Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa

Mitsui, Hisayuki; Sato, T; Sato, Yukari; Ito, Naofumi; Minamisawa, Kiwamu

doi:10.1007/s00438-004-0992-x

Cited by 55 publications

(107 citation statements)

References 35 publications

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“…These data suggest that, even at sublethal levels, NCR247-peptide treatment activates a cytoplasmic stress response in S. meliloti cells. This finding is particularly intriguing because it could explain why S. meliloti rpoH1 mutants die soon after being internalized within plant cells that express NCR peptides (27,28). Collectively, our data strongly suggest that cationic NCR peptides exert their effects by targeting the S. meliloti cell envelope, periplasm, and cytoplasm and suggest mechanisms through which S. meliloti adapts to NCR peptide-mediated stress in vitro and during symbiosis.…”

Section: Discussionmentioning

confidence: 68%

“…Genes specifically induced by NCR247 include genes involved in glycogen metabolism (glgA1, glgC, and glgX1), potassium transport (kdpA-C), global stress responses (fecI and rpoH1), and hypothetical genes. The effect on rpoH1 expression is particularly notable, because RpoH1 is required for bacteroid differentiation and survival in host legumes that produce cationic NCR peptides (27,28). RpoH1 regulates a suite of genes during heat and pH stress (29, 30), and we found that a subset of RpoH1-dependent genes was induced in NCR247-treated cells (Dataset S1).…”

Section: Ncr247-peptide Treatment Affects the Expression Of Genes Andmentioning

confidence: 88%

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Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

139

142

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The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called "nodule-specific cysteine-rich" (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.rhizobia-legume | host-microbe interactions

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Section: Discussionmentioning

confidence: 68%

Section: Ncr247-peptide Treatment Affects the Expression Of Genes Andmentioning

confidence: 88%

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

139

142

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“…Mutants that are defective in global bacterial transcriptional responses under stress conditions are also defective in symbiosis. A mutant in rpoH1, encoding a putative σ 32 -factor that is predicted to interact with bacterial RNA polymerase, appears to invade normally, but forms bacteroids that senesce prematurely 86 . By contrast, a mutant in relA is defective at multiple stages in nodule formation 87 ; relA mutants lack the stringent response -a bacterial transcriptional response to starvation 87 .…”

Section: Box 3 Host Invasion Parallels Between Rhizobia and Animal Pamentioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).The recent completion of the Sinorhizobium meliloti genome sequence, and the progress towards the completion of the Medicago truncatula genome sequence, have led to a surge in the molecular characterization of the determinants that are involved in the development of the symbiosis between rhizobial bacteria and leguminous plants. Aromatic compounds from legumes called flavonoids first signal the rhizobial bacteria to produce lipochitooligosaccharide compounds called Nod factors 1 . Nod factors that are secreted by the bacteria activate multiple responses in the host plant that prepare the plant to receive the invading bacteria. Nod factors and symbiotic exopolysaccharides induce the plant to form infection threads, which are thin tubules filled with bacteria that penetrate into the plant cortical tissue and deliver the bacteria to their target cells. Plant cells in the inner cortex internalize the invading bacteria in host-membrane-bound compartments that mature into structures known Correspondence to G.C.W. gwalker@mit.edu. Competing interests statementThe authors declare no competing financial interests. DATABASES Invasion of plant rootsAlthough plant roots are exposed to various micro-organisms in the soil, their cell walls form a strong protective barrier against most harmful species. The early steps in the invasion of barrel medic (M. truncatula) and alfalfa (Medicago sativa) roots by S. meliloti are characterized by the reciprocal exchange of signals that allow the bacteria to use the plant root hair cells as a means of entry. Initial signal exchangeFlavonoid compounds (2-phenyl-1,4-benzopyrone derivatives) produced by leguminous plants are the first signals to be exchanged by host-rhizobial symbiont pairs 1 (FIG. 1). Flavonoids bind bacterial NodD proteins, which are members of the LysR family of transcriptional regulators, and activate these proteins to induce the transcription of rhizobial genes 1,2 . For example, the M. sativa-derived flavonoid luteolin stimulates binding of an active form of NodD1 to an S. meliloti 'nod-box' p...

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“…One possibility is that the genes may be differentially regulated to provide GroEL/GroES at different times or at different levels. Such regulation has been observed in a number of species (5,12,16,25,26,30,41). A second possibility is that the genes may encode proteins with different substrate specificities.…”

mentioning

confidence: 96%

“…All of the single S. meliloti groEL mutants are viable (5,30,34,35), but groEL1 and groEL2 cannot be disrupted at the same time (34). The effect of groE mutations on growth rate has been determined only for the groEL1 mutant, which has a longer doubling time at 30°C than the wild type (27,35).…”

mentioning

confidence: 99%

Only One of Five groEL Genes Is Required for Viability and Successful Symbiosis in Sinorhizobium meliloti

2007

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Many bacterial species contain multiple copies of the genes that encode the chaperone GroEL and its cochaperone, GroES, including all of the fully sequenced root-nodulating bacteria that interact symbiotically with legumes to generate fixed nitrogen. In particular, in Sinorhizobium meliloti there are four groESL operons and one groEL gene. To uncover functional redundancies of these genes during growth and symbiosis, we attempted to construct strains containing all combinations of groEL mutations. Although a double groEL1 groEL2 mutant cannot be constructed, we demonstrate that the quadruple groEL1 groESL3 groEL4 groESL5 and groEL2 groESL3 groEL4 groESL5 mutants are viable. Therefore, like E. coli and other species, S. meliloti requires only one groEL gene for viability, and either groEL1 or groEL2 will suffice. The groEL1 groESL5 double mutant is more severely affected for growth at both 30°C and 40°C than the single mutants, suggesting overlapping functions in stress response. During symbiosis the quadruple groEL2 groESL3 groEL4 groESL5 mutant acts like the wild type, but the quadruple groEL1 groESL3 groEL4 groESL5 mutant acts like the groEL1 single mutant, which cannot fully induce nod gene expression and forms ineffective nodules. Therefore, the only groEL gene required for symbiosis is groEL1. However, we show that the other groE genes are expressed in the nodule at lower levels, suggesting minor roles during symbiosis. Combining our data with other data, we conclude that groESL1 encodes the housekeeping GroEL/GroES chaperone and that groESL5 is specialized for stress response.

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Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa

Cited by 55 publications

References 35 publications

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

Only One of Five groEL Genes Is Required for Viability and Successful Symbiosis in Sinorhizobium meliloti

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