Rhizobitoxine modulates plant–microbe interactions by ethylene inhibition

Sugawara, Masayuki; Okazaki, Shin; Nukui, Noriyuki; Ezura, Hiroshi; Mitsui, Hisayuki; Minamisawa, Kiwamu

doi:10.1016/j.biotechadv.2006.01.004

Cited by 87 publications

(53 citation statements)

References 58 publications

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“…Rhizobitoxine inhibits 1-aminocyclopropane-1-carboxylic acid synthase, a rate-limiting step in legume ethylene biosynthesis (Yasuta et al 1999). Ethylene is a negative regulator of nodulation in many legumes (Sugawara et al 2006), and Rtxproducing rhizobia have been shown to increase the total number of nodules that legumes form (Duodu et al 1999;Okazaki et al 2003;Yuhashi et al 2000). However, causing plants to form additional nodules will increase the relative fitness of the Rtx(+) strain only if Rtx(+) rhizobia preferentially occupy these additional nodules.…”

Section: Discussionmentioning

confidence: 99%

Measuring the fitness of symbiotic rhizobia

2011

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The legume-rhizobia symbiosis is an important model system for research on the evolution of cooperation and conflict. A key strength of this system is that the fitness consequences of greater or lesser investment in cooperative behaviors can be measured for each partner. Most empirical studies have characterized the fitness of symbiotic rhizobia exclusively by their numbers within nodules, often estimated using nodule size as a proxy. Here we show that the relationship between nodule size and rhizobial numbers can differ drastically between strains of the same species. We further show that differences in accumulation of the storage polyester poly-3-hydroxybutyrate (PHB), which can support future reproduction, can be large enough that even direct measurements of rhizobial numbers alone can lead to qualitatively incorrect conclusions. Both results come from a comparison of strains differing in production of the ethylene-inhibitor rhizobitoxine (Rtx). A broader study (using three legume-rhizobia species pairs) showed that PHB/cell cannot be reliably estimated from its correlation with rhizobia/nodule or nodule size. Differences in PHB between strains or treatments will not always make major contributions to differences in fitness, but situation-specific data are needed before PHB can safely be neglected.

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Section: Discussionmentioning

confidence: 99%

Measuring the fitness of symbiotic rhizobia

2011

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“…The host legumes have several mechanisms for regulating nodule formation (28,36). The plant hormone ethylene is also known to have inhibitory effects on rhizobial infection and the formation of nodule primordia and to limit nodule number (21,24,31). Rhizobia often interfere with ethylene biosynthesis in the host plants by means of rhizobitoxine (25,37,38) or 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase (19,33) and reduce host ethylene emission to overcome the negative regulation.…”

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Expression of the 1-Aminocyclopropane-1-Carboxylic Acid Deaminase Gene Requires Symbiotic Nitrogen-Fixing Regulator GenenifA2inMesorhizobium lotiMAFF303099

Nukui

Minamisawa

Ayabe

et al. 2006

Appl Environ Microbiol

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Many soil bacteria contain 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, which degrades ACC, a precursor of the phytohormone ethylene. In order to examine the regulation of the acdS gene encoding ACC deaminase in Mesorhizobium loti MAFF303099 during symbiosis with the host legume Lotus japonicus, we introduced the ␤-glucuronidase (GUS) gene into acdS so that GUS was expressed under control of the acdS promoter, and we also generated disruption mutants with mutations in a nitrogen fixation regulator gene, nifA. The histochemical GUS assay showed that there was exclusive expression of acdS in mature root nodules. Two homologous nifA genes, mll5857 and mll5837, were found in the symbiosis island of M. loti and were designated nifA1 and nifA2, respectively. Quantitative reverse transcription-PCR demonstrated that nifA2 disruption resulted in considerably diminished expression of acdS, nifH, and nifA1 in bacteroid cells. In contrast, nifA1 disruption slightly enhanced expression of the acdS transcripts and suppressed nifH to some extent. These results indicate that the acdS gene and other symbiotic genes are positively regulated by the NifA2 protein, but not by the NifA1 protein, in M. loti. The mode of gene expression suggests that M. loti acdS participates in the establishment and/or maintenance of mature nodules by interfering with the production of ethylene, which induces negative regulation of nodulation.The formation of nitrogen-fixing root nodules is the result of a series of interactions between (Brady)rhizobium and its legume host plants (8). The host legumes have several mechanisms for regulating nodule formation (28, 36). The plant hormone ethylene is also known to have inhibitory effects on rhizobial infection and the formation of nodule primordia and to limit nodule number (21,24,31). Rhizobia often interfere with ethylene biosynthesis in the host plants by means of rhizobitoxine (25, 37, 38) or 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase (19,33) and reduce host ethylene emission to overcome the negative regulation.ACC deaminase (EC 4.1.99.4) catalyzes the degradation of an ethylene precursor, ACC, into ammonium and ␣-ketobutyrate (13). The ACC deaminase structural gene (acdS) has been found in many rhizosphere bacteria (10, 13), including fast-and slow-growing rhizobia such as Rhizobium leguminosarum bv. viciae 128C53K (19), Bradyrhizobium japonicum USDA110 (16), Mesorhizobium loti MAFF303099 (15), and M. loti R7A (32). In the rhizobacterium Enterobacter cloacae UW4, promoter analysis of the acdS gene showed that expression of this gene requires both ACC and a leucine-responsive regulatory protein (LRP)-like protein and that anaerobic conditions enhance the expression (10). In B. japonicum USDA110 and R. leguminosarum bv. viciae 128C53K, the acdS genes are also probably regulated by an LRP-like protein and a 70 promoter (16,19).In M. loti MAFF303099, acdS was found in the symbiosis island (15). The enhancing effect of the acdS gene on nodulation of Lotus japonicus MG-20 Miyakojima roo...

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“…Several phage-encoded proteins and toxin-antitoxin systems were also identified, adding to the long list already reported for S. meliloti (Bodogai et al 2006; Sharma et al 2008). We also found sequences displaying identity to genes involved in the biosynthesis of rhizobitoxine (RtxA), a bacterial peptide that enhances host legume nodulation by inhibiting ethylene synthesis (Sugawara et al 2006). Furthermore, proteins putatively involved in plasmid segregation (RepA and RepB, encoded by the accessory plasmid pSmeSM11a in S. meliloti SM11; Stiens et al 2006) and conjugative transfer (VirB9-like protein and TraG) were partially sequenced.…”

Section: Resultsmentioning

confidence: 98%

Genomic characterization of Sinorhizobium meliloti AK21, a wild isolate from the Aral Sea Region

et al. 2015

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The symbiotic, nitrogen-fixing bacterium Sinorhizobium meliloti has been widely studied due to its ability to improve crop yields through direct interactions with leguminous plants. S. meliloti AK21 is a wild type strain that forms nodules on Medicago plants in saline and drought conditions in the Aral Sea Region. The aim of this work was to establish the genetic similarities and differences between S. meliloti AK21 and the reference strain S. meliloti 1021. Comparative genome hybridization with the model reference strain S. meliloti 1021 yielded 365 variable genes, grouped into 11 regions in the three main replicons in S. meliloti AK21. The most extensive regions of variability were found in the symbiotic plasmid pSymA, which also contained the largest number of orthologous and polymorphic sequences identified by suppression subtractive hybridization. This procedure identified a large number of divergent sequences and others without homology in the databases, the further investigation of which could provide new insight into the alternative metabolic pathways present in S. meliloti AK21. We identified a plasmid replication module from the repABC replicon family, together with plasmid mobilization-related genes (traG and a VirB9-like protein), which suggest that this indigenous isolate harbors an accessory plasmid. Furthermore, the transcriptomic profiles reflected differences in gene content and regulation between S. meliloti AK21 and S. meliloti 1021 (ExpR and PhoB regulons), but provided evidence for an as yet unknown, alternative mechanism involving activation of the cbb3 terminal oxidase. Finally, phenotypic microarrays characterization revealed a greater versatility of substrate use and chemical degradation than for S. meliloti 1021.Electronic supplementary materialThe online version of this article (doi:10.1186/s40064-015-1062-z) contains supplementary material, which is available to authorized users.

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Rhizobitoxine modulates plant–microbe interactions by ethylene inhibition

Cited by 87 publications

References 58 publications

Measuring the fitness of symbiotic rhizobia

Measuring the fitness of symbiotic rhizobia

Expression of the 1-Aminocyclopropane-1-Carboxylic Acid Deaminase Gene Requires Symbiotic Nitrogen-Fixing Regulator GenenifA2inMesorhizobium lotiMAFF303099

Genomic characterization of Sinorhizobium meliloti AK21, a wild isolate from the Aral Sea Region

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