The role of primary metabolism in plant resistance against herbivory: a study with the native annual Nicotiana attenuata

Pflanzen haben im Laufe einer langen Koevolution mit Herbivoren verschiedene Mechanismen entwickelt, um das Ausmaß und die Auswirkungen von Biomassenschädigung und -verlust durch Herbivorie zu verringern. Direkte und indirekte Verteidigung reduzieren den Schaden an der Pflanze, indem Herbivoren mit mechanischer Abwehr (z. B. Dornen) abgewehrt, mit chemisch-physiologischer Abwehr (Nervengiften wie Nikotin oder verdauungshemmenden Proteinen, Proteaseinhibitoren) in ihrer Entwicklung gestört werden, oder indem die Pflanze durch Abgabe flüchtiger Verbindungen Fraßfeinde oder Parasitoiden von Herbivoren anlockt. Die Untersuchung dieser Mechanismen erfährt heute ein zunehmend starkes Interesse, weniger gut untersucht ist jedoch, inwieweit es Pflanzen möglich ist, nicht nur die Schädigung an sich, sondern auch die negativen Auswirkungen eines bereits eingetretenen Schadensereignisses abzumildern, oder sogar ein bestimmtes Ausmaß an Schaden ohne (Darwin´sche) Fitnessverluste hinzunehmen. Diese - im Allgemeinen als Toleranz bezeichnete - Pflanzenantwort kann auf unterschiedlichen Mechanismen beruhen, die größtenteils nur theoretisch beschrieben sind

The role of primary metabolism in plant resistance against herbivory: a study with the native annual Nicotiana attenuata

Pflanzen haben im Laufe einer langen Koevolution mit Herbivoren verschiedene Mechanismen entwickelt, um das Ausmaß und die Auswirkungen von Biomassenschädigung und -verlust durch Herbivorie zu verringern. Direkte und indirekte Verteidigung reduzieren den Schaden an der Pflanze, indem Herbivoren mit mechanischer Abwehr (z. B. Dornen) abgewehrt, mit chemisch-physiologischer Abwehr (Nervengiften wie Nikotin oder verdauungshemmenden Proteinen, Proteaseinhibitoren) in ihrer Entwicklung gestört werden, oder indem die Pflanze durch Abgabe flüchtiger Verbindungen Fraßfeinde oder Parasitoiden von Herbivoren anlockt. Die Untersuchung dieser Mechanismen erfährt heute ein zunehmend starkes Interesse, weniger gut untersucht ist jedoch, inwieweit es Pflanzen möglich ist, nicht nur die Schädigung an sich, sondern auch die negativen Auswirkungen eines bereits eingetretenen Schadensereignisses abzumildern, oder sogar ein bestimmtes Ausmaß an Schaden ohne (Darwin´sche) Fitnessverluste hinzunehmen. Diese - im Allgemeinen als Toleranz bezeichnete - Pflanzenantwort kann auf unterschiedlichen Mechanismen beruhen, die größtenteils nur theoretisch beschrieben sind

Oviposition by Spodoptera exigua on Solanum dulcamara Alters the Plant’s Response to Herbivory and Impairs Larval Performance

Plant resistance traits against insect herbivores are extremely plastic. Plants respond not only to the herbivory itself, but also to oviposition by herbivorous insects. How prior oviposition affects plant responses to larval herbivory is largely unknown. Combining bioassays and defense protein activity assays with microarray analyses and metabolite profiling, we investigated the impact of preceding oviposition on the interaction of Solanum dulcamara with the generalist lepidopteran herbivore Spodoptera exigua at the levels of the plant’s resistance, transcriptome and metabolome. We found that oviposition increased plant resistance to the subsequent feeding larvae. While constitutive and feeding-induced levels of defensive protease inhibitor activity remained unaffected, pre-exposure to eggs altered S. dulcamara’s transcriptional and metabolic response to larval feeding in leaves local and systemic to oviposition. In particular, genes involved in phenylpropanoid metabolism were more strongly expressed in previously oviposited plants, which was reflected by reciprocal changes of primary metabolites upstream and within these pathways. Our data highlight that plants integrate signals from non-threatening life stages of their natural enemies to optimize their response when they become actually attacked. The observed transcriptional and metabolic reshaping of S. dulcamara’s response to S. exigua herbivory suggests a role of phenylpropanoids in oviposition-primed plant resistance

Induced, Imprinted, and Primed Responses to Changing Environments: Does Metabolism Store and Process Information?

Metabolism is the system layer that determines growth by the rate of matter uptake and conversion into biomass. The scaffold of enzymatic reaction rates drives the metabolic network in a given physico-chemical environment. In response to the diverse environmental stresses, plants have evolved the capability of integrating macro- and micro-environmental events to be prepared, i.e., to be primed for upcoming environmental challenges. The hierarchical view on stress signaling, where metabolites are seen as final downstream products, has recently been complemented by findings that metabolites themselves function as stress signals. We present a systematic concept of metabolic responses that are induced by environmental stresses and persist in the plant system. Such metabolic imprints may prime metabolic responses of plants for subsequent environmental stresses. We describe response types with examples of biotic and abiotic environmental stresses and suggest that plants use metabolic imprints, the metabolic changes that last beyond recovery from stress events, and priming, the imprints that function to prepare for upcoming stresses, to integrate diverse environmental stress histories. As a consequence, even genetically identical plants should be studied and understood as phenotypically plastic organisms that continuously adjust their metabolic state in response to their individually experienced local environment. To explore the occurrence and to unravel functions of metabolic imprints, we encourage researchers to extend stress studies by including detailed metabolic and stress response monitoring into extended recovery phases

Reverse Genetics in Ecological Research

By precisely manipulating the expression of individual genetic elements thought to be important for ecological performance, reverse genetics has the potential to revolutionize plant ecology. However, untested concerns about possible side-effects of the transformation technique, caused by Agrobacterium infection and tissue culture, on plant performance have stymied research by requiring onerous sample sizes. We compare 5 independently transformed Nicotiana attenuata lines harboring empty vector control (EVC) T-DNA lacking silencing information with isogenic wild types (WT), and measured a battery of ecologically relevant traits, known to be important in plant-herbivore interactions: phytohormones, secondary metabolites, growth and fitness parameters under stringent competitive conditions, and transcriptional regulation with microarrays. As a positive control, we included a line silenced in trypsin proteinase inhibitor gene (TPI) expression, a potent anti-herbivore defense known to exact fitness costs in its expression, in the analysis. The experiment was conducted twice, with 10 and 20 biological replicates per genotype. For all parameters, we detected no difference between any EVC and WT lines, but could readily detect a fitness benefit of silencing TPI production. A statistical power analyses revealed that the minimum sample sizes required for detecting significant fitness differences between EVC and WT was 2–3 orders of magnitude larger than the 10 replicates required to detect a fitness effect of TPI silencing. We conclude that possible side-effects of transformation are far too low to obfuscate the study of ecologically relevant phenotypes

A Naturally Associated Rhizobacterium of Arabidopsis thaliana Induces a Starvation-Like Transcriptional Response while Promoting Growth

Plant growth promotion by rhizobacteria is a known phenomenon but the underlying mechanisms are poorly understood. We searched for plant growth-promoting rhizobacteria that are naturally associated with Arabidopsis thaliana to investigate the molecular mechanisms that are involved in plant growth-promotion. We isolated a Pseudomonas bacterium (Pseudomonas sp. G62) from roots of field-grown Arabidopsis plants that has not been described previously and analyzed its effect on plant growth, gene expression and the level of sugars and amino acids in the host plant. Inoculation with Pseudomonas sp. G62 promoted plant growth under various growth conditions. Microarray analysis revealed rapid changes in transcript levels of genes annotated to energy-, sugar- and cell wall metabolism in plants 6 h after root inoculation with P. sp. G62. The expression of several of these genes remained stable over weeks, but appeared differentially regulated in roots and shoots. The global gene expression profile observed after inoculation with P. sp. G62 showed a striking resemblance with previously described carbohydrate starvation experiments, although plants were not depleted from soluble sugars, and even showed a slight increase of the sucrose level in roots 5 weeks after inoculation. We suggest that the starvation-like transcriptional phenotype - while steady state sucrose levels are not reduced - is induced by a yet unknown signal from the bacterium that simulates sugar starvation. We discuss the potential effects of the sugar starvation signal on plant growth promotion

Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata

Exposure to smoke is required for the germination of seeds from dormant genotypes of Nicotiana attenuata, a post-fire annual of the Great Basin Desert. Germination can be elicited by GA(1,3,4,7) treatments and inhibited by the GA biosynthesis inhibitor