon treatment with coronalon, a jasmonate mimic eliciting responses similar to those caused by insect feeding. Quantitative variation was found for the emission of the monoterpene (E)-b-ocimene, the sesquiterpene (E,E)-a-farnesene, the irregular homoterpene 4,8,12-trimethyltridecatetra-1,3,7,11-ene, and the benzenoid compound methyl salicylate. Differences in the relative emissions of (E)-b-ocimene and (E,E)-a-farnesene from accession Wassilewskija (Ws), a high-(E)-b-ocimene emitter, and accession Columbia (Col-0), a trace-(E)-b-ocimene emitter, were attributed to allelic variation of two closely related, tandem-duplicated terpene synthase genes, TPS02 and TPS03. The Ws genome contains a functional allele of TPS02 but not of TPS03, while the opposite is the case for Col-0. Recombinant proteins of the functional Ws TPS02 and Col-0 TPS03 genes both showed (E)-b-ocimene and (E,E)-a-farnesene synthase activities. However, differential subcellular compartmentalization of the two enzymes in plastids and the cytosol was found to be responsible for the ecotype-specific differences in (E)-b-ocimene/(E,E)-a-farnesene emission. Expression of the functional TPS02 and TPS03 alleles is induced in leaves by elicitor and insect treatment and occurs constitutively in floral tissues. Our studies show that both pseudogenization in the TPS family and subcellular segregation of functional TPS enzymes control the variation and plasticity of induced volatile emissions in wild plant species.
Volatile organic compounds have been reported to serve some important roles in plant communication with other organisms, but little is known about the biological functions of most of these substances. To gain insight into this problem, we have compared diVerences in Xoral and vegetative volatiles between two closely related plant species with diVerent life histories. The self-pollinating annual, Arabidopsis thaliana, and its relative, the outcrossing perennial, Arabidopsis lyrata, have markedly divergent life cycles and breeding systems. We show that these diVerences are in part reXected in the formation of distinct volatile mixtures in Xowers and foliage. Volatiles emitted from
Homeotic changes played a considerable role during the evolution of flowers, but how floral homeotic mutants initially survive in nature has remained enigmatic. To better understand the evolutionary potential of floral homeotic mutants, we established as a model system Stamenoid petals (Spe), a natural variant of Capsella bursa-pastoris (Brassicaceae). In the flowers of Spe plants, petals are transformed into stamens, whereas all other floral organs are unaffected. In contrast with most other homeotic mutants, the Spe variant occurs in relatively stable populations in the wild. In order to determine how the profound change in floral architecture influences plant performance in the wild, we performed common garden experiments running over 3 years. Here, we show that Spe and wild-type plants attract the same assemblage of floral visitors: mainly hoverflies, wild bees and thrips. However, floral visitation is about twice as frequent in wild-type plants as in Spe plants. Nevertheless, the numbers of seeds per fruit were about the same in both variants. Wild-type plants produced more flowers, fruits and seeds per plant than Spe plants, whereas the germination capacity of Spe seeds was higher than that of the wild-type. Determination of volatile composition revealed monoterpenes and 3,4-dimethylbenzaldehyde, which were detected only in wild-type flowers, presumably because they are produced only by petals. Our data indicate that the similar fitness of Spe and wild-type C. bursa-pastoris in the field results from complex compensation between plant architecture and germination capacity. In contrast, flower structure and floral visitation are only of minor importance, possibly because C. bursa-pastoris is mainly self-pollinating.
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