Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory

Approximately 0.2 % of all angiosperms are classified as metal hyperaccumulators based on their extraordinarily high leaf metal contents, for example >1 % zinc, >0.1 % nickel or >0.01 % cadmium (Cd) in dry biomass. So far, metal hyperaccumulation has been considered to be a taxon-wide, constitutively expressed trait, the extent of which depends solely on available metal concentrations in the soil. Here we show that in the facultative metallophyte Arabidopsis halleri, both insect herbivory and mechanical wounding of leaves trigger an increase specifically in leaf Cd accumulation. Moreover, the Cd concentrations accumulated in leaves can serve as an elemental defense against herbivory by larvae of the Brassicaceae specialist small white (Pieris rapae), thus allowing the plant to take advantage of this non-essential trace element and toxin. Metal homeostasis genes are overrepresented in the systemic transcriptional response of roots to the wounding of leaves in A. halleri, supporting that leaf Cd accumulation is preceded by systemic signaling events. A similar, but quantitatively less pronounced transcriptional response was observed in A. thaliana, suggesting that the systemically regulated modulation of metal homeostasis in response to leaf wounding also occurs in non-hyperaccumulator plants. This is the first report of an environmental stimulus influencing metal hyperaccumulation.

Induced Jasmonate Signaling Leads to Contrasting Effects on Root Damage and Herbivore Performance

Induced defenses play a key role in plant resistance against leaf feeders. However, very little is known about the signals that are involved in defending plants against root feeders and how they are influenced by abiotic factors. We investigated these aspects for the interaction between rice (Oryza sativa) and two root-feeding insects: the generalist cucumber beetle (Diabrotica balteata) and the more specialized rice water weevil (Lissorhoptrus oryzophilus). Rice plants responded to root attack by increasing the production of jasmonic acid (JA) and abscisic acid, whereas in contrast to in herbivore-attacked leaves, salicylic acid and ethylene levels remained unchanged. The JA response was decoupled from flooding and remained constant over different soil moisture levels. Exogenous application of methyl JA to the roots markedly decreased the performance of both root herbivores, whereas abscisic acid and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid did not have any effect. JA-deficient antisense 13-lipoxygenase (asLOX) and mutant allene oxide cyclase hebiba plants lost more root biomass under attack from both root herbivores. Surprisingly, herbivore weight gain was decreased markedly in asLOX but not hebiba mutant plants, despite the higher root biomass removal. This effect was correlated with a herbivore-induced reduction of sucrose pools in asLOX roots. Taken together, our experiments show that jasmonates are induced signals that protect rice roots from herbivores under varying abiotic conditions and that boosting jasmonate responses can strongly enhance rice resistance against root pests. Furthermore, we show that a rice 13-lipoxygenase regulates root primary metabolites and specifically improves root herbivore growth.

Identification, quantification, spatiotemporal distribution and genetic variation of major latex secondary metabolites in the common dandelion (Taraxacum officinale agg.)

The secondary metabolites in the roots, leaves and flowers of the common dandelion (Taraxacum officinale agg.) have been studied in detail. However, little is known about the specific constituents of the plant’s highly specialized laticifer cells. Using a combination of liquid and gas chromatography, mass spectrometry and nuclear magnetic resonance spectrometry, we identified and quantified the major secondary metabolites in the latex of different organs across different growth stages in three genotypes, and tested the activity of the metabolites against the generalist root herbivore Diabrotica balteata. We found that common dandelion latex is dominated by three classes of secondary metabolites: phenolic inositol esters (PIEs), triterpene acetates (TritAc) and the sesquiterpene lactone taraxinic acid β-d-glucopyranosyl ester (TA-G). Purification and absolute quantification revealed concentrations in the upper mg g−1 range for all compound classes with up to 6% PIEs, 5% TritAc and 7% TA-G per gram latex fresh weight. Contrary to typical secondary metabolite patterns, concentrations of all three classes increased with plant age. The highest concentrations were measured in the main root. PIE profiles differed both quantitatively and qualitatively between plant genotypes, whereas TritAc and TA-G differed only quantitatively. Metabolite concentrations were positively correlated within and between the different compound classes, indicating tight biosynthetic co-regulation. Latex metabolite extracts strongly repelled D. balteata larvae, suggesting that the latex constituents are biologically active.

The Role of Plant Primary and Secondary Metabolites in Root-Herbivore Behaviour, Nutrition and Physiology

Many insect herbivores feed on belowground plant tissues. In this chapter, we discuss how they have adapted to deal with root primary and secondary metabolites. It is becoming evident that root herbivores can use root volatiles and exudates for host location and foraging. Their complex sensory apparatus suggests a sophisticated recognition and signal transduction system. Furthermore, endogenous metabolites trigger attractive or repellent responses in root feeders, indicating that they may specifically fine-tune food uptake to meet their dietary needs. Little evidence for direct toxic effects of root secondary metabolites has accumulated so far, indicating high prevalence of tolerance mechanisms. Root herbivores furthermore facilitate the entry of soil microbes into the roots, which may influence root nutritional quality. Investigating the role of plant metabolites in an ecologically and physiologically relevant context will be crucial to refine our current models on root-herbivore physiology and behaviour in the future.

A complete english dictionary of the roots of the world-language Volapük, invented by Mgr. Schleyer Johann Martin

comp. and transl. by Scherzinger J. Arnold

Induced Immunity Against Belowground Insect Herbivores- Activation of Defenses in the Absence of a Jasmonate Burst

Roots respond dynamically to belowground herbivore attack. Yet, little is known about the mechanisms and ecological consequences of these responses. Do roots behave the same way as leaves, or do the paradigms derived from aboveground research need to be rewritten? This is the central question that we tackle in this article. To this end, we review the current literature on induced root defenses and present a number of experiments on the interaction between the root herbivore Diabrotica virgifera and its natural host, maize. Currently, the literature provides no clear evidence that plants can recognize root herbivores specifically. In maize, mild mechanical damage is sufficient to trigger a root volatile response comparable to D. virgifera induction. Interestingly, the jasmonate (JA) burst, a highly conserved signaling event following leaf attack, is consistently attenuated in the roots across plant species, from wild tobacco to Arabidopsis. In accordance, we found only a weak JA response in D. virgifera attacked maize roots. Despite this reduction in JA-signaling, roots of many plants start producing a distinct suite of secondary metabolites upon attack and reconfigure their primary metabolism. We, therefore, postulate the existence of additional, unknown signals that govern induced root responses in the absence of a jasmonate burst. Surprisingly, despite the high phenotypic plasticity of plant roots, evidence for herbivore-induced resistance below ground is virtually absent from the literature. We propose that other defensive mechanisms, including resource reallocation and compensatory growth, may be more important to improve plant immunity below ground.

Two enzymes responsible for the formation of herbivore-induced volatiles of maize, the methyltransferase AAMT1 and the terpene synthase TPS23, are regulated by a similar signal transduction pathway

Herbivore-induced volatiles play an important role in the indirect defense of plants. After herbivore damage, volatiles are released from the plant and can attract herbivore enemies that protect the plant from additional damage. The herbivore-induced volatile blend is complex and usually consists of mono- and sesquiterpenes, aromatic compounds, and indole. Although these classes of compounds are generally produced at different times after herbivore damage, the release of the terpene (E)-β-caryophyllene and the aromatic ester methyl anthranilate appear to be tightly coordinated. We have studied the herbivore induction patterns of two terpene synthases from Zea mays L. (Poaceae), TPS23 and TPS10, as well as S-adenosyl-L-methionine:anthranilic acid carboxyl methyltransferases (AAMT1), which are critical for the production of terpenes and anthranilate compounds, respectively. The transcript levels of tps23 and aamt1 displayed the same kinetics after damage by the larvae of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae), and showed the same organ-specific and haplotype-specific expression patterns. Despite its close functional relation to TPS23, the terpene synthase TPS10 is not expressed in roots and does not display the haplotype-specific expression pattern. The results indicate that the same JA-mediated signaling cascade maycontrol the production of both the terpene (E)-β-caryophyllene and aromatic ester methyl anthranilate.

Herbivore-induced plant volatiles mediate host selection by a root herbivore

In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D. virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S. littoralis. We identified (E)-β-caryophyllene, which is induced by D. virgifera, and ethylene, which is suppressed by S. littoralis, as two signals used by D. virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.

A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner

1.Leaf-herbivore attack often triggers induced resistance in plants. However, certain specialist herbivores can also take advantage of the induced metabolic changes. In some cases, they even manipulate plant resistance, leading to a phenomenon called induced susceptibility. Compared to above-ground plant-insect interactions, little is known about the prevalence and consequences of induced responses below-ground. 2.A recent study suggested that feeding by the specialist root herbivore Diabrotica virgifera virgifera makes maize roots more susceptible to conspecifics. To better understand this phenomenon, we conducted a series of experiments to study the behavioural responses and elucidate the underlying biochemical mechanisms. 3.We found that D. virgifera benefitted from feeding on a root system in groups of intermediate size (3–9 larvae/plant in the laboratory), whereas its performance was reduced in large groups (12 larvae/plant). Interestingly, the herbivore was able to select host plants with a suitable density of conspecifics by using the induced plant volatile (E)-β-caryophyllene in a dose-dependent manner. Using a split root experiment, we show that the plant-induced susceptibility is systemic and, therefore, plant mediated. Chemical analyses on plant resource reallocation and defences upon herbivory showed that the systemic induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations and (ii) relaxation of defence inducibility. 4.These findings show that herbivores can use induced plant volatiles in a density-dependent manner to aggregate on a host plant and change its metabolism to their own benefit. Our study furthermore helps to explain the remarkable ecological success of D. virgifera in maize fields around the world.

A specialist root herbivore exploits defensive metabolites to locate nutritious tissues

he most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots

Carbon-11 Reveals Opposing Roles of Auxin and Salicylic Acid in Regulating Leaf Physiology, Leaf Metabolism, and Resource Allocation Patterns that Impact Root Growth in Zea mays

Auxin (IAA) is an important regulator of plant development and root differentiation. Although recent studies indicate that salicylic acid (SA) may also be important in this context by interfering with IAA signaling, comparatively little is known about its impact on the plant’s physiology, metabolism, and growth characteristics. Using carbon-11, a short-lived radioisotope (t 1/2 = 20.4 min) administered as 11CO2 to maize plants (B73), we measured changes in these functions using SA and IAA treatments. IAA application decreased total root biomass, though it increased lateral root growth at the expense of primary root elongation. IAA-mediated inhibition of root growth was correlated with decreased 11CO2 fixation, photosystem II (PSII) efficiency, and total leaf carbon export of 11C-photoassimilates and their allocation belowground. Furthermore, IAA application increased leaf starch content. On the other hand, SA application increased total root biomass, 11CO2 fixation, PSII efficiency, and leaf carbon export of 11C-photoassimilates, but it decreased leaf starch content. IAA and SA induction patterns were also examined after root-herbivore attack by Diabrotica virgifera to place possible hormone crosstalk into a realistic environmental context. We found that 4 days after infestation, IAA was induced in the midzone and root tip, whereas SA was induced only in the upper proximal zone of damaged roots. We conclude that antagonistic crosstalk exists between IAA and SA which can affect the development of maize plants, particularly through alteration of the root system’s architecture, and we propose that the integration of both signals may shape the plant’s response to environmental stress.

Heavy Metals in Crop Plants: Transport and Redistribution Processes on the Whole Plant Level

Copper, zinc, manganese, iron, nickel and molybdenum are essential micronutrients for plants. However, when present in excess they may damage the plant or decrease the quality of harvested plant products. Some other heavy metals such as cadmium, lead or mercury are not needed by plants and represent pollutants. The uptake into the roots, the loading into the xylem, the acropetal transport to the shoot with the transpiration stream and the further redistribution in the phloem are crucial for the distribution in aerial plant parts. This review is focused on long-distance transport of heavy metals via xylem and phloem and on interactions between the two transport systems. Phloem transport is the basis for the redistribution within the shoot and for the accumulation in fruits and seeds. Solutes may be transferred from the xylem to the phloem (e.g., in the small bundles in stems of cereals, in minor leaf veins). Nickel is highly phloem-mobile and directed to expanding plant parts. Zinc and to a lesser degree also cadmium are also mobile in the phloem and accumulate in meristems (root tips, shoot apex, axillary buds). Iron and manganese are characterized by poor phloem mobility and are retained in older leaves.

Effects of PEG-Induced Water Deficit in Solanum nigrum on Zn and Ni Uptake and Translocation in Split Root Systems

Drought strongly influences root activities in crop plants and weeds. This paper is focused on the performance of the heavy metal accumulator Solanum nigrum, a plant which might be helpful for phytoremediation. The water potential in a split root system was decreased by the addition of polyethylene glycol (PEG 6000). Rubidium, strontium and radionuclides of heavy metals were used as markers to investigate the uptake into roots, the release to the shoot via the xylem, and finally the basipetal transport via the phloem to unlabeled roots. The uptake into the roots (total contents in the plant) was for most makers more severely decreased than the transport to the shoot or the export from the shoot to the unlabeled roots via the phloem. Regardless of the water potential in the labeling solution, 63Ni and 65Zn were selectively redistributed within the plant. From autoradiographs, it became evident that 65Zn accumulated in root tips, in the apical shoot meristem and in axillary buds, while 63Ni accumulated in young expanded leaves and roots but not in the meristems. Since both radionuclides are mobile in the phloem and are, therefore, well redistributed within the plant, the unequal transfer to shoot and root apical meristems is most likely caused by differences in the cell-to-cell transport in differentiation zones without functional phloem (immature sieve tubes).

Belowground herbivore tolerance involves delayed overcompensatory root regrowth in maize

Plants can tolerate leaf-herbivore attack through metabolic reconfigurations that allow for the rapid regrowth of lost leaves. Several studies indicate that root-attacked plants can re-allocate resources to the aboveground parts. However, the connection between tolerance and root regrowth remains poorly understood. We investigated the timing and extent of root regrowth of tolerant and susceptible lines of maize, Zea mays L. (Poaceae), attacked by the western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), in the laboratory and the field. Infested tolerant maize plants produced more root biomass and even overcompensated for the lost roots, whereas this effect was absent in susceptible lines. Furthermore, the tolerant plants slowed growth of new roots in the greenhouse and in the field 4–8 days after infestation, whereas susceptible plants slowed growth of new roots only in the field and only after 12 days of infestation. The quick response of tolerant lines may have enabled them to escape root attack by starving the herbivores and by saving resources for regrowth after the attack had ceased. We conclude that both timing and the extent of regrowth may determine plant tolerance to root herbivory.

Belowground ABA boosts aboveground production of DIMBOA and primes induction of chlorogenic acid in maize

Plants are important mediators between above- and belowground herbivores. Consequently, interactions between root and shoot defences can have far-reaching impacts on entire food webs. We recently reported that infestation of maize roots by the root feeding larvae of the beetle Diabrotica virgifera virgifera boosts shoot resistance against herbivores and pathogens. Root herbivory also induced DIMBOA levels and primed for enhanced induction of chlorogenic acid, two secondary metabolites that have been associated with biotic stress resistance. Interestingly, ABA emerged as a putative long-distance signal, possibly responsible for this effect. In this addendum, we investigate the role of root-derived ABA in the systemic regulation of aboveground DIMBOA, and the phenolic compounds chlorogenic acid, caffeic and ferulic acid. We discuss the relevance of the plant hormone in relation to defence against the leaf herbivore Spodoptera littoralis. Soil-drench treatment with ABA mimicked root herbivore-induced accumulation of DIMBOA in the leaves. Similarly, ABA mimicked aboveground priming of chlorogenic acid production, resulting in augmented accumulation of this compound upon subsequent shoot attack by S. littoralis. These findings confirm our notion that ABA acts as an important signal in the regulation of aboveground defence upon belowground herbivory. However, based on our previous finding that ABA alone is not sufficient to trigger aboveground resistance against S. littoralis caterpillars, the results suggest that the ABA-inducible effects on DIMBOA and chlorogenic acid are not solely responsible for root herbivore-induced resistance against S. littoralis. Full text HTML PDF