Malate. Jack of all trades or master of a few?

Fernie, Alisdair R.; Martinoia, Enrico

doi:10.1016/j.phytochem.2009.04.023

Cited by 162 publications

(130 citation statements)

References 70 publications

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“…A recent work shows that B. subtilis prefers MA as a carbon source and inflicts metabolite repression to take up other carbon sources for an efficient MA uptake (for review, see Fernie and Martinoia, 2009;Kleijn et al, 2010). This recent data validates the specificity and preference of B. subtilis for MA.…”

Section: Foliar Mamps Trigger Root Fb17 Colonizationsupporting

confidence: 61%

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

et al. 2012

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This study demonstrated that foliar infection by Pseudomonas syringae pv tomato DC3000 induced malic acid (MA) transporter (ALUMINUM-ACTIVATED MALATE TRANSPORTER1 [ALMT1]) expression leading to increased MA titers in the rhizosphere of Arabidopsis (Arabidopsis thaliana). MA secretion in the rhizosphere increased beneficial rhizobacteria Bacillus subtilis FB17 (hereafter FB17) titers causing an induced systemic resistance response in plants against P. syringae pv tomato DC3000. Having shown that a live pathogen could induce an intraplant signal from shoot-to-root to recruit FB17 belowground, we hypothesized that pathogen-derived microbe-associated molecular patterns (MAMPs) may relay a similar response specific to FB17 recruitment. The involvement of MAMPs in triggering plant innate immune response is well studied in the plant's response against foliar pathogens. In contrast, MAMPs-elicited plant responses on the roots and the belowground microbial community are not well understood. It is known that pathogen-derived MAMPs suppress the root immune responses, which may facilitate pathogenicity. Plants subjected to known MAMPs such as a flagellar peptide, flagellin22 (flg22), and a pathogen-derived phytotoxin, coronatine (COR), induced a shoot-to-root signal regulating ALMT1 for recruitment of FB17. Micrografts using either a COR-insensitive mutant (coi1) or a flagellin-insensitive mutant (fls2) as the scion and ALMT1 pro :b-glucuronidase as the rootstock revealed that both COR and flg22 are required for a graft transmissible signal to recruit FB17 belowground. The data suggest that MAMPs-induced signaling to regulate ALMT1 is salicylic acid and JASMONIC ACID RESISTANT1 (JAR1)/JASMONATE INSENSITIVE1 (JIN1)/MYC2 independent. Interestingly, a cell culture filtrate of FB17 suppressed flg22-induced MAMPsactivated root defense responses, which are similar to suppression of COR-mediated MAMPs-activated root defense, revealing a diffusible bacterial component that may regulate plant immune responses. Further analysis showed that the biofilm formation in B. subtilis negates suppression of MAMPs-activated defense responses in roots. Moreover, B. subtilis suppression of MAMPs-activated root defense does require JAR1/JIN1/MYC2. The ability of FB17 to block the MAMPselicited signaling pathways related to antibiosis reflects a strategy adapted by FB17 for efficient root colonization. These experiments demonstrate a remarkable strategy adapted by beneficial rhizobacteria to suppress a host defense response, which may facilitate rhizobacterial colonization and host-mutualistic association.

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Section: Foliar Mamps Trigger Root Fb17 Colonizationsupporting

confidence: 61%

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

et al. 2012

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“…Both, malate and citrate are centrally positioned in the plant primary metabolism network, and are found in the apoplast as well as in several cellular compartments such as the cytosol, mitochondria, peroxisomes, glyoxysomes, chloroplasts and vacuoles (3,26,27). Latter organelle can occupy up to 90% of the cell volume, making the vacuole responsible for dynamic storage of malate.…”

Section: Attdt Activity Limits Vacuolar Malate Accumulation In Arabidmentioning

confidence: 99%

Purification and functional characterization of the vacuolar malate transporter tDT from Arabidopsis

Frei

Eisenach

Martinoia

et al. 2018

Journal of Biological Chemistry

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The exact transport characteristics of the vacuolar dicarboxylate transporter tDT from Arabidopsis are elusive. To overcome this limitation, we combined a range of experimental approaches comprising generation/analysis of tDT overexpressors, 13 CO 2 feeding and quantification of 13 C enrichment, functional characterization of tDT in proteoliposomes and electrophysiological studies on vacuoles. tdt knock-out plants showed decreased malate and increased citrate concentrations in leaves during the diurnal light-dark rhythm and after onset of drought, when compared to wild types. Interestingly, under latter two conditions tDT overexpressors exhibited malate-and citrate levels opposite to tdt knock-out plants. Highly purified tDT protein transports malate and citrate in a 1:1 antiport mode. The apparent affinity for malate decreased with decreasing pH, while citrate affinity increased. This observation indicates that tDt exhibits a preference for dianion substrates, which is supported by electrophysiological analysis on intact vacuoles. tDT also accepts fumarate and succinate as substrates, but not α-ketoglutarate, gluconate, sulphate or phosphate. Taking tDT as an example we demonstrated that it is possible to reconstitute a vacuolar metabolite transporter functionally in proteoliposomes. The displayed, so far unknown counter-exchange properties of tDT now explains the frequently observed reciprocal concentration changes of malate and citrate in leaves from various plant species. tDT from Arabidopsis is the first member of the wellknown and widely present SLC13 group of carrier proteins, exhibiting an antiport mode of transport.

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“…This finding led to follow-up work demonstrating that the level of malate played an important role in tomato fruit ripening influencing starch accumulation, total soluble solid levels at ripening, and postharvest properties (Centeno et al, 2011), when taken alongside the results of many recent studies on the control of stomatal aperture by malate (NunesNesi et al, 2007;Lee et al, 2008;Araújo et al, 2011;Penfield et al, 2012), thus expanding the documented biological roles for this acid beyond those previously documented (Fernie and Martinoia, 2009;Meyer et al, 2010). This finding thus suggests that malate metabolism may exert a key influence on the normal ripening and metabolism of tomato fruit.…”

mentioning

confidence: 91%

Alteration of the Interconversion of Pyruvate and Malate in the Plastid or Cytosol of Ripening Tomato Fruit Invokes Diverse Consequences on Sugar But Similar Effects on Cellular Organic Acid, Metabolism, and Transitory Starch Accumulation

et al. 2012

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The aim of this work was to investigate the effect of decreased cytosolic phosphoenolpyruvate carboxykinase (PEPCK) and plastidic NADP-dependent malic enzyme (ME) on tomato (Solanum lycopersicum) ripening. Transgenic tomato plants with strongly reduced levels of PEPCK and plastidic NADP-ME were generated by RNA interference gene silencing under the control of a ripening-specific E8 promoter. While these genetic modifications had relatively little effect on the total fruit yield and size, they had strong effects on fruit metabolism. Both transformants were characterized by lower levels of starch at breaker stage. Analysis of the activation state of ADP-glucose pyrophosphorylase correlated with the decrease of starch in both transformants, which suggests that it is due to an altered cellular redox status. Moreover, metabolic profiling and feeding experiments involving positionally labeled glucoses of fruits lacking in plastidic NADP-ME and cytosolic PEPCK activities revealed differential changes in overall respiration rates and tricarboxylic acid (TCA) cycle flux. Inactivation of cytosolic PEPCK affected the respiration rate, which suggests that an excess of oxaloacetate is converted to aspartate and reintroduced in the TCA cycle via 2-oxoglutarate/glutamate. On the other hand, the plastidic NADP-ME antisense lines were characterized by no changes in respiration rates and TCA cycle flux, which together with increases of pyruvate kinase and phosphoenolpyruvate carboxylase activities indicate that pyruvate is supplied through these enzymes to the TCA cycle. These results are discussed in the context of current models of the importance of malate during tomato fruit ripening.

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Malate. Jack of all trades or master of a few?

Cited by 162 publications

References 70 publications

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

Purification and functional characterization of the vacuolar malate transporter tDT from Arabidopsis

Alteration of the Interconversion of Pyruvate and Malate in the Plastid or Cytosol of Ripening Tomato Fruit Invokes Diverse Consequences on Sugar But Similar Effects on Cellular Organic Acid, Metabolism, and Transitory Starch Accumulation

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