In Arabidopsis, systemic acquired resistance against pathogens has been associated with the accumulation of salicylic acid (SA) and the expression of the pathogenesis-related proteins PR-1, PR-2, and PR-5. We report here the isolation of two nonallelic mutants impaired in the pathway leading to SA biosynthesis. These SA induction-deficient ( sid ) mutants do not accumulate SA after pathogen inoculation and are more susceptible to both virulent and avirulent forms of Pseudomonas syringae and Peronospora parasitica. However, sid mutants are not as susceptible to these pathogens as are transgenic plants expressing the nahG gene encoding an SA hydroxylase that degrades SA to catechol. In contrast to NahG plants, only the expression of PR-1 is strongly reduced in sid mutants, whereas PR-2 and PR-5 are still expressed after pathogen attack. Furthermore, the accumulation of the phytoalexin camalexin is normal. These results indicate that SA-independent compensation pathways that do not operate in NahG plants are active in sid mutants. One of the mutants is allelic to eds5 (for enhanced disease susceptibility), whereas the other mutant has not been described previously. INTRODUCTIONInfection with necrotizing pathogens often leads to the subsequent systemic induction of resistance. This is referred to as systemic acquired resistance (SAR), which is characterized by a long-lasting defense response against a broad spectrum of pathogens (Kuc, 1982;Ryals et al., 1994;Sticher et al., 1997). After the initial observation that treatment of plants with salicylic acid (SA) leads to resistance (White, 1979), several lines of evidence have shown that SA is associated with SAR. The expression of a number of pathogenesis-related (PR) proteins is highly correlated with acquired resistance Uknes et al., 1992). The synthesis of PR proteins can be induced by treatment with SA and also by the application of functional analogs of SA, such as 2,6-dichloroisonicotinic acid (INA;Métraux et al., 1991) or benzo(1,2,3)thiadiazole-7-carbothioic acid S -methyl ester (BTH; Görlach et al., 1996).The accumulation of SA in plant tissues correlates with the presence of PR proteins and resistance (Malamy et al., 1990;Métraux et al., 1990;Yalpani et al., 1991). In addition, transgenic tobacco (Gaffney et al., 1993) and Arabidopsis plants that express the Pseudomonas putida nahG gene, encoding an SA hydroxylase, which degrades SA to catechol, are hypersusceptible to infection with virulent pathogens and cannot develop SAR. Experiments with NahG plants also showed that SA is involved in gene-for-gene defense responses . These findings provide strong evidence for the involvement of SA in SAR.SA also has been proposed to be the systemic signal for SAR (Malamy et al., 1990;Métraux et al., 1990). However, although SA synthesized in infected leaves can be shown to be transported to uninfected leaves in tobacco and cucumber (Shulaev et al., 1995;Mölders et al., 1996), grafting experiments with tobacco plants expressing NahG, cholera toxin, or reduced levels of ...
Plant roots forage the soil for minerals whose concentrations can be orders of magnitude away from those required for plant cell function. Selective uptake in multicellular organisms critically requires epithelia with extracellular diffusion barriers. In plants, such a barrier is provided by the endodermis and its Casparian strips--cell wall impregnations analogous to animal tight and adherens junctions. Interestingly, the endodermis undergoes secondary differentiation, becoming coated with hydrophobic suberin, presumably switching from an actively absorbing to a protective epithelium. Here, we show that suberization responds to a wide range of nutrient stresses, mediated by the stress hormones abscisic acid and ethylene. We reveal a striking ability of the root to not only regulate synthesis of suberin, but also selectively degrade it in response to ethylene. Finally, we demonstrate that changes in suberization constitute physiologically relevant, adaptive responses, pointing to a pivotal role of the endodermal membrane in nutrient homeostasis.
The eds5 mutant of Arabidopsis (earlier named sid1 ) was shown previously to accumulate very little salicylic acid and PR-1 transcript after pathogen inoculation and to be hypersusceptible to pathogens. We have isolated EDS5 by positional cloning and show that it encodes a protein with a predicted series of nine to 11 membrane-spanning domains and a coil domain at the N terminus. EDS5 is homologous with members of the MATE (multidrug and toxin extrusion) transporter family. EDS5 expression is very low in unstressed plants and strongly induced by pathogens and UV-C light. The transcript starts to accumulate 2 hr after inoculation of Arabidopsis with an avirulent strain of Pseudomonas syringae or UV-C light exposure, and it stays induced for ف 2 days. EDS5 also is expressed after treatments with salicylic acid, indicating a possible positive feedback regulation. EDS5 expression after infection by certain pathogens as well as after UV-C light exposure depends on the pathogen response proteins EDS1, PAD4, and NDR1, indicating that the signal transduction pathways after UV-C light exposure and pathogen inoculation share common elements. INTRODUCTIONPlants react to an attack by phytopathogenic microorganisms with an array of inducible defense responses. Whether a plant is resistant or susceptible to a potential pathogen depends largely on how fast a pathogen is recognized and defense responses are activated. For instance, in gene-forgene resistance, the product of an avirulence gene of the pathogen is recognized by a corresponding resistance gene product of the plant, leading to the rapid activation of various defense responses. Such a pathogen is avirulent to the plant, its invasion can be stopped, and the plant is resistant. Disease ensues when the pathogen is not recognized rapidly and defense mechanisms are activated too slowly to stop the infection process. In this case, the pathogen is virulent and the plant is susceptible. In addition, defense responses can be induced systemically in all parts of the plant by pathogens, soil-borne microorganisms, chemicals, or certain forms of stress. This form of induced resistance is referred to as systemic acquired resistance Sticher et al., 1997).Salicylic acid (SA) is synthesized after inoculation of plants with pathogens or exposure to certain abiotic stresses, such as ozone and UV-C light. SA was found to be essential for gene-for-gene resistance, systemic acquired resistance, and reduction of disease development after inoculation with virulent pathogens (Delaney et al., 1994;Nawrath and Métraux, 1999).In Arabidopsis, the elucidation of the signal transduction pathway downstream of SA leading to the expression of a number of pathogenesis-related (PR) proteins, such as PR-1 , PR-2 , and PR-5 , has been centered on the characterization of the npr1/nim1 mutant (Cao et al., 1994;Delaney et al., 1995). The npr1/nim1 mutant does not express PR-1 , PR-2 , and PR-5 after treatment with SA analogs, such as isonicotinic acid (Cao et al., 1994;Delaney et al., 1995). However, when...
Casparian strips are ring-like cell-wall modifications in the root endodermis of vascular plants. Their presence generates a paracellular barrier, analogous to animal tight junctions, that is thought to be crucial for selective nutrient uptake, exclusion of pathogens, and many other processes. Despite their importance, the chemical nature of Casparian strips has remained a matter of debate, confounding further molecular analysis. Suberin, lignin, lignin-like polymers, or both, have been claimed to make up Casparian strips. Here we show that, in Arabidopsis, suberin is produced much too late to take part in Casparian strip formation. In addition, we have generated plants devoid of any detectable suberin, which still establish functional Casparian strips. In contrast, manipulating lignin biosynthesis abrogates Casparian strip formation. Finally, monolignol feeding and lignin-specific chemical analysis indicates the presence of archetypal lignin in Casparian strips. Our findings establish the chemical nature of the primary root-diffusion barrier in Arabidopsis and enable a mechanistic dissection of the formation of Casparian strips, which are an independent way of generating tight junctions in eukaryotes.root development | plant nutrition | polarized epithelium
In Arabidopsis, systemic acquired resistance against pathogens has been associated with the accumulation of salicylic acid (SA) and the expression of the pathogenesis-related proteins PR-1, PR-2, and PR-5. We report here the isolation of two nonallelic mutants impaired in the pathway leading to SA biosynthesis. These SA induction-deficient ( sid ) mutants do not accumulate SA after pathogen inoculation and are more susceptible to both virulent and avirulent forms of Pseudomonas syringae and Peronospora parasitica. However, sid mutants are not as susceptible to these pathogens as are transgenic plants expressing the nahG gene encoding an SA hydroxylase that degrades SA to catechol. In contrast to NahG plants, only the expression of PR-1 is strongly reduced in sid mutants, whereas PR-2 and PR-5 are still expressed after pathogen attack. Furthermore, the accumulation of the phytoalexin camalexin is normal. These results indicate that SA-independent compensation pathways that do not operate in NahG plants are active in sid mutants. One of the mutants is allelic to eds5 (for enhanced disease susceptibility), whereas the other mutant has not been described previously.
Cutinized and suberized cell walls form physiological important plant-environment interfaces as they act as barriers limiting water and nutrient loss and protect from radiation and invasion by pathogens. Due to the lack of protocols for the isolation and analysis of cutin and suberin in Arabidopsis, the model plant for molecular biology, mutants and transgenic plants with a defined altered cutin or suberin composition are unavailable, causing that structure and function of these apoplastic barriers are still poorly understood. Transmission electron microscopy (TEM) revealed that Arabidopsis leaf cuticle thickness ranges from only 22 nm in leaf blades to 45 nm on petioles, causing the difficulty in cuticular membrane isolation. We report the use of polysaccharide hydrolases to isolate Arabidopsis cuticular membranes, suitable for depolymerization and subsequent compositional analysis. Although cutin characteristic xhydroxy acids (7%) and mid-chain hydroxylated fatty acids (8%) were detected, the discovery of a,x-diacids (40%) and 2-hydroxy acids (14%) as major depolymerization products reveals a so far novel monomer composition in Arabidopsis cutin, but with chemical analogy to root suberin. Histochemical and TEM analysis revealed that suberin depositions were localized to the cell walls in the endodermis of primary roots and the periderm of mature roots of Arabidopsis. Enzyme digested and solvent extracted root cell walls when subjected to suberin depolymerization conditions released x-hydroxy acids (43%) and a,x-diacids (24%) as major components together with carboxylic acids (9%), alcohols (6%) and 2-hydroxyacids (0.1%). This similarity to suberin of other species indicates that Arabidopsis roots can serve as a model for suberized tissue in general.
SummaryThe signal transduction network controlling plant responses to pathogens includes pathways requiring the signal molecules salicylic acid (SA), jasmonic acid (JA), and ethylene (ET). The network topology was explored using global expression phenotyping of wild-type and signaling-defective mutant plants, including eds3, eds4, eds5, eds8, pad1, pad2, pad4, NahG, npr1, sid2, ein2, and coi1. Hierarchical clustering was used to de®ne groups of mutations with similar effects on gene expression and groups of similarly regulated genes. Mutations affecting SA signaling formed two groups: one comprised of eds4, eds5, sid2, and npr1-3 affecting only SA signaling; and the other comprised of pad2, eds3, npr1-1, pad4, and NahG affecting SA signaling as well as another unknown process. Major differences between the expression patterns in NahG and the SA biosynthetic mutant sid2 suggest that NahG has pleiotropic effects beyond elimination of SA. A third group of mutants comprised of eds8, pad1, ein2, and coi1 affected ethylene and jasmonate signaling. Expression patterns of some genes revealed mutual inhibition between SA-and JA-dependent signaling, while other genes required JA and ET signaling as well as the unknown signaling process for full expression. Global expression phenotype similarities among mutants suggested, and experiments con®rmed, that EDS3 affects SA signaling while EDS8 and PAD1 affect JA signaling. This work allowed modeling of network topology, de®nition of co-regulated genes, and placement of previously uncharacterized regulatory genes in the network.
The plant cuticle composed of cutin, a lipid-derived polyester, and cuticular waxes covers the aerial portions of plants and constitutes a hydrophobic extracellular matrix layer that protects plants against environmental stresses. The botrytis-resistant 1 (bre1) mutant of Arabidopsis reveals that a permeable cuticle does not facilitate the entry of fungal pathogens in general, but surprisingly causes an arrest of invasion by Botrytis. BRE1 was identified to be long-chain acyl-CoA synthetase2 (LACS2) that has previously been shown to be involved in cuticle development and was here found to be essential for cutin biosynthesis. bre1/lacs2 has a five-fold reduction in dicarboxylic acids, the typical monomers of Arabidopsis cutin. Comparison of bre1/lacs2 with the mutants lacerata and hothead revealed that an increased permeability of the cuticle facilitates perception of putative elicitors in potato dextrose broth, leading to the presence of antifungal compound(s) at the surface of Arabidopsis plants that confer resistance to Botrytis and Sclerotinia. Arabidopsis plants with a permeable cuticle have thus an altered perception of their environment and change their physiology accordingly.
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