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Publications - Stress and Develop Biology

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Publications

Geissler, K.; Eschen-Lippold, L.; Naumann, K.; Schneeberger, K.; Weigel, D.; Scheel, D.; Rosahl, S.; Westphal, L.; Mutations in the EDR1 Gene Alter the Response of Arabidopsis thaliana to Phytophthora infestans and the Bacterial PAMPs flg22 and elf18 Mol. Plant Microbe Interact. 28, 122-133, (2015) DOI: 10.1094/MPMI-09-14-0282-R

Mechanistically, nonhost resistance of Arabidopsis thaliana against the oomycete Phytophthora infestans is not well understood. Besides PEN2 and PEN3, which contribute to penetration resistance, no further components have been identified so far. In an ethylmethane sulphonate–mutant screen, we mutagenized pen2-1 and screened for mutants with an altered response to infection by P. infestans. One of the mutants obtained, enhanced response to Phytophthora infestans6 (erp6), was analyzed. Whole-genome sequencing of erp6 revealed a single nucleotide polymorphism in the coding region of the kinase domain of At1g08720, which encodes the putative MAPKKK ENHANCED DISEASE RESISTANCE1 (EDR1). We demonstrate that three independent lines with knock-out alleles of edr1 mount an enhanced response to P. infestans inoculation, mediated by increased salicylic acid signaling and callose deposition. Moreover, we show that the single amino acid substitution in erp6 causes the loss of in vitro autophosphorylation activity of EDR1. Furthermore, growth inhibition experiments suggest a so-far-unknown involvement of EDR1 in the response to the pathogen-associated molecular patterns flg22 and elf18. We conclude that EDR1 contributes to the defense response of A. thaliana against P. infestans. Our data position EDR1 as a negative regulator in postinvasive nonhost resistance.
Publications

Schön, M.; Töller, A.; Diezel, C.; Roth, C.; Westphal, L.; Wiermer, M.; Somssich, I. E.; Analyses of wrky18 wrky40 Plants Reveal Critical Roles of SA/EDS1 Signaling and Indole-Glucosinolate Biosynthesis for Golovinomyces orontii Resistance and a Loss-of Resistance Towards Pseudomonas syringae pv. tomato AvrRPS4 Mol. Plant Microbe Interact. 26, 758-767, (2013) DOI: 10.1094/MPMI-11-12-0265-R

Simultaneous mutation of two WRKY-type transcription factors, WRKY18 and WRKY40, renders otherwise susceptible wild-type Arabidopsis plants resistant towards the biotrophic powdery mildew fungus Golovinomyces orontii. Resistance in wrky18 wrky40 double mutant plants is accompanied by massive transcriptional reprogramming, imbalance in salicylic acid (SA) and jasmonic acid (JA) signaling, altered ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) expression, and accumulation of the phytoalexin camalexin. Genetic analyses identified SA biosynthesis and EDS1 signaling as well as biosynthesis of the indole-glucosinolate 4MI3G as essential components required for loss-of-WRKY18 WRKY40–mediated resistance towards G. orontii. The analysis of wrky18 wrky40 pad3 mutant plants impaired in camalexin biosynthesis revealed an uncoupling of pre- from postinvasive resistance against G. orontii. Comprehensive infection studies demonstrated the specificity of wrky18 wrky40–mediated G. orontii resistance. Interestingly, WRKY18 and WRKY40 act as positive regulators in effector-triggered immunity, as the wrky18 wrky40 double mutant was found to be strongly susceptible towards the bacterial pathogen Pseudomonas syringae DC3000 expressing the effector AvrRPS4 but not against other tested Pseudomonas strains. We hypothesize that G. orontii depends on the function of WRKY18 and WRKY40 to successfully infect Arabidopsis wild-type plants while, in the interaction with P. syringae AvrRPS4, they are required to mediate effector-triggered immunity.
Publications

Kirsten, S.; Navarro-Quezada, A.; Penselin, D.; Wenzel, C.; Matern, A.; Leitner, A.; Baum, T.; Seiffert, U.; Knogge, W.; Necrosis-Inducing Proteins of Rhynchosporium commune, Effectors in Quantitative Disease Resistance Mol. Plant Microbe Interact. 25, 1314-1325, (2012) DOI: 10.1094/MPMI-03-12-0065-R

The barley pathogen Rhynchosporium commune secretes necrosis-inducing proteins NIP1, NIP2, and NIP3. Expression analysis revealed that NIP1 transcripts appear to be present in fungal spores already, whereas NIP2 and NIP3 are synthesized after inoculation of host plants. To assess the contribution of the three effector proteins to disease development, deletion mutants were generated. The development of these fungal mutants on four barley cultivars was quantified in comparison with that of the parent wild-type strain and with two fungal strains failing to secrete an “active” NIP1 avirulence protein, using quantitative polymerase chain reaction as well as microscopic imaging after fungal green fluorescent protein tagging. The impact of the three deletions varied quantitatively depending on the host genotype, suggesting that the activities of the fungal effectors add up to produce stronger growth patterns and symptom development. Alternatively, recognition events of differing intensities may be converted into defense gene expression in a quantitative manner.
Publications

Eschen-Lippold, L.; Altmann, S.; Rosahl, S.; DL-β-Aminobutyric Acid–Induced Resistance of Potato Against Phytophthora infestans Requires Salicylic Acid but Not Oxylipins Mol. Plant Microbe Interact. 23, 585-592, (2010) DOI: 10.1094/MPMI-23-5-0585

Inducing systemic resistance responses in crop plants is a promising alternative way of disease management. To understand the underlying signaling events leading to induced resistance, functional analyses of plants defective in defined signaling pathway steps are required. We used potato, one of the economically most-important crop plants worldwide, to examine systemic resistance against the devastating late blight pathogen Phytophthora infestans, induced by treatment with dl-β-aminobutyric acid (BABA). Transgenic plants impaired in either the 9-lipoxygenase pathway, which produces defense-related compounds, or the 13-lipoxygenase pathway, which generates jasmonic acid–derived signals, expressed wild-type levels of BABA-induced resistance. Plants incapable of accumulating salicylic acid (SA), on the other hand, failed to mount this type of induced resistance. Consistently, treatment of these plants with the SA analog 2,6-dichloroisonicotinic acid restored BABA-induced resistance. Together, these results demonstrate the indispensability of a functional SA pathway for systemic resistance in potato induced by BABA.
Publications

Halim, V. A.; Eschen-Lippold, L.; Altmann, S.; Birschwilks, M.; Scheel, D.; Rosahl, S.; Salicylic Acid Is Important for Basal Defense of Solanum tuberosum Against Phytophthora infestans Mol. Plant Microbe Interact. 20, 1346-1352, (2007) DOI: 10.1094/MPMI-20-11-1346

The importance of the signaling compound salicylic acid for basal defense of potato (Solanum tuberosum L. cv. Désirée) against Phytophthora infestans, the causal agent of late blight disease, was assessed using transgenic NahG potato plants which are unable to accumulate salicylic acid. Although the size of lesions caused by P. infestans was not significantly different in wild-type and transgenic NahG plants, real-time polymerase chain reaction analyses revealed a drastic enhancement of pathogen growth in potato plants depleted of salicylic acid. Increased susceptibility of NahG plants correlated with compromised callose formation and reduced early defense gene expression. NahG plants pretreated with the salicylic acid analog 2,6-dichloro-isonicotinic acid allowed pathogen growth to a similar extent as did wild-type plants, indicating that salicylic acid is an important compound required for basal defense of potato against P. infestans.
Publications

Li, C.-M.; Haapalainen, M.; Lee, J.; Nürnberger, T.; Romantschuk, M.; Taira, S.; Harpin of Pseudomonas syringae pv. phaseolicola Harbors a Protein Binding Site Mol. Plant Microbe Interact. 18, 60-66, (2005) DOI: 10.1094/MPMI-18-0060

Harpin HrpZ of plant-pathogenic bacterium Pseudomonas syringae elicits a hypersensitive response (HR) in some nonhost plants, but its function in the pathogenesis process is still obscure. HrpZ-interacting proteins were identified by screening a phage-display library of random peptides. HrpZ of the bean pathogen P. syringae pv. Phaseolicola (HrpZPph) shows affinity to peptides with a consensus amino acid motif W(L)ARWLL(G/L). To localize the peptide-binding site, the hrpZPph gene was mutagenized with randomly placed 15-bp insertions, and the mutant proteins were screened for the peptide-binding ability. Mutations that inhibited peptide-binding localized to the central region of hrpZPph, which is separate from the previously determined HR-inducing region. Antiserum raised against one of the hrpZPph-binding peptides recognized small proteins in bean, tomato, parsley, and Arabidopsis thaliana but none in tobacco. On native protein blots, hrpZPph bound to a bean protein with similar pI as the protein recognized by the peptide antiserum. The result suggests a protein-protein interaction between the harpin and a host plant protein, possibly involved in the bacterial pathogenesis.
Publications

Gao, L.-L.; Knogge, W.; Delp, G.; Smith, F. A.; Smith, S. E.; Expression Patterns of Defense-Related Genes in Different Types of Arbuscular Mycorrhizal Development in Wild-Type and Mycorrhiza-Defective Mutant Tomato Mol. Plant Microbe Interact. 17, 1103-1113, (2004) DOI: 10.1094/MPMI.2004.17.10.1103

The expression of defense-related genes was analyzed in the interactions of six arbuscular mycorrhizal (AM) fungi with the roots of wild-type tomato (Lycopersicon esculentum Mill.) cv. 76R and of the near-isogenic mycorrhiza-defective mutant rmc. Depending on the fungal species, wild-type tomato forms both major morphological AM types, Arum and Paris. The mutant rmc blocks the penetration of the root surface or invasion of the root cortex by most species of AM fungi, but one fungus has been shown to develop normal mycorrhizas. In the wild-type tomato, accumulation of mRNA representing a number of defense-related genes was low in Arum-type interactions, consistent with findings for this AM morphotype in other plant species. In contrast, Paris-type colonization, particularly by members of the family Gigasporaceae, was accompanied by a substantial transient increase in expression of some defense-related genes. However, the extent of root colonization did not differ significantly in the two wild-type AM morpho-types, suggesting that accumulation of defense gene products per se does not limit mycorrhiza development. In the mutant, interactions in which the fungus failed to penetrate the root lacked significant accumulation of defense gene mRNAs. However, phenotypes in which the fungus penetrated epidermal or hypodermal cells were associated with an enhanced and more prolonged gene expression. These results are discussed in relation to the mechanisms that may underlie the specificity of the interactions between AM fungi and the rmc mutant.
Publications

Schürch, S.; Linde, C. C.; Knogge, W.; Jackson, L. F.; McDonald, B. A.; Molecular Population Genetic Analysis Differentiates Two Virulence Mechanisms of the Fungal Avirulence Gene NIP1 Mol. Plant Microbe Interact. 17, 1114-1125, (2004) DOI: 10.1094/MPMI.2004.17.10.1114

Deletion or alteration of an avirulence gene are two mechanisms that allow pathogens to escape recognition mediated by the corresponding resistance gene in the host. We studied these two mechanisms for the NIP1 avirulence gene in field populations of the fungal barley pathogen Rhynchosporium secalis. The product of the avirulence gene, NIP1, causes leaf necrosis and elicits a defense response on plants with the Rrs1 resistance gene. A high NIP1 deletion frequency (45%) was found among 614 isolates from different geographic populations on four continents. NIP1 was also sequenced for 196 isolates, to identify DNA polymorphisms and corresponding NIP1 types. Positive diversifying selection was found to act on NIP1. A total of 14 NIP1 types were found, 11 of which had not been described previously. The virulence of the NIP1 types was tested on Rrs1 and rrs1 barley lines. Isolates carrying three of these types were virulent on the Rrs1 cultivar. One type each was found in California, Western Europe, and Jordan. Additionally, a field experiment with one pair of near-isogenic lines was conducted to study the selection pressure imposed by Rrs1 on field populations of R. secalis. Deletion of NIP1 was the only mechanism used to infect the Rrs1 cultivar in the field experiment. In this first comprehensive study on the population genetics of a fungal avirulence gene, virulence to Rrs1 in R. secalis was commonly achieved through deletion of the NIP1 avirulence gene but rarely also through point mutations in NIP1.
Publications

Steiner-Lange, S.; Fischer, A.; Boettcher, A.; Rouhara, I.; Liedgens, H.; Schmelzer, E.; Knogge, W.; Differential Defense Reactions in Leaf Tissues of Barley in Response to Infection by Rhynchosporium secalis and to Treatment with a Fungal Avirulence Gene Product Mol. Plant Microbe Interact. 16, 893-902, (2003) DOI: 10.1094/MPMI.2003.16.10.893

Expression of defense-associated genes was analyzed in leaf tissues of near-isogenic resistant and susceptible barley cultivars upon infection by Rhynchosporium secalis. The genes encoding pathogenesis-related (PR) proteins PR-1, PR-5, and PR-9 are specifically expressed in the mesophyll of resistant plants, whereas a germin-like protein (OxOLP) is synthesized in the epidermis irrespective of the resistance genotype. Restriction-mediated differential display was employed to identify additional epidermis-specific genes. This resulted in the detection of another PR gene, PR-10, along with a lipoxygenase gene, LoxA, and a gene of unknown function, pI2-4, which are specifically induced in the epidermis of resistant plants. The gene encoding a putative protease inhibitor, SD10, is preferentially but not exclusively expressed in the epidermis. The fungal avirulence gene product NIP1 triggers the induction of the four PR genes only. At least two additional elicitors, therefore, must be postulated, one for the unspecific induction of OxOLP and one for the resistance-specific induction of LoxA, pI2-4, and SD10. PR-10 expression can be assumed to be the consequence of NIP1 perception by epidermis cells. In contrast, gene expression in the mesophyll is likely to be triggered by an as yet unknown signal that appears to originate in the epidermis and that is strongly amplified in the mesophyll.
Publications

Varet, A.; Parker, J.; Tornero, P.; Nass, N.; Nürnberger, T.; Dangl, J. L.; Scheel, D.; Lee, J.; NHL25 and NHL3, Two NDR1/HIN1-Like Genes in Arabidopsis thaliana with Potential Role(s) in Plant Defense Mol. Plant Microbe Interact. 15, 608-616, (2002) DOI: 10.1094/MPMI.2002.15.6.608

The Arabidopsis genome contains 28 genes with sequence homology to the Arabidopsis NDR1 gene and the tobacco HIN1 gene. Expression analysis of eight of these genes identified two (NHL25 and NHL3 for NDR1/HIN1-like) that show pathogen-dependent mRNA accumulation. Transcripts did not accumulate during infection with virulent Pseudomonas syringae pv. tomato DC3000 but did accumulate specifically when the bacteria carried any of the four avirulence genes avrRpm1, avrRpt2, avrB, or avrRps4. Furthermore, expression of avrRpt2 in plants containing the corresponding resistance gene, RPS2, was sufficient to induce transcript accumulation. However, during infection with an avirulent oomycete, Peronospora parasitica isolate Cala-2, only NHL25 expression was reproducibly induced. Salicylic acid (SA) treatment can induce expression of NHL25 and NHL3. Studies performed on nahG plants showed that, during interaction with avirulent bacteria, only the expression of NHL25 but not that of NHL3 was affected. This suggests involvement of separate SA-dependent and SA-independent pathways, respectively, in the transcriptional activation of these genes. Bacteria-induced gene expression was not abolished in ethylene- (etr1-3 and ein2-1) and jasmonate- (coi1-1) insensitive mutants or in mutants impaired in disease resistance (ndr1-1 and pad4-1). Interestingly, NHL3 transcripts accumulated after infiltration with the avirulent hrcC mutant of Pseudomonas syringae pv. tomato DC3000 and nonhost bacteria but not with the virulent Pseudomonas syringae pv. tomato DC3000, suggesting that virulent bacteria may suppress NHL3 expression during pathogenesis. Hence, the expression patterns and sequence homology to NDR1 and HIN1 suggest one or more potential roles for these genes in plant resistance.
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