Identifying abnormalities in symbiotic development between Trifolium spp. and Rhizobium leguminosarum bv. trifolii leading to sub-optimal and ineffective nodule phenotypes

Melino, Vanessa; Drew, Elizabeth; Ballard, Ross; Reeve, Wayne; Thomson, G.; White, Rosemary G.; O’Hara, G.W.

doi:10.1093/aob/mcs206

Cited by 26 publications

(29 citation statements)

References 47 publications

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“…Initial attempts were made to grow Rl -SRDI565 in completely defined medium, such as M9 minimal media containing 125 μg mL −1 biotin 21 , to allow assessment of different carbon sources on bacterial growth. However, optimal growth could only be achieved using a yeast extract-based medium 15 . In particular robust growth was achieved using a 5% dilution of 1 g L −1 yeast extract (Y 5% media) containing 5 mmol mannitol (Y 5% M), while no detectable bacterial growth was observed on Y 5% media alone.…”

Section: Resultsmentioning

confidence: 99%

“…14 Colonization of trifolium species with Rl -SRDI565 results in suboptimal nodulation and nitrogen fixation in some species and ineffective nitrogen fixation in others, leading to reduced shoot nitrogen content relative to other commercial strains. 15 Interestingly, the genome of Rl -SRDI565 encodes all the genes needed for a functional sulfo-ED pathway, 16 although there is no evidence to show that this is operative and/or that Rl -SRDI565 can use SQ as a major carbon source.…”

Section: Introductionmentioning

confidence: 99%

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A sulfoglycolytic Entner-Doudoroff pathway inRhizobium leguminosarumbv.trifoliiSRDI565

Li¹,

Epa²,

Scott

et al. 2019

Preprint

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32Rhizobia are nitrogen fixing bacteria that engage in symbiotic relationships with plant hosts 33 but can also persist as free-living bacteria with the soil and rhizosphere. Here we show that free 34 living Rhizobium leguminosarum SRDI565 can grow on the sulfosugar sulfoquinovose (SQ) 35 using a sulfoglycolytic Entner-Doudoroff (sulfo-ED) pathway resulting in production of 36 sulfolactate (SL) as the major metabolic end-product. Comparative proteomics supports the 37 involvement of a sulfo-ED operon encoding an ABC transporter cassette, sulfo-ED enzymes 38 and an SL exporter. Consistent with an oligotrophic lifestyle, proteomics data revealed little 39 change in expression of the sulfo-ED proteins during growth on SQ versus mannitol, a result 40 confirmed through biochemical assay of sulfoquinovosidase activity in cell lysates (data are 41 available via ProteomeXchange with identifier PXD015822). Metabolomics analysis showed 42 that growth on SQ involves gluconeogenesis to satisfy metabolic requirements for glucose-6-43 phosphate and fructose-6-phosphate. Metabolomics analysis also revealed the unexpected 44 production of small amounts of sulfofructose and 2,3-dihydroxypropanesulfonate, which are 45 proposed to arise from promiscuous activities of the glycolytic enzyme phosphoglucose 46 isomerase and a non-specific aldehyde reductase, respectively. This work shows that rhizobial 47 metabolism of the abundant sulfosugar SQ may contribute to persistence of the bacteria in the 48 soil and to mobilization of sulfur in the pedosphere. 49 50 Results 127Analysis of the genome of Rl-SRDI565 revealed a sulfo-ED operon that had the same 128 genes, but no synteny with the P. putida SQ1 operon (Figure 1). Genes with high homology to 129 the P. putida proteins included a putative SQase, SQ dehydrogenase, SL lactonase, SG 130 dehydratase, KDSG aldolase and SLA dehydrogenase, and an SL exporter (see Figures S1-S6). 131The Rl-SRDI565 operon contains some important differences compared to that of P. putida 132 SQ1. In particular, it lacks a putative SQ mutarotase, 20 and appears to use an ABC transporter 133 cassette to import SQ/SQGro in place of an SQ/SQGro importer/permease. The putative sulfo-134 ED pathway in Rl-SRDI565 is consistent with the proposed protein functions outlined in Figure 135 1b, with a comparison to the classical ED pathway in Figure 1c. 136

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A sulfoglycolytic Entner-Doudoroff pathway inRhizobium leguminosarumbv.trifoliiSRDI565

Li¹,

Epa²,

Scott

et al. 2019

Preprint

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“…(); (9) J. Howieson personal Communication; (10) Melino et al . (); (11) Reeve et al . (); (12) Reeve et al .…”

Section: Resultsmentioning

confidence: 99%

Assessment of core and accessory genetic variation in Rhizobium leguminosarum symbiovar trifolii strains from diverse locations and host plants using PCR-based methods

Mauchline

Hayat

Roberts

et al. 2014

Lett Appl Microbiol

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The nitrogen-fixing symbiosis between Rhizobium leguminosarum and host legumes is recognized as a key part of sustainable agriculture. A culture collection containing rhizobia isolated from legumes of economic importance in the UK and worldwide, maintained at Rothamsted Research for many years, provided material for this study. We aimed to develop and validate efficient molecular diagnostics to investigate whether the host plant or geographical location had a greater influence on the genetic diversity of rhizobial isolates, and the extent to which the core bacterial genome and the accessory symbiosis genes located on plasmids were affected. To achieve this, core housekeeping genes and those involved in symbiosis interactions were sequenced and compared with genome-sequenced strains in the public domain. Results showed that some Rh. leguminosarum symbiovar trifolii strains nodulating clovers and Rh. leguminosarum sv. viciae strains nodulating peas and vicias shared identical housekeeping genes, clover nodule isolates from the same location could have divergent symbiosis genes, and others isolated on different continents could be very similar. This illustrates the likely co-migration of rhizobia and their legume hosts when crops are planted in new areas and indicates that selective pressure may arise from both local conditions and crop host genotypes.

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“…Commonly, Rlt strains isolated from red, white, or Persian clovers nodulated efficiently their original host plants (Beauregard et al 2004 ). However, various responses of host plants from the same cross-inoculation group or the same species to a particular rhizobial strain have also been described, but the cause of this symbiotic incompatibility was mostly unexplained (Balatti and Pueppke 1992 ; Tesfaye and Holl 1999 ; Beauregard et al 2004 ; Brito et al 2008 ; Melino et al 2012 ). Miller et al ( 2007 ) described efficient symbiosis of the Rlt strain with T. ambiguum (Caucasian clover) and inefficient symbiosis with T. repens.…”

Section: Discussionmentioning

confidence: 99%

“…In another case, Rlt strains are able to form effective nodules on Trifolium ambiguum (Caucasian clover) but ineffective ones on T. repens, T. pratense and vice versa (Beauregard et al 2004 ; Miller et al 2007 ). Melino et al ( 2012 ) reported sub-optimal or ineffective symbiotic association between an Rlt strain and T. subterraneum , T. purpureum , and Trifolium polymorphum . These reports show that rhizobial strains commonly found in agricultural soils are frequently poorly compatible with commercially grown clover species but little is known of the cause of their ineffectivity.…”

Section: Introductionmentioning

confidence: 99%

Host-dependent symbiotic efficiency of Rhizobium leguminosarum bv. trifolii strains isolated from nodules of Trifolium rubens

Marek-Kozaczuk

Wdowiak-Wróbel

Kalita

et al. 2017

Antonie van Leeuwenhoek

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Trifolium rubens L., commonly known as the red feather clover, is capable of symbiotic interactions with rhizobia. Up to now, no specific symbionts of T. rubens and their symbiotic compatibility with Trifolium spp. have been described. We characterized the genomic diversity of T. rubens symbionts by analyses of plasmid profiles and BOX–PCR. The phylogeny of T. rubens isolates was inferred based on the nucleotide sequences of 16S rRNA and two core genes (atpD, recA). The nodC phylogeny allowed classification of rhizobia nodulating T. rubens as Rhizobium leguminosarum symbiovar trifolii (Rlt). The symbiotic efficiency of the Rlt isolates was determined on four clover species: T. rubens, T. pratense, T. repens and T. resupinatum. We determined that Rlt strains formed mostly inefficient symbiosis with their native host plant T. rubens and weakly effective (sub-optimal) symbiosis with T. repens and T. pratense. The same Rlt strains were fully compatible in the symbiosis with T. resupinatum. T. rubens did not exhibit strict selectivity in regard to the symbionts and rhizobia closely related to Rhizobium grahamii, Rhizobium galegae and Agrobacterium radiobacter, which did not nodulate Trifolium spp., were found amongst T. rubens nodule isolates.Electronic supplementary materialThe online version of this article (doi:10.1007/s10482-017-0922-7) contains supplementary material, which is available to authorized users.

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Identifying abnormalities in symbiotic development between Trifolium spp. and Rhizobium leguminosarum bv. trifolii leading to sub-optimal and ineffective nodule phenotypes

Cited by 26 publications

References 47 publications

A sulfoglycolytic Entner-Doudoroff pathway inRhizobium leguminosarumbv.trifoliiSRDI565

A sulfoglycolytic Entner-Doudoroff pathway inRhizobium leguminosarumbv.trifoliiSRDI565

Assessment of core and accessory genetic variation in Rhizobium leguminosarum symbiovar trifolii strains from diverse locations and host plants using PCR-based methods

Host-dependent symbiotic efficiency of Rhizobium leguminosarum bv. trifolii strains isolated from nodules of Trifolium rubens

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