Papers by Enrico Martinoia
Proceedings of the National Academy of Sciences of the United States of America, Dec 26, 2012
Plant Biotechnology Journal, Mar 25, 2018
Arsenic (As) is a poisonous element that causes severe skin lesions and cancer in humans. Rice (O... more Arsenic (As) is a poisonous element that causes severe skin lesions and cancer in humans. Rice (Oryza sativa L.) is a major dietary source of As in humans who consume this cereal as a staple food. We hypothesized that increasing As vacuolar sequestration would inhibit its translocation into the grain and reduce the amount of As entering the food chain. We developed transgenic rice plants expressing two different vacuolar As sequestration genes, ScYCF1 and OsABCC1, under the control of the RCc3 promoter in the root cortical and internode phloem cells, along with a bacterial γ-glutamylcysteine synthetase driven by the maize UBI promoter. The transgenic rice plants exhibited reduced root-to-shoot and internode-to-grain As translocation, resulting in a 70% reduction in As accumulation in the brown rice without jeopardizing agronomic traits. This technology could be used to reduce As intake, particularly in populations of South East Asia suffering from As toxicity, and thereby improve human health.
BMC Biology, Oct 25, 2017
Hormone transporters are crucial for plant hormone action, which is underlined by severe developm... more Hormone transporters are crucial for plant hormone action, which is underlined by severe developmental and physiological impacts caused by their loss-offunction mutations. Here, we summarize recent knowledge on the individual roles of plant hormone transporters in local and long-distance transport. Our inventory reveals that many hormones are transported by members of distinct transporter classes, with an apparent dominance of the ATP-binding cassette (ABC) family and of the Nitrate transport1/Peptide transporter family (NPF). The current need to explore further hormone transporter regulation, their functional interaction, transport directionalities, and substrate specificities is briefly reviewed. Plants need many hormone transporters The hormone concept was coined in the beginning of the 20th century, although it had been already postulated by the Darwins based on their observation that phototropic bending of coleoptiles employs a spatial separation between the place of sensing in the shoot tip and the place of bending in the shoot below [1]. Today we know that what Darwin called 'certain influence' [1] is the phytohormone auxin, which is synthesized in the coleoptile tip, where light is sensed, and transported down to the appropriate site of action in the shoot [2]. Since then, many plant hormones have been identified and most have been found to be synthesized at different sites from their actions. Thus, it has become evident that hormones are transported, and consequently, hormone transporters are essential for precise regulation of plant growth and development by plant hormones. Now we understand that the proper integration of environmental
Nature Cell Biology, Sep 7, 2008
Carbon dioxide uptake and water vapour release in plants occur through stomata, which are formed ... more Carbon dioxide uptake and water vapour release in plants occur through stomata, which are formed by guard cells. These cells respond to light intensity, CO2 and water availability, and plant hormones. The predicted increase in the atmospheric concentration of CO2 is expected to have a profound effect on our ecosystem. However, many aspects of CO2-dependent stomatal movements are still not understood. Here we show that the ABC transporter AtABCB14 modulates stomatal closure on transition to elevated CO2. Stomatal closure induced by high CO2 levels was accelerated in plants lacking AtABCB14. Apoplastic malate has been suggested to be one of the factors mediating the stomatal response to CO2 (Refs 4,5) and indeed, exogenously applied malate induced a similar AtABCB14-dependent response as high CO2 levels. In isolated epidermal strips that contained only guard cells, malate-dependent stomatal closure was faster in plants lacking the AtABCB14 and slower in AtABCB14-overexpressing plants, than in wild-type plants, indicating that AtABCB14 catalyses the transport of malate from the apoplast into guard cells. Indeed, when AtABCB14 was heterologously expressed in Escherichia coli and HeLa cells, increases in malate transport activity were observed. We therefore suggest that AtABCB14 modulates stomatal movement by transporting malate from the apoplast into guard cells, thereby increasing their osmotic pressure.
Frontiers in Plant Science, 2021
Nitrogen (N) as well as Phosphorus (P) are key nutrients determining crop productivity. Legumes h... more Nitrogen (N) as well as Phosphorus (P) are key nutrients determining crop productivity. Legumes have developed strategies to overcome nutrient limitation by, for example, forming a symbiotic relationship with N-fixing rhizobia and the release of P-mobilizing exudates and are thus able to grow without supply of N or P fertilizers. The legume-rhizobial symbiosis starts with root release of isoflavonoids that act as signaling molecules perceived by compatible bacteria. Subsequently, bacteria release nod factors, which induce signaling cascades allowing the formation of functional N-fixing nodules. We report here the identification and functional characterization of a plasma membrane-localized MATE-type transporter (LaMATE2) involved in the release of genistein from white lupin roots. The LaMATE2 expression in the root is upregulated under N deficiency as well as low phosphate availability, two nutritional deficiencies that induce the release of this isoflavonoid. LaMATE2 silencing redu...
Frontiers in Plant Science, 2019
The PDR-type ABCG transporter, ABCG36/PDR8/PEN3, is thought to be implicated in the export of a f... more The PDR-type ABCG transporter, ABCG36/PDR8/PEN3, is thought to be implicated in the export of a few structurally unrelated substrates, including the auxin precursor, indole-3-butyric acid (IBA), although a clear-cut proof of transport is lacking. An outward facing, lateral root (LR) location for ABCG36 fuelled speculations that it might secrete IBA into the rhizosphere. Here, we provide strong evidence that ABCG36 catalyzes the export of IBA-but not of indole-3-acetic acid-through the plasma membrane. ABCG36 seems to function redundantly with the closely related isoform ABCG37/PDR9/PIS1 in a negative control of rootward IBA transport in roots, which might be dampened by concerted, lateral IBA export. Analyses of single and double mutant phenotypes suggest that both ABCG36 and ABCG37 function cooperatively in auxin-controlled plant development. Both seem to possess a dual function in the control of auxin homeostasis in the root tip and long-range transport in the mature root correlating with non-polar and polar expression profiles in the LR cap and epidermis, respectively.
Annals of Botany, 2000
Cluster root formation in white lupin (Lupinus albus L.) is induced mainly by phosphorus (P) star... more Cluster root formation in white lupin (Lupinus albus L.) is induced mainly by phosphorus (P) starvation, and seems to be regulated by the endogenous P status of the plant. Increased formation of cluster roots, when indole acetic acid is supplied to the growth medium of P sucient plants, and inhibitory eects of kinetin application suggest the involvement of endogenous phytohormones (auxins and cytokinins), which may act in an antagonistic manner in the P-starvation response. Phosphorus de®ciency-induced adaptations of white lupin, involved in P acquisition and mobilization of sparingly available P sources, are predominantly con®ned to the cluster roots, and moreover to distinct stages during their development. Increased accumulation and exudation of citrate and a concomitant release of protons were found to be mainly restricted to mature root clusters after prolonged culture (3±4 weeks) under P-de®cient conditions. Inhibition of citrate exudation by exogenous application of anion channel antagonists such as ethacrynic-and anthracene-9-carboxylic acids may indicate involvement of an anion channel. Phosphorus de®ciencyinduced accumulation and subsequent exudation of citric acid seems to be a consequence of both enhanced biosynthesis and reduced turnover of citric acid in the cluster root tissue, indicated by enhanced expression of sucrose synthase, fructokinase, phosphoglucomutase, phosphoenol-pyruvate carboxylase, but reduced activity of aconitase and slower root respiration. The release of acid phosphatase and of phenolic compounds (iso¯avonoids) as well as the induction of a putative high-anity P uptake system was more highly expressed in juvenile, mature and even senescent cluster regions than in apical zones of non-proteoid roots. An AFLP-cDNA library for cluster root-speci®c gene expression was constructed to assist in the identi®cation of further genes involved in cluster root development.
Molecular plant, Jan 19, 2016
Terrestrial plants have two to four times more ATP-binding cassette (ABC) transporter genes than ... more Terrestrial plants have two to four times more ATP-binding cassette (ABC) transporter genes than do other organisms, including their ancestral microalgae. Recent studies found that plants harboring mutations in these transporters exhibit dramatic phenotypes, many of which are related to developmental processes and functions necessary for life on dry land. These results suggest that ABC transporters multiplied during evolution and assumed novel functions that allowed plants to adapt to terrestrial environmental conditions. Examining the literature on plant ABC transporters from this viewpoint led us to propose that diverse ABC transporters enabled many unique and essential aspects of a terrestrial plant's lifestyle, by transporting various compounds across specific membranes of the plant.
Current Opinion in Plant Biology, 2015
Mycorrhizas play a pivotal role in phosphorus (P) acquisition of plant roots, by enhancing the so... more Mycorrhizas play a pivotal role in phosphorus (P) acquisition of plant roots, by enhancing the soil volume that can be explored. Non-mycorrhizal plant species typically occur either in relatively fertile soil or on soil with a very low P availability, where there is insufficient P in the soil solution for mycorrhizal hyphae to be effective. Soils with a very low P availability are either old and severely weathered or relatively young with high concentrations of oxides and hydroxides of aluminium and iron that sorb P. In such soils, cluster roots and other specialised roots that release P-mobilising carboxylates are more effective than mycorrhizas. Cluster roots are ephemeral structures that release carboxylates in an exudative burst. The carboxylates mobilise sparingly-available sources of soil P. The relative investment of biomass in cluster roots and the amount of carboxylates that are released during the exudative burst differ between species on severely weathered soils with a low total P concentration and species on young soils with high total P concentrations but low P availability. Taking a modelling approach, we explore how the optimal cluster-root strategy depends on soil characteristics, thus offering insights for plant breeders interested in developing crop plants with optimal cluster-root strategies.
Signaling and Communication in Plants, 2014
The first evidence showing that ABC transporters are involved in heavy metal resistance in eukary... more The first evidence showing that ABC transporters are involved in heavy metal resistance in eukaryotic cells has been obtained from experiments in Schizosaccharomyces pombe and Saccharomyces cerevisae, where a half-size transporter of the ABCB subclass and an ABCC-type transporter, respectively, have been shown to confer heavy metal tolerance. Biochemical studies have indicated that vacuolar ABC transporters should also play an important role in heavy metal detoxification in plants. But it was only recently that two ABCC-type transporters, AtABCC1 and AtABCC2, have been identified as major apo-phytochelatin and phytochelatin-heavy metal(oid) complex transporters. Several plasma membrane transporters have also been shown to confer heavy metal resistance. However, with the exception of STAR1, an UDP glucose exporter, which—by altering cell wall composition—confers aluminum tolerance, the substrates required to be transported to confer heavy metal resistance by these plasma membrane-localized ABC proteins are still not elucidated. A mitochondrial ABC transporter AtATM3 was shown to be required for plant growth and development. The different studies indicate that this transporter is important for the production of cytosolic iron sulfur complexes and molybdenum cofactors, prosthetic groups required for several enzymes. However, the final proof as to which substrate is transported by AtATM3 is still missing. Several laboratories took advantage of the fact that ABC transporters are involved in heavy metal tolerance to generate transgenic plants suitable for phytoremediation. The results show that overexpression of ABC proteins alone is not sufficient to produce plants that can efficiently decontaminate soils, but they indicate that this class of transporters, when combined with other transporters and enzymes involved in heavy metal transport and detoxification, may prove a good solution to produce plants that can stabilize, and in the long term clean up, soils contaminated with heavy metals.
Proceedings of the National Academy of Sciences of the United States of America, Jan 4, 2014
Arsenic (As) is a chronic poison that causes severe skin lesions and cancer. Rice (Oryza sativa L... more Arsenic (As) is a chronic poison that causes severe skin lesions and cancer. Rice (Oryza sativa L.) is a major dietary source of As; therefore, reducing As accumulation in the rice grain and thereby diminishing the amount of As that enters the food chain is of critical importance. Here, we report that a member of the Oryza sativa C-type ATP-binding cassette (ABC) transporter (OsABCC) family, OsABCC1, is involved in the detoxification and reduction of As in rice grains. We found that OsABCC1 was expressed in many organs, including the roots, leaves, nodes, peduncle, and rachis. Expression was not affected when plants were exposed to low levels of As but was up-regulated in response to high levels of As. In both the basal nodes and upper nodes, which are connected to the panicle, OsABCC1 was localized to the phloem region of vascular bundles. Furthermore, OsABCC1 was localized to the tonoplast and conferred phytochelatin-dependent As resistance in yeast. Knockout of OsABCC1 in rice re...
Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine, Jan 10, 2015
Approximately 0.2 % of all angiosperms are classified as metal hyperaccumulators based on their e... more 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, sup...
The present invention relates to a composition for phytochelatin transport, comprising DNA molecu... more The present invention relates to a composition for phytochelatin transport, comprising DNA molecules encoding ABCC (MRP, multidrug resistance-associated protein)-like ABC (ATP-binding cassette) transporter proteins in plants. The composition for phytochelatin transport according to the present invention can accumulate and sequester phytochelatin alone or in combination with a toxic substance by transporting same into the vacuole of a cell, and thus reduce the content of the toxic substance which moves from the root of a plant to the shoot thereof. Therefore, the DNA molecules of the present invention can be applied to the development of crops in which the content of toxic substances existing in edible plant parts such as leaves, stems, and fruits are reduced. Furthermore, the DNA molecules of the present invention are applied to inedible plants to develop plants which are useful in phytoremediation, or phytoextraction, by increasing the accumulated amounts of arsenic, arsenic compounds, and cadmium, and the resistances thereto, thereby economically cleaning the environment in an environmentally friendly manner is possible.
Frontiers in Plant Science, 2012
In contrast to mammalian ABCB1 proteins, narrow substrate specificity has been extensively docume... more In contrast to mammalian ABCB1 proteins, narrow substrate specificity has been extensively documented for plant orthologs shown to catalyze the transport of the plant hormone, auxin. Using the crystal structures of the multidrug exporters Sav1866 and MmABCB1 as templates, we have developed structural models of plant ABCB proteins with a common architecture. Comparisons of these structures identified kingdom-specific candidate substrate-binding regions within the translocation chamber formed by the transmembrane domains of ABCBs from the model plant Arabidopsis. These results suggest an early evolutionary divergence of plant and mammalian ABCBs. Validation of these models becomes a priority for efforts to elucidate ABCB function and manipulate this class of transporters to enhance plant productivity and quality.
Proceedings of the National Academy of Sciences of the United States of America, Jan 7, 2010
Arsenic is an extremely toxic metalloid causing serious health problems. In Southeast Asia, aquif... more Arsenic is an extremely toxic metalloid causing serious health problems. In Southeast Asia, aquifers providing drinking and agricultural water for tens of millions of people are contaminated with arsenic. To reduce nutritional arsenic intake through the consumption of contaminated plants, identification of the mechanisms for arsenic accumulation and detoxification in plants is a prerequisite. Phytochelatins (PCs) are glutathione-derived peptides that chelate heavy metals and metalloids such as arsenic, thereby functioning as the first step in their detoxification. Plant vacuoles act as final detoxification stores for heavy metals and arsenic. The essential PC-metal(loid) transporters that sequester toxic metal(loid)s in plant vacuoles have long been sought but remain unidentified in plants. Here we show that in the absence of two ABCC-type transporters, AtABCC1 and AtABCC2, Arabidopsis thaliana is extremely sensitive to arsenic and arsenic-based herbicides. Heterologous expression o...
Plant Physiology, 2000
Several lines of evidence suggest that regulation of intracellular Ca 2ϩ levels is crucial for ad... more Several lines of evidence suggest that regulation of intracellular Ca 2ϩ levels is crucial for adaptation of plants to environmental stress. We have cloned and characterized Arabidopsis auto-inhibited Ca 2ϩ-ATPase, isoform 4 (ACA4), a calmodulinregulated Ca 2ϩ-ATPase. Confocal laser scanning data of a green fluorescent protein-tagged version of ACA4 as well as western-blot analysis of microsomal fractions obtained from two-phase partitioning and Suc density gradient centrifugation suggest that ACA4 is localized to small vacuoles. The N terminus of ACA4 contains an auto-inhibitory domain with a binding site for calmodulin as demonstrated through calmodulin-binding studies and complementation experiments using the calcium transport yeast mutant K616. ACA4 and PMC1, the yeast vacuolar Ca 2ϩ-ATPase, conferred protection against osmotic stress such as high NaCl, KCl, and mannitol when expressed in the K616 strain. An N-terminally modified form of ACA4 specifically conferred increased NaCl tolerance, whereas full-length ATPase had less effect.
The Arabidopsis book / American Society of Plant Biologists, 2011
ABC transporters constitute one of the largest protein families found in all living organisms. AB... more ABC transporters constitute one of the largest protein families found in all living organisms. ABC transporters are driven by ATP hydrolysis and can act as exporters as well as importers. The plant genome encodes for more than 100 ABC transporters, largely exceeding that of other organisms. In Arabidopsis, only 22 out of 130 have been functionally analyzed. They are localized in most membranes of a plant cell such as the plasma membrane, the tonoplast, chloroplasts, mitochondria and peroxisomes and fulfill a multitude of functions. Originally identified as transporters involved in detoxification processes, they have later been shown to be required for organ growth, plant nutrition, plant development, response to abiotic stresses, pathogen resistance and the interaction of the plant with its environment. To fulfill these roles they exhibit different substrate specifies by e.g. depositing surface lipids, accumulating phytate in seeds, and transporting the phytohormones auxin and absci...
The Plant Cell, 2011
Transgenic tomato (Solanum lycopersicum) plants expressing a fragment of the Sl SDH2-2 gene encod... more Transgenic tomato (Solanum lycopersicum) plants expressing a fragment of the Sl SDH2-2 gene encoding the iron sulfur subunit of the succinate dehydrogenase protein complex in the antisense orientation under the control of the 35S promoter exhibit an enhanced rate of photosynthesis. The rate of the tricarboxylic acid (TCA) cycle was reduced in these transformants, and there were changes in the levels of metabolites associated with the TCA cycle. Furthermore, in comparison to wild-type plants, carbon dioxide assimilation was enhanced by up to 25% in the transgenic plants under ambient conditions, and mature plants were characterized by an increased biomass. Analysis of additional photosynthetic parameters revealed that the rate of transpiration and stomatal conductance were markedly elevated in the transgenic plants. The transformants displayed a strongly enhanced assimilation rate under both ambient and suboptimal environmental conditions, as well as an elevated maximal stomatal aper...
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Papers by Enrico Martinoia