Differential Expression of Eight Chitinase Genes in <i>Medicago truncatula</i> Roots During Mycorrhiza Formation, Nodulation, and Pathogen Infection

Salzer, Peter; Bonanomi, Athos; Beyer, Katinka; Vögeli‐Lange, Regina; Aeschbacher, Roger A.; Lange, J.; Wiemken, Andres; Kim, Dong-Jin; Cook, Douglas R.; Boller, Thomas

doi:10.1094/mpmi.2000.13.7.763

Cited by 163 publications

(147 citation statements)

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“…Although chitinases can be induced in pathogenic interactions (Salzer et al 2000), specific class III chitinases have been found to be up-regulated in arbuscular mycorrhizal (AM) Medicago truncatula roots, but not in interactions with pathogens (Salzer et al 2000). Predominant expression of these chitinases was in the arbuscule-containing cells (Bonanomi et al 2001;Hogekamp et al 2011), where they may play a role in suppressing plant defence by the reduction of chitin-like elicitors during the formation of functional symbiotic interfaces (Salzer et al 2000). A similar role may be envisaged in S. vomeracea mycorrhizal protocorms, but further studies are required to investigate regulation of SvChit3 by other biotic and abiotic stimuli.…”

Section: Discussionmentioning

confidence: 99%

Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship

Perotto

Rodda

Benetti

et al. 2014

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Main conclusionOrchid mycorrhiza has been often interpreted as an antagonistic relationship. Our data on mycorrhizal protocorms do not support this view as plant defence genes were not induced, whereas some nodulinlike genes were significantly up-regulated.Orchids fully depend on symbiotic interactions with specific soil fungi for seed germination and early development. Germinated seeds give rise to a protocorm, a heterotrophic organ that acquires nutrients, including organic carbon, from the mycorrhizal partner. It has long been debated if this interaction is mutualistic or antagonistic. To investigate the molecular bases of the orchid response to mycorrhizal invasion, we developed a symbiotic in vitro system between Serapias vomeracea, a Mediterranean green meadow orchid, and the rhizoctonia-like fungus Tulasnella calospora. 454 pyrosequencing was used to generate an inventory of plant and fungal genes expressed in mycorrhizal protocorms, and plant genes could be reliably identified with a customized bioinformatic pipeline. A small panel of plant genes was selected and expression was assessed by real-time quantitative PCR in mycorrhizal and non-mycorrhizal protocorm tissues. Among these genes were some markers of mutualistic (e.g. nodulins) as well as antagonistic (e.g. pathogenesis-related and wound/stress-induced) genes. None of the pathogenesis or wound/stress-related genes were significantly up-regulated in mycorrhizal tissues, suggesting that fungal colonization does not trigger strong plant defence responses. In addition, the highest expression fold change in mycorrhizal tissues was found for a nodulin-like gene similar to the plastocyanin domaincontaining ENOD55. Another nodulin-like gene significantly more expressed in the symbiotic tissues of mycorrhizal protocorms was similar to a sugar transporter of the SWEET family. Two genes coding for mannose-binding lectins were significantly up-regulated in the presence of the mycorrhizal fungus, but their role in the symbiosis is unclear.

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Section: Discussionmentioning

confidence: 99%

Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship

Perotto

Rodda

Benetti

et al. 2014

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“…Staehelin et al, 1992;Vasse et al, 1993;Mithö fer et al, 1996;Goormachtig et al, 1998;Salzer et al, 2000). The demonstration that NopL is a repressor of plant defense reactions suggests that invading rhizobia can manipulate metabolic pathways of their hosts using mechanisms that are common to pathogens.…”

Section: Table I Plant Growth and Nodule Formation Of L Japonicus Pmentioning

confidence: 99%

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

et al. 2004

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Bacterial effector proteins delivered into eukaryotic cells via bacterial type III secretion systems are important virulence factors in plant-pathogen interactions. Type III secretion systems have been found in Rhizobium species that form symbiotic, nitrogen-fixing associations with legumes. One such bacterium, Rhizobium sp. NGR234, secretes a number of type III effectors, including nodulation outer protein L (NopL, formerly y4xL). Here, we show that expression of nopL in tobacco (Nicotiana tabacum) prevents full induction of pathogenesis-related (PR) defense proteins. Transgenic tobacco plants that express nopL and were infected with potato virus Y (necrotic strain 605) exhibited only very low levels of chitinase (class I) and ␤-1,3-glucanase (classes I and III) proteins. Northern-blot analysis indicated that expression of nopL in plant cells suppresses transcription of PR genes. Treatment with ethylene counteracted the effect of NopL on chitinase (class I). Transgenic Lotus japonicus plants that expressed nopL exhibited delayed development and low chitinase levels. In vitro experiments showed that NopL is a substrate for plant protein kinases. Together, these data suggest that NopL, when delivered into the plant cell, modulates the activity of signal transduction pathways that culminate in activation of PR proteins.Plants have evolved many defenses against invading pathogens. Among them are preformed antimicrobial compounds, as well as inducible defense proteins, the so-called pathogenesis-related (PR) proteins (van Loon, 1997). It has been shown, for example, that pathogen-induced chitinases (EC 3.2.1.14) and ␤-1,3-glucanases (EC 3.2.1.39) synergistically lyse fungal cell walls (Mauch et al., 1988). Specific recognition of pathogens often induces a hypersensitive response, which is characterized by an oxidative burst and localized death of the host cells. In most cases, the induction of a hypersensitive response arrests invasion by the pathogen (Dangl and Jones, 2001).Virulence in gram-negative bacteria often depends on proteins injected into eukaryotic cells. Some bacteria elaborate a specialized protein secretion apparatus, the type III secretion system (TTSS). The TTSS exports a set of proteins from the bacteria, some of which are delivered directly into the eukaryotic cells-a process called translocation (Cornelis and van Gijsegem, 2000;Plano et al., 2001). Most translocated type III effectors act on the cytoskeleton or interfere with intracellular signaling cascades of the host cell. Yersinia pestis, for example, injects at least six type III effectors into host cells, where they thwart the signaling machinery of the immune system (Cornelis, 2002). Plant pathogens such as Pseudomonas syringae and Xanthomonas campestris also use TTSSs (Kjemtrup et al., 2000; Lahaye and Bonas, 2001). Mounting evidence suggests that type III effectors translocated into plant cells (Casper-Lindley et al., 2002;Szurek et al., 2002) act as virulence factors in susceptible hosts. One likely function of type III effectors is ...

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“…Transcripts of the class IV chitinase gene, Mtchit 4, continuously accumulated in the interaction of M. truncatula Jemalong A17 with S. meliloti 1021. In our previous work (Salzer et al 2000), however, we were not able to identify a chitinase gene that is specifically induced during interactions with S. meliloti. In order to learn more about chitinase gene expression during nodule formation and about the effects of rhizobial signal molecules, we extended our studies on the M. truncatula ecotype R108-1.…”

Section: Introductionmentioning

confidence: 67%

“…Culture and inoculation with the AM fungus Glomus intraradices was performed as previously described (Salzer et al 2000) with about 400 spores, which had been isolated from Daucus carota/Glomus intraradices in vitro cultures (Be´card and Fortin 1988). In control experiments, an equivalent amount of water was added.…”

Section: Treatments and Culture Of Plants Bacteria And Fungimentioning

confidence: 99%

“…The ecotype R108-1 is known for its superior in vitro regeneration and transformation properties (Hoffmann et al 1997). In our previous work we isolated partial chitinase DNA sequences from an M. truncatula bacterial artificial chromosome (BAC) library and determined transcript levels by semi-quantitative reverse transcription-polymerase chain reaction (RT-PCR) in various pathogenic and symbiotic interactions (Salzer et al 2000). Transcripts of the class IV chitinase gene, Mtchit 4, continuously accumulated in the interaction of M. truncatula Jemalong A17 with S. meliloti 1021.…”

Section: Introductionmentioning

confidence: 99%

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Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108-1: a comparison between symbiosis-specific class�V and defence-related class�IV chitinases

Salzer

Feddermann

Wiemken

et al. 2004

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The Medicago truncatula (Gaertn.) ecotypes Jemalong A17 and R108-1 differ in Sinorhizobium meliloti-induced chitinase gene expression. The pathogen-inducible class IV chitinase gene, Mtchit 4, was strongly induced during nodule formation of the ecotype Jemalong A17 with the S. meliloti wild-type strain 1021. In the ecotype R108-1, the S. meliloti wild types Sm1021 and Sm41 did not induce Mtchit 4 expression. On the other hand, expression of the putative class V chitinase gene, Mtchit 5, was found in roots of M. truncatula cv. R108-1 nodulated with either of the rhizobial strains. Mtchit 5 expression was specific for interactions with rhizobia. It was not induced in response to fungal pathogen attack, and not induced in roots colonized with arbuscular mycorrhizal (AM) fungi. Elevated Mtchit 5 gene expression was first detectable in roots forming nodule primordia. In contrast to Mtchit 4, expression of Mtchit 5 was stimulated by purified Nod factors. Conversely, Mtchit 4 expression was strongly elevated in nodules formed with the K-antigen-deficient mutant PP699. Expression levels of Mtchit 5 were similarly increased in nodules formed with PP699 and its parental wild-type strain Sm41. Phylogenetic analysis of the deduced amino acid sequences of Mtchit 5 (calculated molecular weight = 41,810 Da, isoelectric point pH 7.7) and Mtchit 4 (calculated molecular weight 30,527 Da, isoelectric point pH 4.9) revealed that the putative Mtchit 5 chitinase forms a separate clade within class V chitinases of plants, whereas the Mtchit 4 chitinase clusters with pathogen-induced class IV chitinases from other plants. These findings demonstrate that: (i) Rhizobium-induced chitinase gene expression in M. truncatula occurs in a plant ecotype-specific manner, (ii) Mtchit 5 is a putative chitinase gene that is specifically induced by rhizobia, and (iii) rhizobia-specific and defence-related chitinase genes are differentially influenced by rhizobial Nod factors and K antigens.Keywords Class IV and V chitinase AE K antigen AE Medicago truncatula ecotypes R108-1 and Jemalong A17 AE Nod factors AE Sinorhizobium AE Suppression of plant defence

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Differential Expression of Eight Chitinase Genes in Medicago truncatula Roots During Mycorrhiza Formation, Nodulation, and Pathogen Infection

Cited by 163 publications

References 76 publications

Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship

Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108-1: a comparison between symbiosis-specific class�V and defence-related class�IV chitinases

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