Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis

Aims

Arbuscular mycorrhizal (AM) fungi associate with the majority of terrestrial plants, influencing their growth, nutrient uptake and defence chemistry. Consequently, AM fungi can significantly impact plant-herbivore interactions, yet surprisingly few studies have investigated how AM fungi affect plant responses to root herbivores. This study aimed to investigate how AM fungi affect plant tolerance mechanisms to belowground herbivory.

Methods

We examined how AM fungi affect plant (Saccharum spp. hybrid) growth, nutrient dynamics and secondary chemistry (phenolics) in response to attack from a root-feeding insect (Dermolepida albohirtum).

Results

Root herbivory reduced root mass by almost 27%. In response, plants augmented investment in aboveground biomass by 25%, as well as increasing carbon concentrations. The AM fungi increased aboveground biomass, phosphorus and carbon. Meanwhile, root herbivory increased foliar phenolics by 31% in mycorrhizal plants, and increased arbuscular colonisation of roots by 75% overall. AM fungi also decreased herbivore performance, potentially via increasing root silicon concentrations.

Conclusions

Our results suggest that AM fungi may be able to augment plant tolerance to root herbivory via resource allocation aboveground and, at the same time, enhance plant root resistance by increasing root silicon. The ability of AM fungi to facilitate resource allocation aboveground in this way may be a more widespread strategy for plants to cope with belowground herbivory.

     

Effects of insect attack to stems on plant survival,growth, reproduction and photosynthesis

Studies of insect herbivory have mostly focused on leaf‐feeding even though most woody plant biomass is stem tissue. Attack to stems has the potential to be more detrimental to plant performance than attack to leaves. Here we asked how severe is the impact of insect stem herbivory on plant performance. We quantify the effect of insect stem herbivory via a meta‐analysis of 119 papers in 100 studies (papers by the same authors were treated as the same study). These studies involved 92 plant species and 70 species of insect herbivore (including simulated herbivory). Attack to plant stems reduced plant performance by an average of approximately 22%. Stem herbivory had greatest impacts on plant and branch survival, which was reduced by 63%. Measures of plant reproduction and vegetative biomass were reduced by 33% and 16% respectively, while measurements of photosynthetic rate were not significantly different between plants with and without stem herbivore attack. Stem herbivory led to a decline in leader performance but an increase in performance of laterals, highlighting the importance of plant compensation. Juvenile plants were more severely affected by stem herbivory than adult plants, and studies conducted in greenhouses found more severe effects than studies conducted in the field. Stem herbivory did not have a significant effects on any of the non‐performance responses measured (defence compounds, SLA, root:shoot, phenology and plant carbon and nitrogen). We compare our results with results from various meta‐analyses considering herbivory on other plant parts. The impact of insect herbivory to stems on plant performance appears at least as severe as insect herbivory to roots and leaves, if not more.     

Herbivore induced plant volatiles: Their role in plant defense for pest management

Plants respond to herbivory through different defensive mechanisms. The induction of volatile emission is one of the important and immediate response of plants to herbivory. Herbivore-induced plant volatiles (HIPVs) are involved in plant communication with natural enemies of the insect herbivores, neighboring plants, and different parts of the damaged plant. Release of a wide variety of HIPVs in response to herbivore damage and their role in plant-plant, plant-carnivore and intraplant communications represents a new facet of the complex interactions among different trophic levels. HIPVs are released from leaves, flowers, and fruits into the atmosphere or into the soil from roots in response to herbivore attack. Moreover, HIPVs act as feeding and/or oviposition deterrents to insect pests. HIPVs also mediate the interactions between the plants and the microorganisms. This review presents an overview of HIPVs emitted by plants, their role in plant defense against herbivores and their implications for pest management.     

Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions

Complex relationships occur among plants, mycorrhizal fungi, and herbivores. By altering plant nutrient status, mycorrhizas may alter herbivory or plant tolerance to herbivory via compensatory regrowth. We examined these interactions by assessing grasshopper preference and plant growth and fungal colonization responses to herbivory under mycorrhizal and non‐mycorrhizal conditions within tallgrass prairie microcosms. Mycorrhizal symbiosis increased plant regrowth following defoliation, and some strongly mycotrophic plant species showed overcompensation in response to herbivory when they were mycorrhizal. Although grasshoppers spent more time on mycorrhizal plants, herbivory intensity did not differ between mycorrhizal and non‐mycorrhizal plants. Aboveground herbivory by grasshoppers significantly increased mycorrhizal fungal colonization of plant roots. Thus mycorrhizas may greatly benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the symbiosis. Our results also indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts.     

Effects of a nematode Meloidogyne incognita and its interaction with above‐ground herbivory on an invasive wetland plant,alligator weed (Alternanthera philoxeroides)

Invasive plants may be attacked both above ground and below ground. Few studies have, however, investigated the simultaneous effects of above‐ground and below‐ground herbivory. In the present study, we report the effects of beetle herbivory and nematode infection on alligator weed, Alternanthera philoxeroides, an invasive plant in China. We found that the root‐knot nematode Meloidogyne incognita widely occurred on the plant in south China. To examine its effect on the plant in conjunction with above‐ground herbivory, we conducted a field common garden experiment with a local insect defoliator, Cassida piperata. We also included the native congener Alternanthera sessilis in our experiments for a comparison of the response of invasive and native species. We found no significant effects on plant biomass of the nematode infection in conjunction with the above‐ground herbivory. Further chemical analysis, however, showed that the water‐soluble carbohydrate content in roots of A. philoxeroides was significantly increased in plants attacked by both the nematode and the herbivore compared with the water‐soluble carbohydrate content in plants attacked by only the nematode or herbivore alone. We found no such change in the native congener A. sessilis. Together these results may suggest that A. philoxeroides tolerates joint above‐ground and below‐ground damage by allocating more resources to below‐ground material.     

Specific impacts of two root herbivores and soil nutrients on plant performance and insect–insect interactions

Soil‐dwelling insects commonly co‐occur and feed simultaneously on belowground plant parts, yet patterns of damage and consequences for plant and insect performance remain poorly characterized. We tested how two species of root‐feeding insects affect the performance of a perennial plant and the mass and survival of both conspecific and heterospecific insects. Because root damage is expected to impair roots’ ability to take up nutrients, we also evaluated how soil fertility alters belowground plant–insect and insect–insect interactions. Specifically, we grew common milkweed Asclepias syriaca in low or high nutrient soil and added seven densities of milkweed beetles Tetraopes tetraophthalmus, wireworms (mainly Hypnoides abbreviatus), or both species. The location and severity of root damage was species‐specific: Tetraopes caused 59% more damage to main roots than wireworms, and wireworms caused almost seven times more damage to fine roots than Tetraopes. Tetraopes damage decreased shoot, main root and fine root biomass, however substantial damage by wireworms did not decrease any component of plant biomass. With the addition of soil nutrients, main root biomass increased three times more, and fine root biomass increased five times more when wireworms were present than when Tetraopes were present. We detected an interactive effect of insect identity and nutrient availability on insect mass. Under high nutrients, wireworm mass decreased 19% overall and was unaffected by the presence of Tetraopes. In contrast, Tetraopes mass increased 114% overall and was significantly higher when wireworms were also present. Survival of wireworms decreased in the presence of Tetraopes, and both species’ survival was negatively correlated with conspecific density. We conclude that insect identity, density and soil nutrients are important in mediating the patterns and consequences of root damage, and suggest that these factors may account for some of the contradictory plant responses to belowground herbivory reported in the literature.     

Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory

Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root–leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco ( Nicotiana tabacum ) system we highlight two examples of this phenomenon. First, the secondary metabolite nicotine is produced in roots, yet translocated aboveground for use as a foliar resistance trait. We demonstrate that nematode root herbivory interferes with foliar nicotine dynamics, resulting in positive effects on aboveground phytophagous insects. Notably, nematode-induced facilitation only occurred on nicotine-producing plants, and not on nicotine-deficient mutants. In the second case, we use stable isotope and invertase enzyme analyses to demonstrate that foliar herbivory elicits a putative tolerance response whereby aboveground nutritional reserves are allocated to roots, resulting in facilitation of phytoparasitic nematodes. Thus, plants integrate roots in resistance and tolerance mechanisms for leaf defense, and such root–leaf connections inherently link the dynamics of above- and belowground consumers.     

The aluminium signal: New dimensions to mechanisms of aluminium tolerance

The physiological basis of plant reaction to and tolerance of aluminium (Al) is poorly understood. We review the results of investigations into Al toxicity and root physiology to develop a theoretical basis for explaining the reaction of the root to Al, including suggested roles for Ca²⁺, mucilaginous cap secretions and endogenous growth regulators in mediating a transmitted response between Al-damaged cap cells and the interacting cell populations of the cap and root. This information is used to identify possible mechanisms of Al tolerance, notably involving signal transduction, Al uptake pathways and root morphogenesis; and to briefly discuss how procedures selecting for Al tolerance may be improved by incorporating the concept of stimulus-response coupling. Similarities in the responses of roots to Al and other signals (e.g. gravity, light, mechanical impedance) are used to develop the hypothesis that roots respond to environmental signals by way of a common regulatory system. New research prospects for extending our perception of Al tolerance mechanisms are identified.     

Insect herbivory and plant adaptation in an early successional community*

To address the role of insect herbivores in adaptation of plant populations and the persistence of selection through succession, we manipulated herbivory in a long‐term field experiment. We suppressed insects in half of 16 plots over nine years and examined the genotypic structure and chemical defense of common dandelion (Taraxacum officinale), a naturally colonizing perennial apomictic plant. Insect suppression doubled dandelion abundance in the first few years, but had negligible effects thereafter. Using microsatellite DNA markers, we genotyped >2500 plants and demonstrate that insect suppression altered the genotypic composition of plots in both sampling years. Phenotypic and genotypic estimates of defensive terpenes and phenolics from the field plots allowed us to infer phenotypic plasticity and the response of dandelion populations to insect‐mediated natural selection. The effects of insect suppression on plant chemistry were, indeed, driven both by plasticity and plant genotypic identity. In particular, di‐phenolic inositol esters were more abundant in plots exposed to herbivory (due to the genotypic composition of the plots) and were also induced in response to herbivory. This field experiment thus demonstrates evolutionary sorting of plant genotypes in response to insect herbivores that was in same direction as the plastic defensive response within genotypes.     

Does mother know best? The preference–performance hypothesis and parent–offspring conflict in aboveground–belowground herbivore life cycles

1. A substantial amount of research on host‐plant selection by insect herbivores is focused around the preference–performance hypothesis (PPH). To date, the majority of studies have primarily considered insects with aboveground life cycles, overlooking insect herbivores that have both aboveground and belowground life stages, for which the PPH could be equally applicable. 2. This study investigated the factors influencing the performance of the root‐feeding vine weevil (Otiorhynchus sulcatus) larvae and whether this was linked to the oviposition behaviour of the maternal adult living aboveground. 3. Maternal insects feeding aboveground reduced root biomass by 34% and increased root carbon by 4%. Larvae feeding on plants subjected to aboveground herbivory had reduced mass. Irrespective of the presence of maternal herbivory, larval mass was positively correlated with root biomass. 4. Larval mass was also reduced by conspecific larvae, previously feeding on roots (19% reduction). However, the mechanism underpinning this effect remains unclear, as in contrast to maternal herbivory aboveground, prior larval feeding did not significantly affect root biomass or root carbon concentrations. 5. Maternal insects did not distinguish between plants infested with larvae and those that were free of larvae, in terms of their egg‐laying behaviour. Conversely, maternal insects tended to lay eggs on plants with smaller root systems, a behaviour that is likely to negatively affect offspring performance. 6. The PPH is not supported by our findings for the polyphagous vine weevil feeding on the host plant raspberry (Rubus idaeus), and in fact our results suggest that there is the potential for strong parent–offspring conflict in this system.     

Invasive and native populations of common ragweed exhibit strong tolerance to foliar damage

Tolerance and resistance are defence strategies evolved by plants to cope with damage due to herbivores. The introduction of exotic species to a new biogeographical range may alter the plant–herbivore interactions and induce selection pressures for new plant defence strategies with a modified resource allocation. To detect evolution in tolerance to herbivory in common ragweed, we compared 3 native (North America) and 3 introduced (France) populations, grown in a common garden environment. We explored the effect of leaf herbivory on plant vegetative and reproductive traits. Plants were defoliated by hand, simulating different degrees of insect grazing by removing 0%, 50% or 90% of each leaf blade. Total and shoot dry biomasses were not affected by increasing defoliation, whereas root dry biomass and root:shoot ratio decreased significantly for native and introduced populations. Furthermore, defoliation treatments did not affect any of the plant reproductive traits measured. Hence, common ragweed displayed an efficient reallocation of resources in shoot biomass at the expense of roots following defoliation, which allows the species to tolerate herbivory without obvious costs for fitness. We did not detect any difference in herbivory tolerance between introduced and native populations, but significant differences were found in reproduction with invasive populations producing more seeds than native populations. As a result, tolerance to herbivory has been maintained in the introduced plant populations. We discuss some implications of these preliminary results for biological control strategies dedicated to common ragweed.     

Insect herbivory and ontogeny: How do growth and development influence feeding behaviour,morphology and host use?

Herbivorous insects exploit many different plants and plant parts and often adopt different feeding strategies throughout their life cycle. The conceptual framework for investigating insect–plant interactions relies heavily on explanations invoking plant chemistry, neglecting a suite of competing and interacting pressures that may also limit herbivory. In the present paper, the methods by which ontogeny, feeding strategies and morphological characters inhibit herbivory by mandibulate holometabolous insects are examined. The emphasis on mechanical disruption of plant cells in the insect digestive strategy changes the relative importance of plant ‘defences’, increasing the importance of leaf structure in inhibiting herbivory. Coupled with the implications of substantial morphological and behavioural changes in ontogeny, herbivores adopt a range of approaches to herbivory that are independent of plant chemistry alone. Many insect herbivores exhibit substantial ontogenetic character displacement in mandibular morphology. This is tightly correlated with changes in feeding strategy, with changes to the cutting edges of mandibles increasing the efficiency of feeding. The changes in feeding strategy are also characterized by changes in feeding behaviour, with many larvae feeding gregariously in early instars. Non‐nutritive hypotheses considering the importance of natural enemies, shelter‐building and thermoregulation may also be invoked to explain the ontogenetic consequences of changes to feeding behaviour. There is a need to integrate these factors into a framework considering the gamut of potential explanations of insect herbivory, recognizing that ontogenetic constraints are not only viable explanations but a logical starting point. The interrelations between ontogeny, size, morphology and behaviour highlight the complexity of insect–plant relationships. Given the many methods used by insect herbivores to overcome the challenges of consuming foliage, the need for species‐specific and stage‐ specific research investigating ontogeny and host use by insect herbivores is critical for developing general theories of insect–plant interactions.     

How to quantify plant tolerance to loss of biomass?

In some plant species the whole shoot is occasionally removed, as a result of specialist herbivory, grazing, mowing, or other causes. The plant can adapt to defoliation by allocating more to tolerance and less to growth and defense. Plant tolerance to defoliation (TOL1) is typically measured as the ratio between the average dry weight of a group of damaged plants and a control group of undamaged plants, both measured some time after recovery. We develop a model to clarify what TOL1 actually measures. We advocate keeping regrowth (REG2) and shoot–root ratio, both elements of TOL1, separate in the analysis. Based on a resource trade‐off, exotic Jacobaea vulgaris plants from populations in the USA (no specialist herbivory) are expected to grow faster and be less tolerant than native Dutch populations (with specialist herbivory). Indeed Dutch plants had both a significantly larger fraction biomass in roots and faster regrowth (REG2), while US plants attained the highest weight in the control without defoliation. Using key‐factor analysis, we illustrate how growth rates, regrowth, and shoot–root ratio each contribute to final biomass (plant fitness). Our proposed method gives more insight in the mechanisms that underly plant tolerance against defoliation and how tolerance contributes to fitness.     

Metabolomics reveals herbivore‐induced metabolites of resistance and susceptibility in maize leaves and roots

Plants respond to herbivory by reprogramming their metabolism. Most research in this context has focused on locally induced compounds that function as toxins or feeding deterrents. We developed an ultra‐high‐pressure liquid chromatography time‐of‐flight mass spectrometry (UHPLC‐TOF‐MS)‐based metabolomics approach to evaluate local and systemic herbivore‐induced changes in maize leaves, sap, roots and root exudates without any prior assumptions about their function. Thirty‐two differentially regulated compounds were identified from Spodoptera littoralis‐infested maize seedlings and isolated for structure assignment by microflow nuclear magnetic resonance (CapNMR). Nine compounds were quantified by a high throughput direct nano‐infusion tandem mass spectrometry/mass spectrometry (MS/MS) method. Leaf infestation led to a marked local increase of 1,3‐benzoxazin‐4‐ones, phospholipids, N‐hydroxycinnamoyltyramines, azealic acid and tryptophan. Only few changes were found in the root metabolome, but 1,3‐benzoxazin‐4‐ones increased in the vascular sap and root exudates. The role of N‐hydroxycinnamoyltyramines in plant–herbivore interactions is unknown, and we therefore tested the effect of the dominating p‐coumaroyltyramine on S. littoralis. Unexpectedly, p‐coumaroyltyramine was metabolized by the larvae and increased larval growth, possibly by providing additional nitrogen to the insect. Taken together, this study illustrates that herbivore attack leads to the induction of metabolites that can have contrasting effects on herbivore resistance in the leaves and roots.     

Leaf herbivory counteracts nematode-triggered repression of jasmonate-related defenses in tomato roots

Shoot herbivores may influence the communities of herbivores associated with the roots via inducible defenses. However, the molecular mechanisms and hormonal signaling underpinning the systemic impact of leaf herbivory on root-induced responses against nematodes remain poorly understood. By using tomato (Solanum lycopersicum) as a model plant, we explored the impact of leaf herbivory by Manduca sexta on the performance of the root knot nematode Meloidogyne incognita. By performing glasshouse bioassays, we found that leaf herbivory reduced M. incognita performance in the roots. By analyzing the root expression profile of a set of oxylipin-related marker genes and jasmonate root content, we show that leaf herbivory systemically activates the 13-Lipoxigenase (LOX) and 9-LOX branches of the oxylipin pathway in roots and counteracts the M. incognita-triggered repression of the 13-LOX branch. By using untargeted metabolomics, we also found that leaf herbivory counteracts the M. incognita-mediated repression of putative root chemical defenses. To explore the signaling involved in this shoot-to-root interaction, we performed glasshouse bioassays with grafted plants compromised in jasmonate synthesis or perception, specifically in their shoots. We demonstrated the importance of an intact shoot jasmonate perception, whereas having an intact jasmonate biosynthesis pathway was not essential for this shoot-to-root interaction. Our results highlight the impact of leaf herbivory on the ability of M. incognita to manipulate root defenses and point to an important role for the jasmonate signaling pathway in shoot-to-root signaling.

Leaf herbivory counteracts the repression of jasmonate-related defenses triggered by a root knot nematode in tomato roots impairing the nematode performance via shoot-to-root jasmonate signaling     

Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis)

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late‐season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.