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Koellner, T. G.

Publications and source records attributed to Koellner, T. G..

5 recordsLinked to original sources

Biosynthesis of iridoid sex pheromones in aphids

Iridoid monoterpenes, widely distributed in plants and insects, have many ecological functions. While the biosynthesis of iridoids has been extensively studied in plants, little is known about how insects synthesize these natural products. Here, we elucidated the biosynthesis of the iridoids cis-trans-nepetalactol and cis-trans-nepetalactone in the pea aphid Acyrthosiphon pisum [Harris], where they act as sex pheromones. The exclusive production of iridoids in hind legs of sexual female aphids allowed us to identify iridoid genes by searching for genes specifically expressed in this tissue. Biochemical characterization of candidate enzymes revealed that the iridoid pathway in aphids proceeds through the same sequence of intermediates as described for plants. The six identified aphid enzymes are unrelated to their counterparts in plants, conclusively demonstrating an independent evolution of the entire iridoid pathway in plants and insects. In contrast to the plant pathway, at least three of the aphid iridoid enzymes are likely membrane-bound. We demonstrated that a lipid environment facilitates the cyclization of a reactive enol intermediate to the iridoid cyclopentanoid-pyran scaffold in vitro, suggesting that membranes are an essential component of the aphid iridoid pathway. Altogether, our discovery of this complex insect metabolic pathway establishes the genetic and biochemical basis for the formation of iridoid sex pheromones in aphids and this discovery also serves as a foundation for understanding the convergent evolution of complex metabolic pathways between kingdoms. Significance StatementPlants, animals and microbes produce a plethora of natural products that are important for defense and communication. Most of these compounds show a phylogenetically restricted occurrence, but in rare instances, the same natural product is biosynthesized by organisms in two different kingdoms. The monoterpene-derived iridoids, for example, have been found in more than 50 plant families, but are also observed in several insect orders. The aphid iridoid pathway discovered in this study, one of the longest and most chemically complex insect-derived natural product biosynthetic pathways reported to date, is compared with iridoid biosynthetic pathways in plants and highlights the mechanisms underlying the convergent evolution of metabolic enzymes in insects and plants.

biochemistry↗

Allelic differences of clustered terpene synthases contribute to correlated intra-specific variation of floral and herbivory induced volatiles in a wild tobacco

O_LIPlant volatile emissions can recruit predators of herbivores for indirect defence and attract pollinators to aid in pollination. Although volatiles involved in defence and pollinator attraction are primarily emitted from leaves and flowers, respectively, they will co-evolve if their underlying genetic basis is intrinsically linked, either due to pleiotropy or genetic linkage. However, direct evidence of co-evolving defence and floral traits is scarce. C_LIO_LIWe characterized intra-specific variation of herbivory-induced plant volatiles (HIPVs), the key components of indirect defence against herbivores, and floral volatiles in the wild tobacco Nicotiana attenuata. C_LIO_LIWe found that variation of (E)-{beta}-ocimene and (E)--bergamotene contributed to the correlated changes in HIPVs and floral volatiles among N. attenuata natural accessions. Intra-specific variations of (E)-{beta}-ocimene and (E)--bergamotene emissions resulted from allelic variation of two genetically co-localized terpene synthase genes, NaTPS25 and NaTPS38 respectively. C_LIO_LIAnalyzing haplotypes of NaTPS25 and NaTPS38 revealed that allelic variations of NaTPS25 and NaTPS38 resulted in correlated changes of (E)-{beta}-ocimene and (E)--bergamotene emission in HIPVs and floral volatiles in N. attenuata. C_LIO_LITogether, these results provide evidence that pleiotropy and genetic linkage result in correlated changes in defences and floral signals in natural populations, and the evolution of plant volatiles is likely under diffuse selection. C_LI

evolutionary biology↗

Evolution of a novel and adaptive floral scent in wild tobacco

Many plants emit diverse floral scents that mediate plant-environment interactions and attain reproductive success. However, how plants evolve novel adaptive floral volatiles remains unclear. Here, we show that in the wild tobacco, Nicotiana attenuata, a dominant species-specific floral volatile (benzyl acetone, BA) that attracts pollinators and deters florivore is synthesized by phenylalanine ammonia-lyase 4 (NaPAL4), isoflavone reductase 3 (NaIFR3), and chalcone synthase 3 (NaCHAL3). Transient expression of NaFIR3 alone in N. attenuata leaves is sufficient and necessary for ectopic foliar BA emissions, and the BA emission level is increased by co-expressing NaIFR3 with NaPAL4 and NaCHAL3. Independent changes in transcription in all three genes contributed to intraspecific variations of floral BA emission. However, among species, the gain-of-expression in NaIFR3 resulted in the biosynthesis of BA that was only found in N. attenuata. This study suggests that novel metabolic pathways associated with adaptation can arise via re-configurations of gene expression.

evolutionary biology↗

A light-dependent molecular link between competition cues and defense responses in plants

One of the principal internal signals controlling plant growth and defense is jasmonate (JA), a potent growth inhibitor that is simultaneously a central regulator of plant immunity to herbivores and pathogens. When shade-intolerant plants perceive the proximity of competitors using the photoreceptor phytochrome B (phyB), they accelerate growth and down-regulate JA responses. However, the mechanisms by which photoreceptors relay light cues to the JA signaling pathway are not understood. Here we identify a sulfotransferase (ST2a) that is strongly up-regulated by plant proximity perceived by phyB via the phyB-Phytochrome Interacting Factor (PIF) signaling module. By catalyzing the formation of a sulfated JA derivative, ST2a acts to degrade bioactive forms of JA and represents a direct molecular link between photoreceptors and hormone signaling in plants. The enzyme provides a molecular mechanism for prioritizing shade avoidance over defense under close plant competition.

plant biology↗

Root volatiles in plant-plant interactions I: Characterization of root sesquiterpene emissions from Centaurea stoebe and their effects on other plants

Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighboring plants. In contrast to interactions above ground, little is known about the role of VOCs in belowground plant-plant interactions. Here, we characterize constitutive root volatile emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these volatiles on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release rates of (E)-{beta}-caryophyllene above 3 g g-1 dw h-1. Sesquiterpene emissions show little variation between different C. stoebe populations, but vary substantially between different Centaurea species. Through root transcriptome sequencing, we identify six root-expressed sesquiterpene synthases (TPSs). Two root-specific TPSs, CsTPS4 and CsTPS5, are sufficient to produce the full blend of emitted root sesquiterpenes. Volatile exposure experiments demonstrate that C. stoebe root volatiles have neutral to positive effects on the germination and growth of different sympatric neighbors. Thus, constitutive root sesquiterpenes produced by two C. stoebe TPSs are associated with facilitation of sympatric neighboring plants. The release of root VOCs may thus influence C. stoebe abundance and plant community structure in nature.

plant biology↗