Abstract
BackgroundArbuscular mycorrhizal (AM) fungi, which engage a mutualistic symbiosis with the roots of most plant species, have received much attention for their ability to alleviate heavy metal stress in plants, including cadmium (Cd). While the molecular bases of Cd tolerance displayed by mycorrhizal plants have been extensively analysed in roots, very little is known regarding the mechanisms by which legume aboveground organs can escape metal toxicity upon AM symbiosis. As a model system to address this question, we used Glomus irregulare-colonised Medicago truncatula plants, which were previously shown to accumulate and tolerate heavy metal in their shoots when grown in a substrate spiked with 2 mg Cd kg-1.ResultsThe measurement of three indicators for metal phytoextraction showed that shoots of mycorrhizal M. truncatula plants have a capacity for extracting Cd that is not related to an increase in root-to-shoot translocation rate, but to a high level of allocation plasticity. When analysing the photosynthetic performance in metal-treated mycorrhizal plants relative to those only Cd-supplied, it turned out that the presence of G. irregulare partially alleviated the negative effects of Cd on photosynthesis. To test the mechanisms by which shoots of Cd-treated mycorrhizal plants avoid metal toxicity, we performed a 2-DE/MALDI/TOF-based comparative proteomic analysis of the M. truncatula shoot responses upon mycorrhization and Cd exposure. Whereas the metal-responsive shoot proteins currently identified in non-mycorrhizal M. truncatula indicated that Cd impaired CO2 assimilation, the mycorrhiza-responsive shoot proteome was characterised by an increase in photosynthesis-related proteins coupled to a reduction in glugoneogenesis/glycolysis and antioxidant processes. By contrast, Cd was found to trigger the opposite response coupled the up-accumulation of molecular chaperones in shoot of mycorrhizal plants relative to those metal-free.ConclusionBesides drawing a first picture of shoot proteome modifications upon AM symbiosis and/or heavy metal stress in legume plants, the current work argues for allocation plasticity as the main driving force for Cd extraction in aboveground tissues of M. truncatula upon mycorrhization. Additionally, according to the retrieved proteomic data, we propose that shoots of mycorrhizal legume plants escape Cd toxicity through a metabolic shift implying the glycolysis-mediated mobilization of defence mechanisms at the expense of the photosynthesis-dependent symbiotic sucrose sink.
Highlights
Arbuscular mycorrhizal (AM) fungi, which engage a mutualistic symbiosis with the roots of most plant species, have received much attention for their ability to alleviate heavy metal stress in plants, including cadmium (Cd)
Shoots of mycorrhizal M. truncatula plants have a capacity for extracting Cd, which is not related to an increase in root-to-shoot translocation rate but to allocation plasticity To go further in analysing the tolerance to Cd displayed by M. truncatula when colonised by the AM fungus Glomus irregulare [22], we have investigated in the current study the potential contribution of mycorrhizal plants to phytoextraction, which refers to the transfer of inorganic contaminants from soil to harvestable aboveground plant tissues [25]
To take into account biomass production, which escapes indices calculated on the basis of Cd concentration [27,28], three main indicators have been used to measure plant effectiveness in extracting Cd from soil: the tolerance index expressed as the ratio of shoot growth parameters for plants grown in polluted soil to plants grown in metal-free soil [26,27,29], the transport factor calculated as the ratio of the total Cd amount in shoots to that in roots [27,30], and Cd partitioning that corresponds to the metal quantity present in plant organs [28]
Summary
Arbuscular mycorrhizal (AM) fungi, which engage a mutualistic symbiosis with the roots of most plant species, have received much attention for their ability to alleviate heavy metal stress in plants, including cadmium (Cd). Several mechanisms susceptible to counteract Cd toxicity have been identified in plants including active efflux and reduced transport at the plasmalemma, metal chelation by high-affinity ligands such as phytochelatins, glutathione and metallothioneins, and compartmentalization into the vacuole [7]. Besides these intracellular processes, exudates secretion, metal binding to the cell wall and rhizospheric microorganisms have the potential to contribute to plant defence mechanisms against Cd toxicity [2,8,9]
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