Lifestyle adaptations of<i>Rhizobium</i>from rhizosphere to symbiosis

Wheatley, Rachel M.; Ford, Brandon; Li, Li; Aroney, Samuel T N; Knights, Hayley E.; Ledermann, Raphael; East, Alison K.; Ramachandran, Vinoy K.; Poole, Philip S.

doi:10.1073/pnas.2009094117

Cited by 93 publications

(113 citation statements)

References 86 publications

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“…It is hard to imagine how the loss of motility per se could enhance root colonization. However, bacterial flagella can be recognized by specific receptors in plant cell membranes and activate a cascade of immune responses controlling bacterial infection (59)(60)(61). Transcriptome analysis of SmR1 attached to wheat roots showed that the flagellar gene cluster was downregulated, suggesting that the bacteria might switch to a twitching type of motility mediated by type IV pili (62).…”

Section: Discussionmentioning

confidence: 99%

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

Amaral

Tuleski

Pankievicz

et al. 2020

mBio

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The plant rhizosphere harbors a diverse population of microorganisms, including beneficial plant growth-promoting bacteria (PGPB), that colonize plant roots and enhance growth and productivity. In order to specifically define bacterial traits that contribute to this beneficial interaction, we used high-throughput transposon mutagenesis sequencing (TnSeq) in two model root-bacterium systems associated with Setaria viridis: Azoarcus olearius DQS4T and Herbaspirillum seropedicae SmR1. This approach identified ∼100 significant genes for each bacterium that appeared to confer a competitive advantage for root colonization. Most of the genes identified specifically in A. olearius encoded metabolism functions, whereas genes identified in H. seropedicae were motility related, suggesting that each strain requires unique functions for competitive root colonization. Genes were experimentally validated by site-directed mutagenesis, followed by inoculation of the mutated bacteria onto S. viridis roots individually, as well as in competition with the wild-type strain. The results identify key bacterial functions involved in iron uptake, polyhydroxybutyrate metabolism, and regulation of aromatic metabolism as important for root colonization. The hope is that by improving our understanding of the molecular mechanisms used by PGPB to colonize plants, we can increase the adoption of these bacteria in agriculture to improve the sustainability of modern cropping systems.IMPORTANCE There is growing interest in the use of associative, plant growth-promoting bacteria (PGPB) as biofertilizers to serve as a sustainable alternative for agriculture application. While a variety of mechanisms have been proposed to explain bacterial plant growth promotion, the molecular details of this process remain unclear. The current research supports the idea that PGPB use in agriculture will be promoted by gaining more knowledge as to how these bacteria colonize plants, promote growth, and do so consistently. Specifically, the research seeks to identify those bacterial genes involved in the ability of two, PGPB strains, Azoarcus olearius and Herbaspirillum seropedicae, to colonize the roots of the C4 model grass Setaria viridis. Applying a transposon mutagenesis (TnSeq) approach, we assigned phenotypes and function to genes that affect bacterial competitiveness during root colonization. The results suggest that each bacterial strain requires unique functions for root colonization but also suggests that a few, critical functions are needed by both bacteria, pointing to some common mechanisms. The hope is that such information can be exploited to improve the use and performance of PGPB in agriculture.

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Section: Discussionmentioning

confidence: 99%

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

Amaral

Tuleski

Pankievicz

et al. 2020

mBio

View full text Add to dashboard Cite

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“…A specialized group of prokaryotes, the diazotrophic bacteria, is able to convert inert atmospheric nitrogen into biologically available ammonium (NH 4 ) by a process called biological N 2 fixation (BNF), which plays an important role for sustainable food production by contributing up to 65% of nitrogen used in agriculture ( Vance and Graham, 1995 ; Udvardi and Poole, 2013 ; Lindström and Mousavi, 2020 ). BNF by rhizobia involves the establishment of a symbiotic relationship, which leads to the formation of a specialized plant organ on the root or on the stem, the nodule ( Masson-Boivin et al, 2009 ; Oldroyd et al, 2011 ; Wheatley et al, 2020 ). Upon sensing plant signal molecules produced by the roots (flavonoids), rhizobia produce lipochitooligosaccharides, called Nod factors (NFs), which modulate the growth of the root tip and induce root hair curling ( Gage and Margolin, 2000 ; Cooper, 2007 ).…”

Section: Introductionmentioning

confidence: 99%

“…This high competitiveness mainly depends on environmental conditions (nitrogen limitation as well as low pH favors P. phymatum dominance) and on host and symbiont genotype ( Elliott et al, 2009 ; Garau et al, 2009 ). In other rhizobia, lipopolysaccharides (LPS), exopolysaccharides (EPS), antibiotic production ( Bhagwat et al, 1991 ; Zdor and Pueppke, 1991 ; Robleto et al, 1998 ; Geddes et al, 2014 ), motility ( Mellor et al, 1987 ), and catabolism of certain compounds ( Kohler et al, 2010 ; Ding et al, 2012 ; Wheatley et al, 2020 ) have been shown to be important for high competitiveness. However, the factors that are important for competitiveness and promiscuity of P. phymatum are still largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Differential Expression of Paraburkholderia phymatum Type VI Secretion Systems (T6SS) Suggests a Role of T6SS-b in Early Symbiotic Interaction

et al. 2021

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Paraburkholderia phymatum STM815, a rhizobial strain of the Burkholderiaceae family, is able to nodulate a broad range of legumes including the agriculturally important Phaseolus vulgaris (common bean). P. phymatum harbors two type VI Secretion Systems (T6SS-b and T6SS-3) in its genome that contribute to its high interbacterial competitiveness in vitro and in infecting the roots of several legumes. In this study, we show that P. phymatum T6SS-b is found in the genomes of several soil-dwelling plant symbionts and that its expression is induced by the presence of citrate and is higher at 20/28°C compared to 37°C. Conversely, T6SS-3 shows homologies to T6SS clusters found in several pathogenic Burkholderia strains, is more prominently expressed with succinate during stationary phase and at 37°C. In addition, T6SS-b expression was activated in the presence of germinated seeds as well as in P. vulgaris and Mimosa pudica root nodules. Phenotypic analysis of selected deletion mutant strains suggested a role of T6SS-b in motility but not at later stages of the interaction with legumes. In contrast, the T6SS-3 mutant was not affected in any of the free-living and symbiotic phenotypes examined. Thus, P. phymatum T6SS-b is potentially important for the early infection step in the symbiosis with legumes.

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“…Conversely transcriptomic analysis of R. leguminosarum, bacteroids reported that pRL100286-87 and pRL100291 genes (the putative orthologs of these genes) were down-regulated in bacteroids of common bean and pea nodules (Green et al, 2019). Even more, mutants in pRL100286-87 genes improved bacterial colonization in pea roots (Wheatley et al, 2020). In R. leguminosarum bv.…”

Section: Discussionmentioning

confidence: 99%

A Novel OmpR-Type Response Regulator Controls Multiple Stages of the Rhizobium etli – Phaseolus vulgaris N2-Fixing Symbiosis

et al. 2020

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OmpR, is one of the best characterized response regulators families, which includes transcriptional regulators with a variety of physiological roles including the control of symbiotic nitrogen fixation (SNF). The Rhizobium etli CE3 genome encodes 18 OmpR-type regulators; the function of the majority of these regulators during the SNF in common bean, remains elusive. In this work, we demonstrated that a R. etli mutant strain lacking the OmpR-type regulator RetPC57 (ΔRetPC57), formed less nodules when used as inoculum for common bean. Furthermore, we observed reduced expression level of bacterial genes involved in Nod Factors production (nodA and nodB) and of plant early-nodulation genes (NSP2, NIN, NF-YA and ENOD40), in plants inoculated with ΔRetPC57. RetPC57 also contributes to the appropriate expression of genes which products are part of the multidrug efflux pumps family (MDR). Interestingly, nodules elicited by ΔRetPC57 showed increased expression of genes relevant for Carbon/Nitrogen nodule metabolism (PEPC and GOGAT) and ΔRetPC57 bacteroids showed higher nitrogen fixation activity as well as increased expression of key genes directly involved in SNF (hfixL, fixKf, fnrN, fixN, nifA and nifH). Taken together, our data show that the previously uncharacterized regulator RetPC57 is a key player in the development of the R. etli - P. vulgaris symbiosis.

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Lifestyle adaptations ofRhizobiumfrom rhizosphere to symbiosis

Cited by 93 publications

References 86 publications

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

Differential Expression of Paraburkholderia phymatum Type VI Secretion Systems (T6SS) Suggests a Role of T6SS-b in Early Symbiotic Interaction

A Novel OmpR-Type Response Regulator Controls Multiple Stages of the Rhizobium etli – Phaseolus vulgaris N2-Fixing Symbiosis

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