RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Lace, Beatrice; Su, Chao; Perez, Daniel Invernot; Rodriguez‐Franco, Marta; Vernié, Tatiana; Batzenschlager, Morgane; Egli, Sabrina; Liu, Cheng-Wu; Ott, Thomas

doi:10.1101/2022.06.03.494689

Cited by 4 publications

(9 citation statements)

References 86 publications

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“…In this study, we found that RPG was localized in puncta, some of which were close to the nucleus in N. benthamiana leaves and L. japonicus root protoplasts. A very recent study in M. truncatula showed that the IT tip-to-nucleus microtubule connectivity is perturbed in rpg-1 [55]. Together, all these studies strongly indicated that RPG plays an important role in nuclear-led IT elongation.…”

Section: Discussionmentioning

confidence: 72%

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

Liu

Cai

et al. 2023

PLoS Genet

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Symbiotic interactions between rhizobia and legumes result in the formation of root nodules, which fix nitrogen that can be used for plant growth. Rhizobia usually invade legume roots through a plant-made tunnel-like structure called an infection thread (IT). RPG (Rhizobium-directed polar growth) encodes a coiled-coil protein that has been identified in Medicago truncatula as required for root nodule infection, but the function of RPG remains poorly understood. In this study, we identified and characterized RPG in Lotus japonicus and determined that it is required for IT formation. RPG was induced by Mesorhizobium loti or purified Nodulation factor and displayed an infection-specific expression pattern. Nodule inception (NIN) bound to the RPG promoter and induced its expression. We showed that RPG displayed punctate subcellular localization in L. japonicus root protoplasts and in root hairs infected by M. loti. The N-terminal predicted C2 lipid-binding domain of RPG was not required for this subcellular localization or for function. CERBERUS, a U-box E3 ligase which is also required for rhizobial infection, was found to be localized similarly in puncta. RPG co-localized and directly interacted with CERBERUS in the early endosome (TGN/EE) compartment and near the nuclei in root hairs after rhizobial inoculation. Our study sheds light on an RPG-CERBERUS protein complex that is involved in an exocytotic pathway mediating IT elongation.

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Section: Discussionmentioning

confidence: 72%

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

Liu

Cai

et al. 2023

PLoS Genet

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“…Although the mixed step of intracellular accommodation including the release of symbiosomes and their persistence in the Medicago and Mimosa dataset displays a peculiar evolutionary pattern (see below and Figure 3), this symbiotic stage also involved genes that are part of the ancestral transcriptomic response. Suppressors of plant defense in nodules, SYMCRK 55 and RSD 56 , as well as the transcription regulator EFD required for both plant and bacteroid differentiation in Medicago 57,58 the M. pudica data, we found VAPYRIN, RPG, some flotillin and remorin genes and the syntaxin SYN, which are well-known infection-associated genes 33,[59][60][61] . We thus hypothesize that a proportion of genes linked with the ancestral RNS transcriptome and associated with intracellular accommodation reflects infection (Figure 4C).…”

Section: Gradual Recruitment Of Plant Symbiotic Gene Expression In Ex...mentioning

confidence: 63%

“…Suppressors of plant defense in nodules, SYMCRK 55 and RSD 56 , as well as the transcription regulator EFD required for both plant and bacteroid differentiation in Medicago 57,58 participate to this ancestral response. Looking specifically at the M. pudica data, we found VAPYRIN, RPG, some flotillin and remorin genes and the syntaxin SYN, which are well-known infection-associated genes 33,59–61 . We thus hypothesize that a proportion of genes linked with the ancestral RNS transcriptome and associated with intracellular accommodation reflects infection (Figure 4C).…”

Section: Resultsmentioning

confidence: 94%

“…In particular, a total of 771/1481 orthogroups (151%/167% increase compared to the mean null expectation) were inferred to have been already up/down-regulated in the most recent common ancestor of all RNS-forming species. Among the 771 ancestrally up-regulated orthogroups, 157 contain genes with a known function, such as the common symbiotic pathway members LjNFR5/MtNFP 25,26 , SYMRK/DMI2 27,28 , CCaMK/DMI3 29 , CYCLOPS/IPD3 30 , the master symbiotic regulator NIN 31 or the infection-associated gene RPG 32,33 . The phylogenetic distribution of three of them, LjNFR5/MtNFP, NIN and RPG, has been recently linked with the ability to form RNS in the NFN clade.…”

Section: Resultsmentioning

confidence: 99%

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Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

Libourel

Keller

Brichet

et al. 2022

Preprint

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Symbiotic interactions have structured past and present ecosystems, and shaped the evolution of life. As any trait, the symbiotic state observed in extant species builds on ancestral and conserved features, and lineage-specific innovations. From these mixed origins, defining the ancestral state of symbiotic associations is challenging although it is instrumental for understanding how symbiotic abilities emerge from non-symbiotic states. Here we aimed at reconstructing the intermediate steps leading to the root-nodule nitrogen-fixing symbiosis (RNS) observed in some extant flowering plants. For this, we compared the transcriptomic responses of nine host plants in response to symbiotic bacteria. We included the mimosoid legume Mimosa pudica for which we assembled a chromosome-level genome and generated the transcriptomic response to experimentally evolved bacterial symbionts. With this dataset, we reconstructed the ancestral RNS transcriptome, composed of most already described symbiotic genes together with hundreds of novel candidates. We found that the response to the chemical signals produced by the symbiont, nodule organogenesis and nitrogen-fixation are predominantly linked to ancestral responses, although these traits have diversified in the different nitrogen-fixing lineages. We detected a clear signature of recent and convergent evolution for the ability to release intracellular symbiosomes in two legume lineages, exemplified by the expression of different classes of small proteins in each group, potentially leading to the convergent gain of symbiotic evolutionary stability. Our findings demonstrate that most of the novelties for RNS were mostly in place in the most recent common ancestor of the RNS-forming species that lived on Earth 110 million years ago.

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“…In this study, we found that RPG was localized in puncta close to the nucleus in N. benthamiana leaves and L. japonicus root protoplasts. A very recent study in M. truncatula showed that the IT tip-to-nucleus microtubule connectivity is perturbed in rpg-1 (Lace et al, 2022). Together all these studies strongly indicated that RPG plays important roles in nuclear-led IT elongation.…”

Section: Discussionmentioning

confidence: 99%

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

Liu²,

Cai

et al. 2022

Preprint

View full text Add to dashboard Cite

Symbiotic interactions between rhizobia and legumes result in the formation of root nodules, which fix nitrogen that can be used for plant growth. Rhizobia usually invade legume roots through a plant-made tunnel-like structure called an infection thread (IT). Rhizobium-directed polar growth (RPG) encodes a coiled-coil protein that was identified in Medicago truncatula as required for root nodule infection, but the function of RPG remains poorly understood. In this study, we identified and characterized RPG in Lotus japonicus and determined that it is required for IT formation. RPG was induced by Mesorhizobium loti or purified Nodulation factor and displayed an infection-specific expression pattern. Nodule inception (NIN) bound to the RPG promoter and induced its expression. A GFP-RPG protein was localized in puncta subcellular localization in L. japonicus root protoplasts and in root hairs infected by M. loti. The N-terminal predicted C2 lipid-binding domain of RPG was not required for this subcellular localization or for function. CERBERUS, a U-box E3 ligase which is also required for rhizobial infection, was found to be localized in similar puncta. RPG co-localized and directly interacted with CERBERUS at the early endosomes (TGN/EE) compartment and near the nuclei in root hairs after rhizobia inoculation. Our study sheds light on that a RPG-CERBERUS protein complex that is involved in an exocytotic pathway mediating IT polarity growth which is driven by nuclear migration.

show abstract

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Cited by 4 publications

References 86 publications

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

RPG interacts with E3-ligase CERBERUS to mediate rhizobial infection in Lotus japonicus

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