Biology subjects

Zuest, T.

Publications and source records attributed to Zuest, T..

9 recordsLinked to original sources

bioRxiv2025

Evolutionary constraints in host shifts: limited adaptation of Plutella xylostella to cardenolide-defended Erysimum cheiranthoides

O_LIPlants and herbivorous insects are engaged in long-term coevolutionary arms races, where gains in novel plant defences and corresponding adaptations in herbivores may drive evolutionary change. One such recent innovation is the gain of cardenolide toxins in the Brassicaceae genus Erysimum, which resulted in the effective deterrence of most herbivores by these plants. Nonetheless, some herbivores continue to attack Erysimum, likely by tolerating cardenolide defences through general detoxification mechanisms that may serve as evolutionary stepping-stones for more specialized resistance. C_LIO_LIWe investigated the interaction between diamondback moth (DBM, Plutella xylostella) and its occasional host plant E. cheiranthoides, by first screening the standing variation in DBM performance, and second by experimentally evolving DBM populations for increased performance on Erysimum. Despite considerable variation among wild DBM populations, larvae consistently avoided Erysimum leaves for feeding, and when constrained to Erysimum, they exhibited reduced growth rate, survival, and lower adult size compared to individuals feeding on control broccoli plants. C_LIO_LISurprisingly, cardenolides could only partly explain the reduced performance of DBM on Erysimum, and experimental evolution failed to improve overall performance. Instead, phenotypes of evolved lines converged on what appears to be a pre-existing, highly plastic phenotype found among wild DBM ancestors and which is characterized by rapid development and high weight gain on control plants, but slow development and low weight gain on Erysimum. C_LIO_LIAlthough DBM failed to evolve improved performance on Erysimum, our results demonstrate that its existing genetic variation and phenotypic plasticity are evidently sufficient to support long-term development on Erysimum, thereby fulfilling a key condition for the future evolution of specialized adaptations. C_LI

evolutionary biology↗

bioRxiv2025

Synthetic communities of maize root bacteria interact and redirect benzoxazinoid metabolization

Plant roots are colonised by diverse microbial communities. These communities are shaped by root exudates including plant specialized metabolites. Benzoxazinoids are such secreted compounds of maize. Individual microbes differ in their ability to tolerate and metabolize antimicrobial benzoxazinoids. To investigate how these traits combine in a community, we designed two synthetic communities of maize root bacteria that share six common strains and differ in their ability to metabolize benzoxazinoids based on the seventh strain. We exposed both communities to the benzoxazinoid MBOA (6-methoxybenzoxazolin-2(3H)-one) and found that the metabolizing community did not degrade MBOA to its aminophenoxazinone, as observed for individual strains, but as a community they formed the corresponding acetamide. MBOA shaped differential compositions of both communities and increased the fraction of MBOA-tolerant strains. The benzoxazinoid metabolizing community showed a higher tolerance to MBOA and was able to utilize MBOA as their sole carbon source for growth. Hence, bacterial interaction results in alternative benzoxazinoid metabolization and increases community performance in presence of these antimicrobial compounds. Future work is needed to uncover the genetics of this metabolic interaction and ecological consequences for the bacterial community and the host plant. ImportanceWe investigated how maize root bacteria - alone or in community - tolerate and metabolize antimicrobial compounds of their host plant. We found the capacity to metabolize such a compound to impact bacterial community size and structure and most importantly, to beneeit community eitness. We also found that interacting bacteria redirected the metabolisation of the antimicrobial compound to an alternative degradation product. Our work highlights the need to study the team work of microbes to uncover their community traits to ultimately understand the ecological consequences for the bacterial community and eventually the host plant.

microbiology↗

bioRxiv2024

Within-plant variation in chemical defence of Erysimum cheiranthoides does not explain Plutella xylostella feeding preference

O_LIPlants invest a substantial fraction of their resources into defence against herbivores, with the highest levels of defence often allocated only to the most valuable tissues. Plants in the genus Erysimum (Brassicaceae) evolved the ability to produce novel cardenolides in addition to ancestrally conserved glucosinolates. While plants co-express both defences, differences in tissue-specific expression might represent an effective cost saving strategy. C_LIO_LILarvae of the glucosinolate-resistant diamondback moth Plutella xylostella occasionally feed on Erysimum cheiranthoides but tend to avoid younger leaves. Here, we predicted that caterpillar feeding preference is shaped by variation in cardenolide levels, thus we quantified within-plant variation in defensive and nutritional traits of vegetative or early reproductive plants and performed feeding assays to evaluate the relative importance of cardenolides. C_LIO_LIIn accordance with optimal defence theory (ODT), youngest leaves contained the most nutrients and the highest levels of cardenolides, glucosinolates, and trichomes, with more extreme within-plant differences found in reproductive plants. Caterpillars consistently avoided the well-defended youngest leaves both on whole plants and with detached leaf discs. Surprisingly, neither experimental addition (by external application) nor removal (by CRISPR-Cas9 knockout) of cardenolides significantly affected caterpillar feeding preference. C_LIO_LIPhysical and chemical defences, including cardenolides, co-vary within E. cheiranthoides to maximise defence of youngest leaves. While P. xylostella clearly responds to some of these traits, the prominent cardenolide defence appears to lack potency against this specialist herbivore. Nonetheless, the careful regulation and re-mobilization of cardenolides to younger leaves during plant development suggests an important role for plant functioning. C_LI One-sentence summaryDistribution of ancestral and novel defensive chemicals Erysimum cheiranthoides vary within plant according to relative leaf value and leaf age, but in isolation, chemical defences are insufficient to affect feeding preference of Plutella xylostella larvae.

ecology↗

bioRxiv2023

The lactonase BxdA mediates metabolic adaptation of maize root bacteria to benzoxazinoids

Root exudates contain secondary metabolites that affect the plants root microbiome. How microbes cope with these bioactive compounds, and how this ability shapes root microbiomes remain largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound (6-methoxy-benzoxazolin-2-one, MBOA) in the maize rhizosphere to 2-amino-7-methoxyphenoxazin-3-one (AMPO). By contrast, bacteria isolated from Arabidopsis, which does not produce benzoxazinoids, were unable to metabolise MBOA. Among Microbacteria strains, this differential metabolisation allowed to identify a conserved gene cluster containing the lactonase bxdA. BxdA converts MBOA to AMPO in vitro and we show that this capacity provided bacteria a growth benefit under carbon-limiting conditions. Together these results reveal that maize root bacteria - through BxdA - are metabolically adapted to the benzoxazinoids of their host. We propose that metabolic adaptation to plant-specialised compounds shapes root bacterial communities across the plant kingdom.

microbiology↗

bioRxiv2021

Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth

Specialized metabolites mediate important interactions in both the rhizosphere and the phyllosphere. How this compartmentalized multifunctionality influences plant-environment interactions is unknown. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth in soils with low bioavailable iron but enhance growth in soils with higher bioavailable iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions but enhance herbivore growth when iron is present in its free form. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with major consequences for plant health in variable environments.

plant biology↗

bioRxiv2020

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↗

bioRxiv2020

Less Is More: A Mutation in the Chemical Defense Pathway of Erysimum cheiranthoides (Brassicaceae) Reduces Total Cardenolide Abundance but Increases Resistance to Insect Herbivores

Many plants produce structurally related defensive metabolites with the same target sites in insect herbivores. Two possible drivers of this chemical diversity are: (i) interacting effects of structurally related compounds increase resistance against individual herbivores, and (ii) variants of the same chemical structures differentially affect diverse herbivore species or feeding guilds. Erysimum cheiranthoides L (Brassicaceae; wormseed wallflower) produces abundant and diverse cardenolide toxins, which are derived from digitoxigenin, cannogenol, and strophanthidin, all of which inhibit Na+/K+-ATPases in animal cells. Here we describe an E. cheiranthoides mutant with 66% lower cardenolide content, resulting from greatly decreased cannogenol- and strophanthidin-derived cardenolides, partially compensated for by increases in digitoxigenin-derived cardenolides. This compositional change created a more even cardenolide distribution, decreased the average cardenolide polarity, but did not impact glucosinolates, a different class of chemical defenses. Growth of generalist herbivores from two feeding guilds, Myzus persicae Sulzer (Hemiptera: Aphididae; green peach aphid) and Trichoplusia ni Hubner (Lepidoptera: Noctuidae; cabbage looper), was decreased on the mutant line compared to wildtype. Both herbivores accumulated cardenolides in proportion to plant content, with T. ni accumulating higher total concentrations than M. persicae. Helveticoside, an abundant cardenolide in E. cheiranthoides, was absent in M. persicae, suggesting that this compound is not present in the phloem. Our results support the hypothesis that cardenolide diversity protects plants against different herbivores, with digitoxigenin-derived compounds providing better protection against insects like M. persicae and T. ni, whereas cannogenol and strophanthidin provide better protection against other herbivores of E. cheiranthoides. FundingThis research was funded by US National Science Foundation awards 1907491 to AAA and 1645256 to GJ and AAA, Swiss National Science Foundation grant PZ00P3-161472 to TZ, and a Triad Foundation grant to GJ.

ecology↗

bioRxiv2020

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↗

bioRxiv2020

Variation in root secondary metabolites is shaped by past climatic conditions

O_LIPlants can adapt to changing environments by adjusting the production and maintenance of diverse sets of bioactive secondary metabolites. To date, the impact of past climatic conditions relative to other factors such as soil abiotic factors and herbivore pressure on the evolution of plant secondary metabolites is poorly understood, especially for plant roots. C_LIO_LIWe explored associations between root latex secondary metabolites in 63 Taraxacum officinale populations across Switzerland and past climatic conditions, soil abiotic parameters, and root herbivore pressure. To assess the contribution of environmental effects, root secondary metabolites were measured in F0 plants in nature and F2 plants under controlled greenhouse conditions. C_LIO_LIConcentrations of root latex secondary metabolites were most strongly associated with past climatic conditions, while current soil abiotic factors or root herbivore pressure did not show a clear association with root latex chemistry. Results were identical for natural and controlled conditions, suggesting heritable trait variation rather than environmental plasticity as underlying factor. C_LIO_LISynthesis. We conclude that climatic conditions likely play a major role in the evolution of root secondary metabolites. Direct abiotic effects are likely underlying this pattern, hinting at a novel role of root latex metabolites the tolerance of abiotic stress. C_LI

ecology↗