Transgenerational Priming Research Articles

Guardians of wheat: Unleashing transgenerational immune priming with Trichoderma against spot blotch

Plants encounter various biotic stresses in their natural habitat, prompting the exploration of innovative protective measures to bolster their immune defences against pathogens. An effective strategy involves priming plant immunity, conferring enduring and comprehensive protection. Defence priming, characterized by heightened responsiveness to attackers following prior stress exposure, intriguingly manifests transgenerationally, transmitting the memory of priming to subsequent plant generations. In our investigation, we delved into the phenomenon of transgenerational immune priming (TGIP) in wheat facilitated by Trichoderma, spanning from the parental generation (G0) to the grand progeny (G2) generation. Successful establishment of transgenerational priming in the G2 generation was achieved by initially priming the G0 generation of wheat with Trichoderma. To assess priming inheritance, seeds from the G1 generation were collected, and both primed and non-primed wheat plants' grand progeny (G2 generation) were cultivated in soil. Subsequent evaluation encompassed the disease phenotype, biochemical parameters, and yield-related traits of the G2 generation wheat when confronted with Bipolaris sorokiniana, the causal agent of spot blotch disease. Our analysis revealed that the G2 generation of primed wheat displayed superior protection against spot blotch compared to non-primed wheat. Biochemical studies indicated no activation of defensive responses in the absence of disease pressure in G2 wheat plants. However, upon pathogen challenge, the grand progeny of primed wheat exhibited a robust defence response, surpassing that of non-primed wheat. This targeted defence response enabled efficient resource utilization and mitigated yield penalties. Furthermore, under biotic stress conditions, the grand progeny of primed wheat exhibited enhanced yield parameters compared to non-primed wheat. Our findings provide conclusive evidence that Trichoderma-mediated priming against B. sorokiniana can be inherited successfully from the parental (G0) generation to the grand progeny (G2) generation of wheat. This study represents the initial documentation of Trichoderma-mediated TGIP in wheat against B. sorokiniana, holding significant promise for sustainable agriculture by offering an environmentally friendly alternative to chemical pesticides.

Genetic mining of desirable alleles for transgenerational stress memory through enhancing drought adaptation in wheat

Plant memory refers to the phenomenon where past environmental experiences influence the responses of plants to current/future events. Drought stress has a mostly significant negative impact on wheat, which is a vital crop for global food security. In the context of germination, plant memory can manifest as 'transgenerational priming', where mother plants exposure to drought stress alters the germination behavior of the next-generation seeds. Therefore, our study aimed to explore the genetic factors underpinning transgenerational drought tolerance in wheat using a diverse collection of 111 by the Genome-Wide Association Study (GWAS). In the seed germination test, all genotypes had higher Germination Percentage (G%) and Germination Pace (GP) from seeds of Stressed Plants (OSP) than those of Non-Stressed Plants (ONP) by 16% and 29%, respectively), indicating that Transgenerational Stress Memory (TSM) may manifest through appearing to possess a more persistent stress memory. For root length, OSP had a greater Root Length (RL) than ONP by 45%, suggesting a more highly developed root system in the OSP seeds. The time at which TSM manifests during the plant life cycle could reflect disparate strategies of TSM duration among genotypes from OSP and ONP. Genetic associations of TSM showed highly significant QTNs for all of the studied traits. For instance, a highly significant QTN (BS00068042_51) located on chromosome 2B at position 107,381,860 bp inside the gene TraesCS2B02G140800 encodes Cytochrome P450 (CYPs) that was found to be associated with the traits of FW and SMC for OSP. CYPs play a significant role in wheat response to environmental stresses. Therefore, further research into the specific alleles/candidate genes and their functions in wheat transgenerational stress memory will provide valuable insights for developing strategies to enhance drought tolerance in wheat crops through genetic manipulation or targeted interventions.

No evidence for trans-generational immune priming in Drosophila melanogaster.

Most organisms are under constant and repeated exposure to pathogens, leading to perpetual natural selection for more effective ways to fight-off infections. This could include the evolution of memory-based immunity to increase protection from repeatedly-encountered pathogens both within and across generations. There is mixed evidence for intra- and trans-generational priming in non-vertebrates, which lack the antibody-mediated acquired immunity characteristic of vertebrates. In this work, we tested for trans-generational immune priming in adult offspring of the fruit fly, Drosophila melanogaster, after maternal challenge with 10 different bacterial pathogens. We focused on natural opportunistic pathogens of Drosophila spanning a range of virulence from 10% to 100% host mortality. We infected mothers via septic injury and tested for enhanced resistance to infection in their adult offspring, measured as the ability to suppress bacterial proliferation and survive infection. We categorized the mothers into four classes for each bacterium tested: those that survived infection, those that succumbed to infection, sterile-injury controls, and uninjured controls. We found no evidence for trans-generational priming by any class of mother in response to any of the bacteria.

Trans-generational immune priming against American Foulbrood does not affect the performance of honeybee colonies.

Honeybees are major pollinators for our food crops, but at the same time they face many stressors all over the world. One of the major threats to honeybee health are bacterial diseases, the most severe of which is the American Foulbrood (AFB). Recently a trans-generational vaccination approach against AFB has been proposed, showing strong potential in protecting the colonies from AFB outbreaks. Yet, what remains unstudied is whether the priming of the colony has any undesired side-effects. It is widely accepted that immune function is often a trade-off against other life-history traits, hence immune priming could have an effect on the colony performance. In this experiment we set up 48 hives, half of them with primed queens and half of them as controls. The hives were placed in six apiaries, located as pair of apiaries in three regions. Through a 2-year study we monitored the hives and measured their health and performance. We measured hive weight and frame contents such as brood amount, worker numbers, and honey yield. We studied the prevalence of the most common honeybee pathogens in the hives and expression of relevant immune genes in the offspring at larval stage. No effect of trans-generational immune priming on any of the hive parameters was found. Instead, we did find other factors contributing on various hive performance parameters. Interestingly not only time but also the region, although only 10 km apart from each other, had an effect on the performance and health of the colonies, suggesting that the local environment plays an important role in hive performance. Our results suggest that exploiting the trans-generational priming could serve as a safe tool in fighting the AFB in apiaries.

Transgenerational effects of chromium stress at the phenotypic and molecular level in Arabidopsis thaliana.

In this study, we describe the results obtained in a study of the transgenerational phenotypic effects of chromium (Cr) stress on the model plant species Arabidopsis thaliana. The F1 generation derived from parents grown under chronic and medium chronic stress showed significantly higher levels of the maximal effective concentration (EC50) compared with F1 plants generated from unstressed parents. Moreover, F1 plants from Cr-stressed parents showed a higher germination rate when grown in the presence of Cr. F1 plants derived from parents cultivated under chronic Cr stress displayed reduced hydrogen peroxide levels under Cr stress compared to controls. At lower Cr stress levels, F1 plants were observed to activate promptly more genes involved in Cr stress responses than F0 plants, implying a memory effect linked to transgenerational priming. At higher Cr levels, and at later stages, F1 plants modulated significantly fewer genes than F0 plants, implying a memory effect leading to Cr stress adaptation. Several bHLH transcription factors were induced by Cr stress in F1 but not in F0 plants, including bHLH100, ORG2 and ORG3. F1 plants optimized gene expression towards pathways linked to iron starvation response. A model of the transcriptional regulation of transgenerational memory to Cr stress is presented here, and could be applied for other heavy metal stresses.

Chloroplast proteomics reveals transgenerational cross-stress priming in Pinus radiata

Plants do have stress memory and chloroplast signaling has been revealed as crucial element to acquire and extend this memory into future generations, allowing plant adaptation to changing environments and providing novel tools in the field of crop improvement. Despite the process is known, how a plant is capable to transfer some aspects of its “life-long learning” to progeny, as well as the role of chloroplast proteome mediating transgenerational cross-stress priming effects, remain unknown. To fill this gap, this study examines the impact of the physiological status of Pinus radiata parentals over the capacity of their progeny to acclimate to their first stress period in a common garden experiment. Seedlings were originated in subpopulations with the same genetic background, but grown in two locations with contrasting environments (stressed vs non-stressed plants). Physiological measurements (fluorescence-based and biochemistry) and chloroplast proteomics were employed to study plant stress responses. Results demonstrated a differential seed priming. Those seedlings originated from stressed plants responded quicker and more efficiently than those originated from unstressed counterparts. Unprimed responses showed proteome remodeling driven by lipid peroxidation and photoinhibition, whereas primed subpopulation quickly faced stress rearranging secondary metabolism, replacing damaged lipids, reducing photooxidative damage, and promoting photorespiration and redox homeostasis in order to reduce lipoperoxidation and maintain photosynthesis. These results not only delve into cross-stress memory in long-lived species, but also suggest a new biotechnological potential for current seed orchards if adequate management is performed. • Parental growing conditions have transgenerational cross-stress priming effects. • Subpopulation originated from stressed plants responded quicker and more efficiently. • Primed responses were driven by photorespiration, redox, and secondary metabolism. • Knowledge acquired suggests a new biotechnological potential for seed orchards.

Transgenerational effect of UV-B priming on photochemistry and associated metabolism in rice seedlings subjected to PEG-induced osmotic stress

Rice being the major food crop for more than half of the world population is severely affected by drought stress starting from the establishment of the seedling. We focused on the UV-B priming mediated transgenerational drought tolerance of a drought-tolerant rice variety (Vaisakh) towards polyethylene glycol (PEG) 6,000 (20%)-induced drought. Results showed that priming in F0 generation and re-priming in F1 generation with UV-B enhanced the PEG stress tolerance potential of rice seedlings with increased expression of genes encoding antioxidant enzymes and stress-related proteins offering better protection to primed plants. UV-B priming maintained oxidative homeostasis of the plant cell thus ensuring uninterrupted mitochondrial and photosynthetic activities. Cumulatively, our results suggest that the transgenerational priming memory retained in the seeds is transferred to offspring without any loss. Moreover, re-priming in F1 generation further boosted the innate tolerance potential of a tolerant variety resulting in stable cellular redox homeostasis.

The costs and benefits of basal infection resistance vs immune priming responses in an insect

In insects, basal pathogen resistance and immune priming can evolve as mutually exclusive strategies, with distinct infection outcomes. However, the evolutionary drivers of such diverse immune functions remain poorly understood. Here, we addressed this key issue by systematically analyzing the differential fitness costs and benefits of priming vs resistance evolution in Tribolium beetle populations infected with Bacillus thuringiensis. Surprisingly, resistant beetles had increased post-infection reproduction and a longer lifespan under both starving as well as fed conditions, with no other measurable costs. In contrast, priming reduced offspring early survival, development rate and reproduction. Priming did improve post-infection survival of offspring, but this added trans-generational benefit of immune priming might not compensate for its pervasive costs. Resistance was thus consistently more beneficial. Overall, our work demonstrates the evolutionary change in trans-generational priming response, and provides a detailed comparison of the complex fitness consequences of evolved priming vs resistance.

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.

Nitrogen inputs influence vegetative metabolism in maize engineered with a seed-specific carotenoid pathway.

Metabolomic profiling of a maize line engineered with an endosperm-specific carotenogenic pathway revealed unexpected metabolic readjustments of primary metabolism in leaves and roots. High-carotenoid (HC) maize was engineered to accumulate high levels of carotenoids in the endosperm. The metabolic interventions influenced the flux through non-target pathways in tissues that were not affected by the targeted intervention. HC maize at the vegetative stage also showed a reduced susceptibility to insect feeding. It is unknown, however, whether the metabolic history of the embryo has any impact on the metabolite composition in vegetative tissues. We, therefore, compared HC maize and its isogenic counterpart (M37W) to test the hypothesis that boosting the carotenoid content in the endosperm triggers compensatory effects in core metabolism in vegetative tissues. Specifically, we investigated whether the metabolite composition of leaves and roots at the V6 stage differs between HC and M37W, and whether N inputs further alter the core metabolism of HC compared to M37W. We found an increase in the abundance of organic acids from the tricarboxylic acid (TCA) cycle in HC even under restricted N conditions. In contrast, low levels of carotenoids and chlorophyll were measured regardless of N levels. Sugars were also significantly depleted in HC under low N. We propose a model explaining the observed genotype-dependent and input-dependent effects, in which organic acids derived from the TCA cycle accumulate during vegetative growth and contribute to the increased demand for pyruvate and/or acetyl-CoA in the endosperm and embryo. This response may in part reflect the transgenerational priming of vegetative tissues in the embryo induced by the increased demand for metabolic precursors during seed development in the previous generation.

Priming of seeds with INA and its transgenerational effect in common bean (Phaseolus vulgaris L.) plants

Priming is a mechanism of defense that prepares the plant’s immune system for a faster and/or stronger activation of cellular defenses against future exposure to different types of stress. This enhanced resistance can be achieved by using inorganic and organic compounds which imitate the biological induction of systemic acquired resistance. INA (2,6 dichloro-isonicotinic acid) was the first synthetic compound created as a resistance inducer for plant-pathogen interactions. However, the use of INA to activate primed resistance in common bean, at the seed stage and during germination, remains experimentally unexplored. Here, we test the hypothesis that INA-seed treatment would induce resistance in common bean plants to Pseudomonas syringae pv. phaseolicola, and that the increased resistance is not accompanied by a tradeoff between plant defense and growth. Additionally, it was hypothesized that treating seeds with INA has a transgenerational priming effect. We provide evidence that seed treatment activates a primed state for disease resistance, in which low nucleosome enrichment and reduced histone activation marks during the priming phase, are associated with a defense-resistant phenotype, characterized by symptom appearance, pathogen accumulation, yield, and changes in gene expression. In addition, the priming status for induced resistance can be inherited to its offspring.

Top‐down effects from parasitoids may mediate plant defence and plant fitness

Abstract Plants face many environmental stresses that can impact their survival, development and fitness. Insects are the most diverse, abundant and threatening herbivores in nature. As a consequence, plants produce direct chemical and physical defences to reduce herbivory. They also release volatiles to recruit natural enemies that indirectly protect them from herbivory. The recruitment of parasitic wasps can benefit plant fitness because they ultimately kill their insect hosts. Recently, studies showed that parasitoids can indirectly mediate plant defences by modulating herbivore oral secretions. In addition to the direct benefits of parasitoids in terms of reducing herbivore survival, we tested if the reduction in induced defences by parasitized caterpillars compared to non‐parasitized caterpillars may reduce the costs associated with defence expression. We provide evidence that tomato plants treated with saliva from parasitized caterpillars have significantly higher fitness parameters including increased flower numbers (16.3%) and heavier fruit weight (13.5%), compared to plants treated with saliva from non‐parasitized caterpillars. Since plants were grown without actual herbivores, the higher values for these fitness parameters were due to lower costs of induced defences and not due to reduced herbivory by parasitized caterpillars. Furthermore, the resulting seed germination time was shorter and the germination rate was higher when the maternal plants were previously exposed to parasitized herbivore treatment compared to control (non‐treated) plants. Overall, application of saliva did not result in transgenerational priming of offspring defence responses. However, offspring of parents exposed to caterpillar saliva had lower constitutive levels and higher induced levels of trypsin inhibitor than offspring from unexposed parents. This study shows that the saliva of parasitized caterpillars can modulate plant defences and further demonstrates that the lower induction of plant defences is associated with elevated plant fitness in the absence of herbivore feeding, suggesting that induced plant defences are costly. A free Plain Language Summary can be found within the Supporting Information of this article.

Low herbicide doses can change the responses of weeds to subsequent treatments in the next generation: metamitron exposed PSII-target-site resistant Chenopodium album as a case study.

It is well known that exposure to mild stress can precondition organisms to better tolerate subsequent stress exposure in the same or future generations. Since herbicide hormesis also represents a moderate stress to exposed plants, a transgenerational priming is likely but not proven. Especially in herbicide-resistant weeds showing enhanced reproductive fitness after regular herbicide treatments, the ability to induce resilient offspring phenotypes via hormesis may hasten the evolution of herbicide resistance in weeds. This hypothesis was studied for the triazinone metamitron in an F1 offspring generation of PSII target-site resistant (TSR) plants of Chenopodium album propagated after parental conditioning with various metamitron doses. In two independent dose-response greenhouse trials, there was a positive correlation between the strength of the stimulatory response during parental preconditioning and the magnitude of transgenerational changes in herbicide sensitivity and hormesis expression. Parental conditioning at subhormetic and toxic concentrations lead to less resilient offspring, while conditioning doses that induced a pronounced hormetic effect in F0 plants had a sensitivity-reducing and hormesis-promoting effect on the offspring. The observed reduction in sensitivity in F1 plants compared to unconditioned F1 plants was up to 2.2-fold. This study demonstrates that hormetic herbicide treatments have the ability to prime weeds for enhanced tolerance to subsequent treatments in the next generation. Effects proved dose sensitive and may act in concert with other stimulatory adaptations in plant populations. This is relevant for weed control and herbicide resistance evolution, but also for herbicide side-effects that go beyond the exposed area. © 2020 The Author. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Recovery and immune priming modulate the evolutionary trajectory of infection-induced reproductive strategies.

In response to parasite exposure, organisms from a variety of taxa undergo a shift in reproductive investment that may trade off with other life-history traits including survival and immunity. By suppressing reproduction in favour of somatic and immunological maintenance, hosts can enhance the probability of survival and recovery from infection. By plastically enhancing reproduction through terminal investment, on the other hand, hosts under the threat of disease-induced mortality could enhance their lifetime reproductive fitness through reproduction rather than survival. However, we know little about the evolution of these strategies, particularly when hosts can recover and even bequeath protection to their offspring. In this study, we develop a stochastic agent-based model that competes somatic maintenance and terminal investment strategies as they trade off differentially with lifespan, parasite resistance, recovery and transgenerational immune priming. Our results suggest that a trade-off between reproduction and recovery can drive directional selection for either terminal investment or somatic maintenance, depending on the cost of reproduction to lifespan. However, some conditions, such as low virulence with a high cost of reproduction to lifespan, can favour diversifying selection for the coexistence of both strategies. The introduction of transgenerational priming into the model favours terminal investment when all strategies are equally likely to produce primed offspring, but favours somatic maintenance if it confers even a slight priming advantage over terminal investment. Our results suggest that both immune priming and recovery may modulate the evolution of reproductive shift diversity and magnitude upon exposure to parasites.

Transgenerational Defense Priming for Crop Protection against Plant Pathogens: A Hypothesis.

Throughout evolution, plants have developed diverse mechanisms of defense that “prime” their innate immune system for more robust and active induction of defense responses against different types of stress. Nowadays there are numerous reports concerning the molecular bases of priming, as well as the generational priming mechanisms. Information concerning transgenerational priming, however, remains deficient. Some reports have indicated, nonetheless, that the priming status of a plant can be inherited to its offspring. Here, we show that the priming agent β-aminobutyric acid induced resistance to Pseudomonas syringae pv. phaseolicola infection in the common bean (Phaseolus vulgaris L.) We have analyzed the transgenerational patterns of gene expression of the PvPR1 gene (Phaseolus vulgaris PR1), a highly responsive gene to priming, and show that a transgenerational priming response against pathogen attack can last for at least two generations. We hypothesize that a defense-resistant phenotype and easily identifiable, generational and transgenerational, “primed patterns” of gene expression are excellent indicators of the priming response in crop plants. Furthermore, we propose here that modern plant breeding methods and crop improvement efforts must include the use of elicitors to prime induced resistance in the field and, above all, to select for induced heritable states in progeny that is primed for defense.

The within-host dynamics of infection in trans-generationally primed flour beetles.

Many taxa exhibit plastic immune responses initiated after primary microbial exposure that provide increased protection against disease-induced mortality and the fitness costs of infection. In several arthropod species, this protection can even be passed from parents to offspring through a phenomenon called trans-generational immune priming. Here, we first demonstrate that trans-generational priming is a repeatable phenomenon in flour beetles (Tribolium castaneum) primed and infected with Bacillus thuringiensis (Bt). We then quantify the within-host dynamics of microbes and host physiological responses in infected offspring from primed and unprimed mothers by monitoring bacterial density and using mRNA-seq to profile host gene expression, respectively, over the acute infection period. We find that priming increases inducible resistance against Bt around a critical temporal juncture where host septicaemic trajectories, and consequently survival, may be determined in unprimed individuals. Our results identify a highly differentially expressed biomarker of priming, containing an EIF4-e domain, in uninfected individuals, as well as several other candidate genes. Moreover, the induction and decay dynamics of gene expression over time suggest a metabolic shift in primed individuals. The identified bacterial and gene expression dynamics are likely to influence patterns of bacterial fitness and disease transmission in natural populations.

Divergent immune priming responses across flour beetle life stages and populations.

Growing evidence shows that low doses of pathogens may prime the immune response in many insects, conferring subsequent protection against infection in the same developmental stage (within‐life stage priming), across life stages (ontogenic priming), or to offspring (transgenerational priming). Recent work also suggests that immune priming is a costly response. Thus, depending on host and pathogen ecology and evolutionary history, tradeoffs with other fitness components may constrain the evolution of priming. However, the relative impacts of priming at different life stages and across natural populations remain unknown. We quantified immune priming responses of 10 natural populations of the red flour beetle Tribolium castaneum, primed and infected with the natural insect pathogen Bacillus thuringiensis. We found that priming responses were highly variable both across life stages and populations, ranging from no detectable response to a 13‐fold survival benefit. Comparing across stages, we found that ontogenic immune priming at the larval stage conferred maximum protection against infection. Finally, we found that various forms of priming showed sex‐specific associations that may represent tradeoffs or shared mechanisms. These results indicate the importance of sex‐, life stage‐, and population‐specific selective pressures that can cause substantial divergence in priming responses even within a species. Our work highlights the necessity of further work to understand the mechanistic basis of this variability.

Use of BABA and INA As Activators of a Primed State in the Common Bean (Phaseolus vulgaris L.).

To survive in adverse conditions, plants have evolved complex mechanisms that “prime” their defense system to respond and adapt to stresses. Their competence to respond to such stresses fundamentally depends on its capacity to modulate the transcriptome rapidly and specifically. Thus, chromatin dynamics is a mechanism linked to transcriptional regulation and enhanced defense in plants. For example, in Arabidopsis, priming of the SA-dependent defense pathway is linked to histone lysine methylation. Such modifications could create a memory of the primary infection that is associated with an amplified gene response upon exposure to a second stress-stimulus. In addition, the priming status of a plant for induced resistance can be inherited to its offspring. However, analyses on the molecular mechanisms of generational and transgenerational priming in the common bean (Phaseolus vulagris L.), an economically important crop, are absent. Here, we provide evidence that resistance to P. syringae pv. phaseolicola infection was induced in the common bean with the synthetic priming activators BABA and INA. Resistance was assessed by evaluating symptom appearance, pathogen accumulation, changes in gene expression of defense genes, as well as changes in the H3K4me3 and H3K36me3 marks at the promoter-exon regions of defense-associated genes. We conclude that defense priming in the common bean occurred in response to BABA and INA and that these synthetic activators primed distinct genes for enhanced disease resistance. We hope that an understanding of the molecular changes leading to defense priming and pathogen resistance will provide valuable knowledge for producing disease-resistant crop varieties by exposing parental plants to priming activators, as well as to the development of novel plant protection chemicals that stimulate the plant's inherent disease resistance mechanisms.

A temperature shock can lead to trans-generational immune priming in the Red Flour Beetle, Tribolium castaneum.

Trans-generational immune priming (TGIP) describes the transfer of immune stimulation to the next generation. As stress and immunity are closely connected, we here address the question whether trans-generational effects on immunity and resistance can also be elicited by a nonpathogen stress treatment of parents. General stressors have been shown to induce immunity to pathogens within individuals. However, to our knowledge, it is as of yet unknown whether stress can also induce trans-generational effects on immunity and resistance. We exposed a parental generation (mothers, fathers, or both parents) of the red flour beetle Tribolium castaneum, a species where TGIP has been previously been demonstrated, to either a brief heat or cold shock and examined offspring survival after bacterial infection with the entomopathogen Bacillus thuringiensis. We also studied phenoloxidase activity, a key enzyme of the insect innate immune system that has previously been demonstrated to be up-regulated upon TGIP. We quantified parental fecundity and offspring developmental time to evaluate whether trans-generational priming might have costs. Offspring resistance was found to be significantly increased when both parents received a cold shock. Offspring phenoloxidase activity was also higher when mothers or both parents were cold-shocked. By contrast, parental heat shock reduced offspring phenoloxidase activity. Moreover, parental cold or heat shock delayed offspring development. In sum, we conclude that trans-generational priming for resistance could not only be elicited by pathogens or pathogen-derived components, but also by more general cues that are indicative of a stressful environment. The interaction between stress responses and the immune system might play an important role also for trans-generational effects.

Keeping it in the family: transgenerational memories of plant defence.

Abstract Plants possess a sophisticated array of systems with which to sense and respond to their internal and external environment. Biological changes triggered by such systems represent examples of phenotypic plasticity. One aspect of phenotypic plasticity that has recently emerged is transgenerational priming of plant defence responses - the persistence of induced resistance responses across generations. There has been a recent surge in interest in epigenetic mechanisms as a basis for phenotypic plasticity, including the ability for such epigenetic changes to be inherited across generations. In this review, we focus on the evidence that attack by pests and disease can stimulate plant defence responses that increase levels of resistance not only in attacked plants, but in their offspring, and discuss mechanisms by which environmental stress signals can be inherited. Finally, we consider the implications of transgenerational defence responses for plants in natural and agricultural systems.