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Machado, R. A. R.

Publications and source records attributed to Machado, R. A. R..

7 recordsLinked to original sources

Photorhabdus metabolites reshape soil microbial communities and promote plant growth and insect resistance

Photorhabdus bacteria are potent insect-killing microbes associated with entomopathogenic nematodes and offer opportunities for environmentally benign pest control. They can be applied as foliar sprays or soil drenches without their nematode vector, resulting in massive amounts of Photorhabdus cells and their (toxic) metabolites introduced into the soil. However, their effects beyond the target organisms are unknown. To fill this knowledge gap, we investigated the soil legacy effects of Photorhabdus cells and their metabolites on soil microbial communities, plant performance and resistance to herbivores. To this end, we first conditioned soils with i) mechanically killed (MK) or Photorhabdus-infected insect larvae, ii) aqueous extracts of MK or Photorhabdus-infected insect larvae, iii) cell-free Photorhabdus supernatants, iv) autoclaved soil complemented with live soil previously conditioned with MK or Photorhabdus-infected insect larvae. We then grew maize plants in these soils and measured plant biomass, profiled soil microbial communities and plant metabolites, and evaluated plant resistance against two pest insects Diabrotica balteata and Spodoptera frugiperda. We found that conditioned soils increased plant biomass by 10-26% relative to controls and significantly altered soil bacterial and nematode communities, and to a lesser extent, fungal communities. Re-inoculating conditioned soil microbiota into autoclaved soils recreated the plant growth-promoting effects, indicating microbial-mediated mechanisms. Additionally, plants grown in soils conditioned with Photorhabdus-infected insect cadavers were often more resistant to herbivorous insect attack, in a strain-specific manner. On average, D. balteata and S. frugiperda larvae gained 10-20% and 10-59% less weight, respectively, when fed on plants grown in conditioned soils than on plants grown in control soils. The plant metabolic profiles of plant leaves and roots also varied with resistance levels. We conclude that Photorhabdus metabolites modulate soil microbial communities towards a structure that enhances plant growth and triggers systemic responses against herbivores.

microbiology↗

Adaptations and responses of the common dandelion to low atmospheric pressure in high altitude environments

Atmospheric pressure is an important, yet understudied factor that may shape plant ecology and evolution. By growing plants under controlled conditions at different experimental stations in the Swiss alps, we evaluated the impact of ecologically realistic atmospheric pressures between 660 and 950 hPa on the growth and defence of different dandelion populations. Low atmospheric pressure was associated with reduced root growth and defensive sesquiterpene lactone production. Defense suppression only occurred in populations originating from lower altitudes. Populations from higher altitudes constitutively produced less sesquiterpene lactones and did not suffer from suppression under low atmospheric pressure. We conclude that atmospheric pressure modulates root growth and defence traits, and that evolutionary history shapes plant phenotypic responses to atmospheric pressure. Our findings have important implications for our understanding of altitudinal gradients and the future use of plants as a source of food and bioactive metabolites in extraterrestrial habitats.

plant biology↗

Integration of plant primary and secondary metabolites as fitness-relevant foraging cues for a specialist herbivore

Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores integrate different metabolite classes into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting sugar perception in the western corn rootworm and benzoxazinoid production in maize, we show that sugars and benzoxazinoids act as distinct and dynamically integrated mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish post-embryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to post-embryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants even when both classes of chemical cues are almost completely absent. This study unravels fine-grained differentiation and integration of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the lack of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

animal behavior and cognition↗

Plant-derived CO2 mediates long-distance host location and quality assessment by a root herbivore

Insect herbivores can use volatile and visual cues to locate and select suitable host plants from a distance. The importance of CO2, arguable the most conserved volatile marker of metabolic activity, is not well understood in this context, even though many herbivores are known to respond to minute differences in CO2 concentrations. To address this gap of knowledge, we manipulated CO2 perception of the larvae of the western corn rootworm (Diabrotica virgifera virgifera; WCR) through RNA interference and studied how CO2 perception impacts their interaction with their host plant, maize (Zea mays). We show that the expression of a putative Group 2 carbon dioxide receptor, DvvGr2, is specifically required for dose-dependent larval responses to CO2 in the ppm range. Silencing DvvGr2 has no effect on the ability of WCR larvae to locate host plants at short distance (<9 cm), but impairs host location at greater distances. Using soil arenas and olfactometer experiments in combination with DvvGr2 silencing and CO2 scrubbing, we demonstrate that WCR larvae use CO2 as a long-range host plant finding cue, but employ other volatiles for short-range host location. We furthermore show that the larvae use CO2 as a fitness-relevant long-distance indicator of plant nutritional status: Maize plants that are well-fertilized emit more CO2 from their roots and are better hosts for WCR than plants that are nutrient-deficient, and the capacity of WCR larvae to distinguish between these plants depends exclusively on their capacity to perceive CO2 through DvvGr2. This study unravels how CO2 can mediate plant-herbivore interactions by serving as a distance-dependent host location and quality assessment cue.

ecology↗

Tissue-specific volatile-mediated defense regulation in maize leaves and roots

O_LIPlant leaves that are exposed to herbivore induced plant volatiles (HIPVs) respond by increasing their defenses. Whether this phenomenon also occurs in the roots is unknown. C_LIO_LIUsing maize (Zea mays), whose leaves respond strongly to leaf HIPVs, we measured the impact of root HIPVs, emanating from plants infested by the banded cucumber beetle (Diabrotica balteata), on constitutive and herbivore-induced levels of root soluble sugars, starch, total soluble proteins, free amino acids, volatile and non-volatile secondary metabolites, defense gene expression, growth and root herbivore resistance of neighboring plants. C_LIO_LIHIPV exposure did not alter constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance and survival of banded cucumber beetle larvae on maize or teosinte. Cross-exposure experiments revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense-regulating HIPVs. C_LIO_LITogether, these results demonstrate that volatile-mediated defense regulation is restricted to the leaves of maize and teosinte, a finding which is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient information conduits below ground. C_LI

plant biology↗

Identification of Photorhabdus symbionts by MALDI-TOF mass spectrometry

Species of the bacterial genus Photorhabus live in a symbiotic relationship with Heterorhabditis entomopathogenic nematodes. Besides their use as biological control agents against agricultural pests, some Photorhabdus species are also a source of natural products and are of medical interest due to their ability to cause tissue infections and subcutaneous lesions in humans. Given the diversity of Photorhabdus species, rapid and reliable methods to resolve this genus to the species level are needed. In this study, we evaluated the potential of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) for the identification of Photorhabdus species. To this end, we established a collection of 54 isolates consisting of type strains and multiple field strains that belong to each of the validly described species and subspecies of this genus. Reference spectra for the strains were generated and used to complement a currently available database. The extended reference database was then used for identification based on the direct transfer sample preparation method and protein fingerprint of single colonies. High discrimination of distantly related species was observed. However, lower discrimination was observed with some of the most closely related species and subspecies. Our results, therefore, suggest that MALDI-TOF MS can be used to correctly identify Photorhabdus strains at the genus and species level, but has limited resolution power for closely related species and subspecies. Our study demonstrates the suitability and limitations of MALDI-TOF-based identification methods for the assessment of the taxonomical position and identification of Photorhabdus isolates. Impact StatementSpecies of the bacterial genus Photorhabus live in close association with soil-born entomopathogenic nematodes. Under natural conditions, these bacteria are often observed infecting soil-associated arthropods, but under certain circumstances, can also infect humans. They produce a large variety of natural products including antibiotics, insecticides, and polyketide pigments that have substantial agricultural, biotechnological and medical potential. In this study, we implement MALDI-TOF MS-based identification method to resolve the taxonomic identity of this bacterial genus, providing thereby a rapid identification tool to understanding its taxonomic diversity to boost scientific progress in medical, agricultural, and biotechnological settings.

microbiology↗

Plant defense resistance in natural enemies of a specialist insect herbivore

Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 years are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective towards the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for five generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity towards the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity towards a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a novel target for the improvement of biological control agents.

plant biology↗