Phenotypic plasticity in plant defense across life stages: Inducibility, transgenerational induction, and transgenerational priming in wild radish

As they develop, many plants deploy shifts in antiherbivore defense allocation due to changing costs and benefits of their defensive traits. Plant defenses are known to be primed or directly induced by herbivore damage within generations and across generations by long-lasting epigenetic mechanisms. However, little is known about the differences between life stages of epigenetically inducible defensive traits across generations. To help fill this knowledge gap, we conducted a multigenerational experiment to determine whether defense induction in wild radish plants was reflected in chromatin modifications (DNA methylation); we then examined differences between seedlings and reproductive plants in current and transgenerational plasticity in chemical (glucosinolates) and physical (trichomes) defenses in this species. Herbivory triggered genome methylation both in targeted plants and their offspring. Within one generation, both defenses were highly inducible at the seedling stage, but only chemical defenses were inducible in reproductive plants. Across generations, herbivory experienced by mother plants caused strong direct induction of physical defenses in their progeny, with effects lasting from seedling to reproductive stages. For chemical defenses, however, this transgenerational induction was evident only in adults. Transgenerational priming was observed in physical and chemical defenses, particularly in adult plants. Our results show that transgenerational plasticity in plant defenses in response to herbivore offense differs for physical and chemical defense and changes across plant life stages.

The green thorns of Ulex europaeus play both defensive and photosynthetic roles: consequences for predictions of the Enemy Release Hypothesis

Ulex europaeus , a thorny shrub native to NW Europe, is one of the worst invasive species worldwide. The mechanisms underlying its invasive success are not completely understood. According to the Enemy Release Hypothesis (ERH), lower pressure by vertebrate herbivores in the invaded areas should lead to lower investment in physical defenses, allowing the plant to invest more in growth and/or reproduction. However, antiherbivore physical defenses in U. europaeus (thorns) are also the main photosynthetic tissue of the plant. Therefore, reduced investment in thorns could compromise growth of Ulex europaeus in the invaded range. We hypothesized that changes in physical defenses of U. europaeus in invaded ranges should reflect reduced effectiveness (e.g., softer, and more palatable tissues) but not reduced biomass allocation. We compared U. europaeus plants from the invaded (Chile) and native (Spain) ranges of distribution regarding: i) spinescence traits (thorn length, width, biomass, slenderness and bending strength) in adult plants, ii) thorn fiber content and digestibility (as proxies for palatability) in adult plants, and iii) spine density in seedlings grown in a common garden. As expected, plants in the invaded range invested more mass in larger thorns, which contained less cellulose, were slenderer and easier to bend than those from plants in the native range. Likewise, seedlings from the invaded range showed lower spine density and more diameter growth, thus supporting the ERH. Our study shows functional changes in spinescence traits between distribution ranges that account for the fact that thorns are both defensive and photosynthetic organs in U. europaeus, and these changes may contribute to explain its invasiveness.

Higher Elevations Tend to Have Higher Proportion of Plant Species With Glandular Trichomes

Glandular trichomes are well known to participate in plant chemical and physical defenses against herbivores, especially herbivorous insects. However, little is known about large-scale geographical patterns in glandular trichome occurrence. Herbivory pressure is thought to be higher at low elevations because of warmer and more stable climates. We therefore predicted a higher proportion of species with glandular trichomes at low elevations than at higher elevations. We compiled glandular trichome data (presence/absence) for 6,262 angiosperm species from the Hengduan Mountains (a global biodiversity hotspot in southwest China). We tested the elevational gradient (800–5,000 m a.s.l.) in the occurrence of plant species with glandular trichomes, and its correlations with biotic (occurrence of herbivorous insects) and abiotic factors, potentially shaping the elevational gradient in the occurrence of glandular trichomes. We found a significantly positive relationship between elevation and the occurrence of glandular trichomes, with the proportion of species having glandular trichomes increasing from 11.89% at 800 m a.s.l. to 17.92% at above 4,700 m. This cross-species relationship remained significant after accounting for phylogenetic relationships between species. Herbivorous insect richness peaked at mid-elevations and its association with the incidence of glandular trichomes was weak. Mean annual temperature was the most important factor associated negatively with glandular trichomes. Our results do not support the hypothesis that plant defenses decrease with increasing elevation. In contrast, a higher proportion of plant species with glandular trichome toward higher elevations is observed. Our results also highlight the importance of considering the simultaneous influences of biotic and abiotic factors in testing geographical variation in multifunctional plant defenses.

The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions

There is no argument to the fact that insect herbivores cause significant losses to plant productivity in both natural and agricultural ecosystems. To counter this continuous onslaught, plants have evolved a suite of direct and indirect, constitutive and induced, chemical and physical defenses, and secondary metabolites are a key group that facilitates these defenses. Polyphenols—widely distributed in flowering plants—are the major group of such biologically active secondary metabolites. Recent advances in analytical chemistry and metabolomics have provided an opportunity to dig deep into extraction and quantification of plant-based natural products with insecticidal/insect deterrent activity, a potential sustainable pest management strategy. However, we currently lack an updated review of their multifunctional roles in insect-plant interactions, especially focusing on their insect deterrent or antifeedant properties. This review focuses on the role of polyphenols in plant-insect interactions and plant defenses including their structure, induction, regulation, and their anti-feeding and toxicity effects. Details on mechanisms underlying these interactions and localization of these compounds are discussed in the context of insect-plant interactions, current findings, and potential avenues for future research in this area.

Nectar bacteria stimulate pollen germination and bursting to enhance their fitness

For many flower visitors, pollen is the primary source of non-carbon nutrition, but pollen has physical defenses that make it difficult for consumers to access nutrients. Nectar-dwelling microbes are nearly ubiquitous among flowers and can reach high densities, despite the fact that floral nectar is nitrogen limited, containing only very low concentrations of non-carbon nutrients. Pollen contains trace micronutrients and high protein content but is protected by a recalcitrant outer shell. Here, we report that a common genus of nectar-dwelling bacteria, Acinetobacter, exploits pollen nutrition by inducing pollen germination and bursting. We use time course germination assays to quantify the effect of Acinetobacter species on pollen germination and pollen bursting. Inoculation with Acinetobacter species resulted in increased germination rates within 15 minutes, and bursting by 45 minutes, as compared to uninoculated pollen. The pollen germination and bursting phenotype is density-dependent, with lower concentrations of A. pollinis SCC477 resulting in a longer lag time before the spike in germination, which is then closely followed by a spike in bursting. Lastly, A. pollinis grows to nearly twice the density with germinable pollen vs ungerminable pollen, indicating that their ability to induce and exploit germination plays an important role in rapid growth. To our knowledge, this is the first direct test of non-plant biological induction of pollen germination, as well as the first evidence of induced germination as a method of nutrient procurement, as the microbes appear to hijack the pollens normally tightly controlled germination mechanisms for their benefit. Our results suggest that further study of microbe-pollen interactions may inform many aspects of pollination ecology, including microbial ecology in flowers, the mechanisms of pollinator nutrient acquisition from pollen, and cues of pollen germination for plant reproduction.

Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape

The recent introduction in a tropical agricultural environment of a weedy open-habitat plant (Solanum myriacanthum) and subsequent host range expansion of a common forest-edge butterfly (Mechanitis menapis) onto that plant provides an opportunity to examine reconfiguration of tritrophic networks in human-impacted landscapes. The objectives of this study were (1) determine if the caterpillars on the exotic host are more or less limited by plant defenses (bottom-up forces) and if they experience enemy release (decrease of top-down pressure) and (2) define how anthropic open pasture habitat influences the herbivore’s tritrophic niche. Field and laboratory monitoring of larval survival and performance on a native (Solanum acerifolium) host plant and the exotic (S. myriacanthum) host plant were conducted in the Mindo Valley, Ecuador. Plant physical defenses were also measured. Results showed that larval mortality was mostly top-down on S. acerifolium, linked to parasitism, but mostly bottom-up on S. myriacanthum, possibly linked to observed increased plant defenses. Thus, in the absence of co-evolved relationships, herbivores on the exotic host experienced little top-down regulation, but stronger bottom-up pressures from plant defenses. These findings provide a rare empirical example of enemy-free space as a mechanism underlying host-range expansion. S. myriacanthum was less colonized in open pastures than in semi-shaded habitats (forest edges, thickets): fewer eggs were found, suggesting limited dispersal of adult butterflies into the harsh open environments, and the survival rate of first instar larvae was lower than on semi-shaded plants, likely linked to the stronger defenses of sun-grown leaves. These findings show how environmental conditions modulate the rewiring of trophic networks in heavily impacted landscapes, and limit a biocontrol by a native herbivore on an invasive plant in open habitats.

Comparative transcriptomic and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids

Background: Young wheat plants are continuously exposed to herbivorous insect attack. To reduce insect damage and maintain their growth, plants evolved different defense mechanisms, including the biosynthesis of deterrent compounds named benzoxazinoids, and/or trichome formation that provides physical barriers. It is unclear whether both of these mechanisms are equally critical in providing an efficient defense for wheat seedlings against aphids—an economically costly pest in cereal production. Results: In this study, we compared the transcriptome, metabolome, benzoxazinoids, and trichome density of three selected wheat genotypes, with a focus on differences related to defense mechanisms. We chose diverse wheat genotypes: two tetraploid wheat genotypes, domesticated durum ‘Svevo’ and wild emmer ‘Zavitan,’ and one hexaploid bread wheat, ‘Chinese Spring.’ The full transcriptomic analysis revealed a major difference between the three genotypes, while the clustering of significantly different genes suggested a higher similarity between the two domesticated wheats than between either and the wild wheat. A pathway enrichment analysis indicated that the genes associated with primary metabolism, as well as the pathways associated with defense such as phytohormones and specialized metabolites, were different between the three genotypes. Measurement of benzoxazinoid levels at the three time points (11, 15, and 18 days after germination) revealed high levels in the two domesticated genotypes, while in wild emmer wheat, they were below detection level. In contrast to the benzoxazinoid levels, the trichome density was dramatically higher in the wild emmer than in the domesticated wheat. Lastly, we tested the bird cherry-oat aphid’s ( Rhopalosiphum padi ) performance and found that Chinese Spring is more resistant than the tetraploid genotypes. Conclusions: Our results show that benzoxazinoids play a more significant defensive role than trichomes. Differences between the abundance of defense mechanisms in the wild and domesticated plants were observed in which wild emmer possesses high physical defenses while the domesticated wheat genotypes have high chemical defenses. These findings provide new insights into the defense adaptations of wheat plants against aphids.

Comparative transcriptomic and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids

Background Young wheat plants are continuously exposed to herbivorous insect attack. To reduce insect damage and maintain their growth, plants evolved different defense mechanisms, including the biosynthesis of deterrent compounds named benzoxazinoids, and/or trichome formation that provides physical barriers. It is unclear whether both of these mechanisms are equally critical in providing an efficient defense for wheat seedlings against aphids—an economically costly pest in cereal production. Results: In this study, we compared the transcriptome, metabolome, benzoxazinoids, and trichome density of three selected wheat genotypes, with a focus on differences related to defense mechanisms. We chose diverse wheat genotypes: two tetraploid wheat genotypes, domesticated durum ‘Svevo’ and wild emmer ‘Zavitan,’ and one hexaploid bread wheat, ‘Chinese Spring.’ The full transcriptomic analysis revealed a major difference between the three genotypes, while the clustering of significantly different genes suggested a higher similarity between the two domesticated wheats than between either and the wild wheat. A pathway enrichment analysis indicated that the genes associated with primary metabolism, as well as the pathways associated with defense such as phytohormones and specialized metabolites, were different between the three genotypes. Measurement of benzoxazinoid levels at the three time points (11, 15, and 18 days after germination) revealed high levels in the two domesticated genotypes, while in wild emmer wheat, they were below detection level. In contrast to the benzoxazinoid levels, the trichome density was dramatically higher in the wild emmer than in the domesticated wheat. Lastly, we tested the bird cherry-oat aphid’s ( Rhopalosiphum padi ) performance and found that Chinese Spring is more resistant than the tetraploid genotypes. Conclusions: Our results show that benzoxazinoids play a more significant defensive role than trichomes. Differences between the abundance of defense mechanisms in the wild and domesticated plants were observed in which wild emmer possesses high physical defenses while the domesticated wheat genotypes have high chemical defenses. These findings provide new insights into the defense adaptations of wheat plants against aphids.

Comparative transcriptome and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids

Background: Young wheat plants are continuously exposed to insect herbivorous attack. To maintain their fitness, plants have evolved different defense mechanisms, including the biosynthesis of deterrent compounds named benzoxazinoids, and/or trichome formation that provides physical barriers. It is unclear whether both of these mechanisms are equally critical in providing an efficient defense for wheat seedlings against the bird cherry-oat ( Rhopalosiphum padi ) aphid—an economically costly pest in cereal production. Results: In this study, we compared the transcriptomic, metabolomic, chemical, and physical defenses of three selected wheat genotypes to aphid performance. We chose diverse wheat genotypes, two tetraploid wheat genotypes, domesticated durum ‘Svevo’ and wild emmer ‘Zavitan,’ and one hexaploid bread wheat, ‘Chinese Spring.’ The full transcriptomic analysis revealed a major difference between the three genotypes, while the clustering of significantly different genes suggested a higher similarity between the two domesticated than the wild wheat. A pathway enrichment analysis indicated that genes associated with primary metabolism, as well as the pathways associated with defense such as phytohormones and specialized metabolites, were altered between the three genotypes. Measurement of benzoxazinoid levels at the three time-points (11, 15 and 18 days-after-germination) revealed high abundance levels in the two domesticated genotypes, while the levels were very low in the wild emmer wheat. The Chinese Spring showed a more diverse benzoxazinoid (known and putative) composition than the other two genotypes. In contrast to the benzoxazinoid levels, the trichome density was dramatically higher in the wild emmer than in the domesticated wheat. Evaluation of aphid reproduction indicated that the domesticated bread wheat is more resistant than the tetraploid genotypes. Conclusions: We compared the amount of benzoxazinoids, the trichome number, and aphid reproduction at three time-points, as well as performing a transcriptome analysis. Overall, the results suggested that although wheat seedlings possess both chemical and physical defenses, the chemical defense plays a more significant defensive role than the physical barriers.