The conditional fluorescent ( flu ) mutant of Arabidopsis accumulates the photosensitizer protochlorophyllide in the dark. After a dark-to-light shift, the generation of singlet oxygen, a nonradical reactive oxygen species, starts within the first minute of illumination and was shown to be confined to plastids. Immediately after the shift, plants stopped growing and developed necrotic lesions. These early stress responses of the flu mutant do not seem to result merely from physicochemical damage. Peroxidation of chloroplast membrane lipids in these plants started rapidly and led to the transient and selective accumulation of a stereospecific and regiospecific isomer of hydroxyoctadecatrieonic acid, free (13 S )-HOTE, that could be attributed almost exclusively to the enzymatic oxidation of linolenic acid. Within the first 15 min of reillumination, distinct sets of genes were activated that were different from those induced by superoxide/hydrogen peroxide. Collectively, these results demonstrate that singlet oxygen does not act primarily as a toxin but rather as a signal that activates several stress-response pathways. Its biological activity in Arabidopsis exhibits a high degree of specificity that seems to be derived from the chemical identity of this reactive oxygen species and/or the intracellular location at which it is generated.
Truffles are symbiotic fungi that form ectomycorrhizas with plant roots. Here we present evidence that at an early stage of the interaction, i.e. prior to physical contact, mycelia of the white truffle Tuber borchii and the black truffle Tuber melanopsorum induce alterations in root morphology of the host Cistus incanus and the nonhost Arabidopsis (Arabidopsis thaliana; i.e. primary root shortening, lateral root formation, root hair stimulation). This was most likely due to the production of indole-3-acetic acid (IAA) and ethylene by the mycelium. Application of a mixture of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid and IAA fully mimicked the root morphology induced by the mycelium for both host and nonhost plants. Application of the single hormones only partially mimicked it. Furthermore, primary root growth was not inhibited in the Arabidopsis auxin transport mutant aux1-7 by truffle metabolites while root branching was less effected in the ethylene-insensitive mutant ein2-LH. The double mutant aux1-7;ein2-LH displayed reduced sensitivity to fungus-induced primary root shortening and branching. In agreement with the signaling nature of truffle metabolites, increased expression of the auxin response reporter DR5::GFP in Arabidopsis root meristems subjected to the mycelium could be observed, confirming that truffles modify the endogenous hormonal balance of plants. Last, we demonstrate that truffles synthesize ethylene from L-methionine probably through the a-keto-g-(methylthio)butyric acid pathway. Taken together, these results establish the central role of IAA and ethylene as signal molecules in truffle/plant interactions.
The jasmonate family of phytohormones, as represented by 12-oxo-phytodienoic acid (OPDA), dinor-phytodienoic acid (dn-OPDA), and jasmonic acid in Arabidopsis (Arabidopsis thaliana), has been implicated in a vast array of different developmental processes and stress responses. Recent reports indicate that OPDA and dn-OPDA occur not only as free acids in Arabidopsis, but also as esters with complex lipids, so-called arabidopsides. Recently, we showed that recognition of the two bacterial effector proteins AvrRpm1 and AvrRpt2 induced high levels of a molecule consisting of two OPDAs and one dn-OPDA esterified to a monogalactosyl diacylglycerol moiety, named arabidopside E. In this study, we demonstrate that the synthesis of arabidopsides is mainly independent of the prokaryotic lipid biosynthesis pathway in the chloroplast, and, in addition to what previously has been reported, arabidopside E as well as an all-OPDA analog, arabidopside G, described here accumulated during the hypersensitive response and in response to wounding. We also show that different signaling pathways lead to the formation of arabidopsides during the hypersensitive response and the wounding response, respectively. However, the formation of arabidopsides during both responses is dependent on an intact jasmonate signaling pathway. Additionally, we report inhibition of growth of the fungal necrotrophic pathogen Botrytis cinerea and in planta release of free jasmonates in a time frame that overlaps with the observed reduction of arabidopside levels. Thus, arabidopsides may have a dual function: as antipathogenic substances and as storage compounds that allow the slow release of free jasmonates.
Plant oxylipins, produced via the lipoxygenase (LOX) pathway, function as signals in defense and development. In fungi, oxylipins are potent regulators of mycotoxin biosynthesis and sporogenesis. Previous studies showed that plant 9-LOX-derived fatty acid hydroperoxides induce conidiation and mycotoxin production. Here, we tested the hypothesis that oxylipins produced by the maize 9-LOX pathway are required by pathogens to produce spores and mycotoxins and to successfully colonize the host. Maize mutants were generated in which the function of a 9-LOX gene, ZmLOX3, was abolished by an insertion of a Mutator transposon in its coding sequence, which resulted in reduced levels of several 9-LOX-derived hydroperoxides. Supporting our hypothesis, conidiation and production of the mycotoxin fumonisin B1 by Fusarium verticillioides were drastically reduced in kernels of the lox3 mutants compared with near-isogenic wild types. Similarly, conidia production and disease severity of anthracnose leaf blight caused by Colletotrichum graminicola were significantly reduced in the lox3 mutants. Moreover, lox3 mutants displayed increased resistance to southern leaf blight caused by Cochliobolus heterostrophus and stalk rots caused by both F. verticillioides and C. graminicola. These data strongly suggest that oxylipin metabolism mediated by a specific plant 9-LOX isoform is required for fungal pathogenesis, including disease development and production of spores and mycotoxins.
Ectomycorrhizas (EMs) alleviate stress tolerance of host plants, but the underlying molecular mechanisms are unknown. To elucidate the basis of EM-induced physiological changes and their involvement in stress adaptation, we investigated metabolic and transcriptional profiles in EM and non-EM roots of gray poplar (Populus 3 canescens) in the presence and absence of osmotic stress imposed by excess salinity. Colonization with the ectomycorrhizal fungus Paxillus involutus increased root cell volumes, a response associated with carbohydrate accumulation. The stress-related hormones abscisic acid and salicylic acid were increased, whereas jasmonic acid and auxin were decreased in EM compared with non-EM roots. Auxin-responsive reporter plants showed that auxin decreased in the vascular system. The phytohormone changes in EMs are in contrast to those in arbuscular mycorrhizas, suggesting that EMs and arbuscular mycorrhizas recruit different signaling pathways to influence plant stress responses. Transcriptome analyses on a whole genome poplar microarray revealed activation of genes related to abiotic and biotic stress responses as well as of genes involved in vesicle trafficking and suppression of auxin-related pathways. Comparative transcriptome analysis indicated EM-related genes whose transcript abundances were independent of salt stress and a set of salt stress-related genes that were common to EM non-salt-stressed and non-EM salt-stressed plants. Salt-exposed EM roots showed stronger accumulation of myoinositol, abscisic acid, and salicylic acid and higher K + -to-Na + ratio than stressed non-EM roots. In conclusion, EMs activated stress-related genes and signaling pathways, apparently leading to priming of pathways conferring abiotic stress tolerance.Under natural conditions, many economically important tree species including fast-growing poplars (Populus spp.) form ectomycorrhizas (EMs) between roots and EM fungi. Colonization with EM fungi leads to profound changes in root architecture and morphology. Usually, EM roots are strongly ramnified and EM root tips show a bulb-like appearance (Smith and Read, 2008). In EMs, plants and fungi interact mutualistically: while the plant receives mineral nutrients and water through the fungus, the fungus is supplied with carbohydrates by its host (Smith and Read, 2008). To fulfill these functions, specific anatomical structures are established, which involve the formation of a hyphal mantle ensheathing the root tip with hyphae emanating into soil for nutrient uptake. Inside the mantle, hyphae grow between, but not inside, the cortex cells within the cell wall, forming an interface called the Hartig net for bidirectional nutrient exchange.The establishment of EMs requires a coordinated developmental program in both partners of the symbiosis. Transcriptional changes during initial stages of host recognition and colonization have been the focus of several recent studies (Johansson et al., 2004;Duplessis et al., 2005;Le Queré et al., 2005;Morel et
The homothallic ascomycete Aspergillus nidulans serves as model organism for filamentous fungi because of its ability to propagate with both asexual and sexual life cycles, and fatty acid-derived substances regulate the balance between both cycles. These so-called psi (precocious sexual inducer) factors are produced by psi factor-producing oxygenases (Ppo enzymes). Bioinformatic analysis predicted the presence of two different heme domains in Ppo proteins: in the N-terminal region, a fatty acid heme dioxygenase/peroxidase domain is predicted, whereas in the C-terminal region, a P450 heme thiolate domain is predicted. To analyze the reaction catalyzed by Ppo enzymes, PpoA was expressed in Escherichia coli as an active enzyme. The protein was purified by 62-fold and identified as a homotetrameric ferric heme protein that metabolizes mono-as well as polyunsaturated C 16 and C 18 fatty acids at pH ϳ7.25. The presence of thiolate-ligated heme was confirmed on the basis of sequence alignments and the appearance of a characteristic 450 nm CO-binding spectrum. Studies on its reaction mechanism revealed that PpoA uses different heme domains to catalyze two separate reactions. Within the heme peroxidase domain, linoleic acid is oxidized to (8R)-hydroperoxyoctadecadienoic acid by abstracting a H-atom from C-8 of the fatty acid, yielding a carbon-centered radical that reacts with molecular dioxygen. In the second reaction step, 8-hydroperoxyoctadecadienoic acid is isomerized within the P450 heme thiolate domain to 5,8-dihydroxyoctadecadienoic acid. We identify PpoA as a bifunctional P450 fusion protein that uses a previously unknown reaction mechanism for forming psi factors.The fungus Aspergillus nidulans (teleomorph Emericella nidulans) is a homothallic ascomycete that has a defined sexual and asexual developmental cycle. Therefore, it serves as a model system for the understanding of fungal development (1). Oxidized unsaturated fatty acids, so-called oxylipins, derived from endogenous fatty acids were found to influence the development of the asexual conidiophores and sexual cleistothecia (2-6). Moreover, they seem to regulate the secondary metabolism of the fungus (7). These substances were collectively named psi factors and are primarily a mixture of hydroxylated oleic (18:1 ⌬9Z
Piriformospora indica has been shown to improve the growth of many plant species including Arabidopsis thaliana, but the mechanism by which this is achieved is still unclear. Arabidopsis root colonization by P. indica was examined in sterile culture on the medium of Murashige and Skoog. P. indica formed intracellular structures in Arabidopsis root epidermal cells and caused changes in root growth, leading to stunted and highly branched root systems. This effect was because of a diffusible factor and could be mimicked by IAA. In addition, P. indica was shown to produce IAA in liquid culture. We suggest that auxin production affecting root growth is responsible for, or at least contributes to, the beneficial effect of P. indica on its host plants.
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