Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Plaza S

PROVIDER: S-EPMC4427619 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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

Plaza Sonia S Weber Johann J Pajonk Simone S Thomas Jérôme J Talke Ina N IN Schellenberg Maja M Pradervand Sylvain S Burla Bo B Geisler Markus M Martinoia Enrico E Krämer Ute U

Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine 20150310 3

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 mechan ...[more]

PMID: 25753945

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Project description:Phytohormones, especially jasmonates, are known to be mediators of the plant responses to wounding and herbivore feeding. Their role in such stress responses has been largely studied locally in treated leaves. However, less is known about the induced systemic distribution of phytohormone signals upon these kinds of stresses. Here, a holistic approach was performed in order to investigate the systemic phytohormone pattern in the rosette of Arabidopsis thaliana after herbivore-related wounding. Levels of different stress-related phytohormones such as jasmonates, abscisic acid, and salicylic acid were analyzed in individual leaves. We demonstrate that the typically used sampling method, where leaves are first cut and immediately frozen, causes false-positive results since cutting already induces systemic jasmonate elevations within less than 1.6 min. Therefore, this approach is not suitable to study systemic phytohormone changes in the whole plant. By developing a new method where leaves are frozen first and subsequently cut, sampling-induced phytohormone elevations could be reduced. Using this new method, we show that jasmonic acid and its active isoleucine conjugate (jasmonoyl-isoleucine) are involved in the fast systemic wound response of Arabidopsis. A systemic induction of the jasmonates' precursor, 12-oxo-phytodienoic acid, was not observed throughout our treatments. The systemic phytohormone distribution pattern is strongly linked to the vascular connections between the leaves, providing further evidence that the vascular system is used for long distance-signaling in Arabidopsis. Besides already known vascular connections, we also demonstrate that the systemic distribution of jasmonate signals can be extended to distant leaves, which are systemically but indirectly connected via another vascularly connected leaf. This holistic approach covering almost the whole Arabidopsis rosette introduces a method to overcome false-positive results in systemic phytohormone determinations and demonstrates that wounding-induced long-distance signaling includes fast changes in jasmonate levels in systemic, non-treated leaves.

Project description:In compatible interactions, biotrophic microbial phytopathogens rely on the supply of assimilates by the colonized host tissue. It has been found in rice that phloem localized SWEET sucrose transporters can be reprogrammed by bacterial effectors to establish compatibility. We observed that sweet11/sweet12 double mutants, but not single mutants, exhibited increased resistance toward the fungal hemibiotroph Colletotrichum higginsianum (Ch), both in the biotrophic and the necrotrophic colonization phase. We therefore investigated if the phloem localized transporters AtSWEET11 and AtSWEET12 represent additive susceptibility factors in the interaction of Arabidopsis with Ch. AtSWEET12-YFP fusion protein driven by the endogenous promoter strongly accumulated at Ch infection sites and in the vasculature upon challenge with Ch. However, susceptibility of sweet12 single mutants to Ch was comparable to wild type, indicating that the accumulation of AtSWEET12 at Ch infection sites does not play a major role for compatibility. AtSWEET12-YFP reporter protein was not detectable at the plant-pathogen interface, suggesting that AtSWEET12 is not targeted by Ch effectors. AtSWEET11-YFP accumulation in pAtSWEET11:AtSWEET11-YFP plants were similar in Ch infected and mock control leaves. A close inspection of major carbohydrate metabolism in non-infected control plants revealed that soluble sugar and starch content were substantially elevated in sweet11/sweet12 double mutants during the entire diurnal cycle, that diurnal soluble sugar turnover was increased more than twofold in sweet11/sweet12, and that accumulation of free hexoses and sucrose was strongly expedited in double mutant leaves compared to wild type and both single mutants during the course of Ch infection. After 2 days of treatment, free and conjugated SA levels were significantly increased in infected and mock control leaves of sweet11/sweet12 relative to all other genotypes, respectively. Induced genes in mock treated sweet11/sweet12 leaves were highly significantly enriched for several GO terms associated with SA signaling and response compared to mock treated wild-type leaves, indicating sugar-mediated priming of the SA pathway in the double mutant. Infection assays with salicylic acid deficient sweet11/sweet12/sid2 triple mutants demonstrated that reduced susceptibility observed in sweet11/sweet12 was entirely dependent on the SA pathway. We suggest a model how defects in phloem loading of sucrose can influence SA priming and hence, compatibility.

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Dataset Information

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

Publications

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

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