Integrating DNA Methylation and Gene Expression Data in the Development of the Soybean-Bradyrhizobium N2-Fixing Symbiosis

Davis-Richardson, Austin G.; Russell, Jordan T.; Dias, Raquel; McKinlay, Andrew J.; Canepa, R; Fagen, Jennie R.; Rusoff, Kristin T.; Drew, Jennifer C.; Kolaczkowski, Bryan; Emerich, David W.; Triplett, Eric W.

doi:10.3389/fmicb.2016.00518

Cited by 17 publications

(23 citation statements)

References 41 publications

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“…Conversely, it remains unknown if methylation of rhizobium DNA contributes to the regulation of N 2 -fixation or bacteroid development. We are aware of only one study (38) comparing DNA methylation of a rhizobium ( Bradyrhizobium diazoefficiens USDA110) between free-living and symbiotic states (soybean nodules), and comparing these changes with differential expression data. Intriguingly, the authors identified a DNA motif that was methylated specifically in bacteroids (38).…”

Section: Introductionmentioning

confidence: 99%

DNA methylation inEnsiferspecies during free-living growth and during nitrogen-fixing symbiosis withMedicagospp.

diCenzo

Cangioli

Nicoud

et al. 2021

Preprint

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Methylation of specific genomic DNA sequences is ubiquitous in bacteria and has known roles in immunity and regulation of cellular processes, such as the cell cycle. Here, we explored DNA methylation in bacteria of the genus Ensifer, including its potential role in regulating the process of terminal differentiation occurring during nitrogen-fixing symbiosis with legumes. Using single-molecule real-time sequencing, six unique genome-wide methylated motifs were identified across four Ensifer strains, five of which were strain-specific. These five motifs were nearly fully methylated across the genomes in all tested conditions, and they were not enriched in the promoter regions of symbiosis, carbon source, or cell cycle-regulated genes, suggesting that most DNA methylation is not a major regulatory mechanism in the genus Ensifer. Only the GANTC motif, recognized by the cell cycle-regulated CcrM methyltransferase, was methylated in all strains. In actively dividing cells, methylation of GANTC motifs increased progressively from the ori to ter region in each replicon, in agreement with a cell cycle-dependent regulation of CcrM. The GANTC methylation profile transited into a genome-wide pattern of near full methylation in the early stage of symbiotic differentiation, followed by a progressive decrease in methylation from the ori to ter regions of fully differentiated symbiotic bacteria. This is evidence of a dysregulated and constitutive CcrM activity during terminal differentiation, which we suggest is a driving factor for endoreduplication of terminally differentiated bacteroids.

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Section: Introductionmentioning

confidence: 99%

DNA methylation inEnsiferspecies during free-living growth and during nitrogen-fixing symbiosis withMedicagospp.

diCenzo

Cangioli

Nicoud

et al. 2021

Preprint

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“…pestis [22] or A . hydrophila [46], the only studies about DNA methylation involvement in symbiosis are limited to bacterial-plant interactions: in Bradyrhizobium , differences observed in DNA-methylation pattern between the free-living state and the symbiotic state suggest a role in cell differentiation [25] and in Mesorhizobium loti overexpression of a methyltransferase delayed nodulation [26, 27]. Here, no difference was observed in the number of emerging IJs between both nemato-bacterial complexes after infestation of both insect models showing the lack of involvement of Dam DNA methylation during P .…”

Section: Discussionmentioning

confidence: 99%

“…pylori [23, 24] have also been described. However, the involvement of DNA methylation in mutualistic associations are focused on host modifications, whereas bacterial DNA methylation data are scarce and limited to bacterial-plant interactions [25–27]. Recently we showed that the overexpression of dam using a medium-copy-number plasmid in P .…”

Section: Introductionmentioning

confidence: 99%

Role of the Photorhabdus Dam methyltransferase during interactions with its invertebrate hosts

et al. 2019

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Photorhabdus luminescens is an entomopathogenic bacterium found in symbiosis with the nematode Heterorhabditis. Dam DNA methylation is involved in the pathogenicity of many bacteria, including P. luminescens, whereas studies about the role of bacterial DNA methylation during symbiosis are scarce. The aim of this study was to determine the role of Dam DNA methylation in P. luminescens during the whole bacterial life cycle including during symbiosis with H. bacteriophora. We constructed a strain overexpressing dam by inserting an additional copy of the dam gene under the control of a constitutive promoter in the chromosome of P. luminescens and then achieved association between this recombinant strain and nematodes. The dam overexpressing strain was able to feed the nematode in vitro and in vivo similarly as a control strain, and to re-associate with Infective Juvenile (IJ) stages in the insect. No difference in the amount of emerging IJs from the cadaver was observed between the two strains. Compared to the nematode in symbiosis with the control strain, a significant increase in LT50 was observed during insect infestation with the nematode associated with the dam overexpressing strain. These results suggest that during the life cycle of P. luminescens, Dam is not involved the bacterial symbiosis with the nematode H. bacteriophora, but it contributes to the pathogenicity of the nemato-bacterial complex.

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“…The study unraveled twice as many hitherto known DNA binding specificities of methytransferases (MTases) and more than 800 distinct reproducible methylated motifs (Blow et al, 2016). The role of epigenetic events becomes more relevant to our perspective when it is reported to drive the phase change of free-living bacteria such as Bradyrhizobium diazoefficiens to symbiotic bacteria because of methylation of specific motifs during the process of symbiosis (Davis-Richardson et al, 2016). Yet another basis of variability in the microbiome is the phenomenon termed as ‘horizontal gene transfer’ (HGT) (de la Cruz and Davies, 2000) that predominantly occurs in rhizosphere environment.…”

Section: Microbiome Offers Genetic Variability To Plantsmentioning

confidence: 99%

Microbiome Selection Could Spur Next-Generation Plant Breeding Strategies

2016

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“No plant is an island too…”Plants, though sessile, have developed a unique strategy to counter biotic and abiotic stresses by symbiotically co-evolving with microorganisms and tapping into their genome for this purpose. Soil is the bank of microbial diversity from which a plant selectively sources its microbiome to suit its needs. Besides soil, seeds, which carry the genetic blueprint of plants during trans-generational propagation, are home to diverse microbiota that acts as the principal source of microbial inoculum in crop cultivation. Overall, a plant is ensconced both on the outside and inside with a diverse assemblage of microbiota. Together, the plant genome and the genes of the microbiota that the plant harbors in different plant tissues, i.e., the ‘plant microbiome,’ form the holobiome which is now considered as unit of selection: ‘the holobiont.’ The ‘plant microbiome’ not only helps plants to remain fit but also offers critical genetic variability, hitherto, not employed in the breeding strategy by plant breeders, who traditionally have exploited the genetic variability of the host for developing high yielding or disease tolerant or drought resistant varieties. This fresh knowledge of the microbiome, particularly of the rhizosphere, offering genetic variability to plants, opens up new horizons for breeding that could usher in cultivation of next-generation crops depending less on inorganic inputs, resistant to insect pest and diseases and resilient to climatic perturbations. We surmise, from ever increasing evidences, that plants and their microbial symbionts need to be co-propagated as life-long partners in future strategies for plant breeding. In this perspective, we propose bottom–up approach to co-propagate the co-evolved, the plant along with the target microbiome, through – (i) reciprocal soil transplantation method, or (ii) artificial ecosystem selection method of synthetic microbiome inocula, or (iii) by exploration of microRNA transfer method – for realizing this next-generation plant breeding approach. Our aim, thus, is to bring closer the information accrued through the advanced nucleotide sequencing and bioinformatics in conjunction with conventional culture-dependent isolation method for practical application in plant breeding and overall agriculture.

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Integrating DNA Methylation and Gene Expression Data in the Development of the Soybean-Bradyrhizobium N2-Fixing Symbiosis

Cited by 17 publications

References 41 publications

DNA methylation inEnsiferspecies during free-living growth and during nitrogen-fixing symbiosis withMedicagospp.

DNA methylation inEnsiferspecies during free-living growth and during nitrogen-fixing symbiosis withMedicagospp.

Role of the Photorhabdus Dam methyltransferase during interactions with its invertebrate hosts

Microbiome Selection Could Spur Next-Generation Plant Breeding Strategies

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