The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus

Madsen, Lene Heegaard; Tirichine, Leïla; Jurkiewicz, Anna; Sullivan, John T.; Heckmann, Anne B.; Bek, Anita S.; Ronson, Clive W.; James, Euan K.; Stougaard, Jens

doi:10.1038/ncomms1009

Cited by 434 publications

(392 citation statements)

References 55 publications

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“…3). Interestingly, these homologs covered the entire symbiotic pathway from the signal perception to the nodulation process via the bacterial and fungal common pathway, as described (Kistner and Parniske, 2002;Markmann and Parniske, 2009;Madsen et al, 2010). Eight of them (Lys-6, SYMREM1, DMI2/SymRK, DMI3/CCaMK, Hap2-1, HMGR, Cyp2, and Cyp4) were identified in both species.…”

Section: Validation Of Microarray Resultsmentioning

confidence: 99%

Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade

et al. 2011

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Comparative transcriptomics of two actinorhizal symbiotic plants, Casuarina glauca and Alnus glutinosa, was used to gain insight into their symbiotic programs triggered following contact with the nitrogen-fixing actinobacterium Frankia. Approximately 14,000 unigenes were recovered in roots and 3-week-old nodules of each of the two species. A transcriptomic array was designed to monitor changes in expression levels between roots and nodules, enabling the identification of up-and downregulated genes as well as root-and nodule-specific genes. The expression levels of several genes emblematic of symbiosis were confirmed by quantitative polymerase chain reaction. As expected, several genes related to carbon and nitrogen exchange, defense against pathogens, or stress resistance were strongly regulated. Furthermore, homolog genes of the common and nodule-specific signaling pathways known in legumes were identified in the two actinorhizal symbiotic plants. The conservation of the host plant signaling pathway is all the more surprising in light of the lack of canonical nod genes in the genomes of its bacterial symbiont, Frankia. The evolutionary pattern emerging from these studies reinforces the hypothesis of a common genetic ancestor of the Fabid (Eurosid I) nodulating clade with a genetic predisposition for nodulation.

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Section: Validation Of Microarray Resultsmentioning

confidence: 99%

Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade

et al. 2011

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“…Root hair infection was shown to be the most controlled entry process and proposed to be the most highly evolved mode of root invasion in legumes (Madsen et al, 2010), while symbiosome accommodation that does not occur in all symbioses (Sprent, 2007) is considered as the most evolved nodule cell infection process. Our work provides support to similar requirements at both root hair and nodule cell entry levels that we speculate to have favoured the coevolution of bacterial capacity to enter root hairs and nodule cells in the course of the legume-rhizobium evolution.…”

Section: Discussionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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“…A series of plant genes involved in perception of rhizobial NF signals have recently been identified in Lotus japonicus, Medicago truncatula, and other legumes Wais et al, 2000;Miwa et al, 2006;Madsen et al, 2010;Oldroyd et al, 2011). NFs are perceived by two receptor kinases, nodulation factor receptor1 (NFR1) and NFR5, which belong to the Lysin-motif receptor-like kinases (RLKs; Madsen et al, 2003;Radutoiu et al, 2003Radutoiu et al, , 2007.…”

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confidence: 99%

A Ubiquitin Ligase of Symbiosis Receptor Kinase Involved in Nodule Organogenesis

et al. 2012

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The symbiosis receptor kinase (SymRK) is required for morphological changes of legume root hairs triggered by rhizobial infection. How protein turnover of SymRK is regulated and how the nodulation factor signals are transduced downstream of SymRK are not known. In this report, a SymRK-interacting E3 ubiquitin ligase (SIE3) was shown to bind and ubiquitinate SymRK. The SIE3-SymRK interaction and the ubiquitination of SymRK were shown to occur in vitro and in planta. SIE3 represents a new class of plant-specific E3 ligases that contain a unique pattern of the conserved CTLH (for C-terminal to LisH), CRA (for CT11-RanBPM), and RING (for Really Interesting New Gene) domains. Expression of SIE3 was detected in all tested tissues of Lotus japonicus plants, and its transcript level in roots was enhanced by rhizobial infection. The SIE3 protein was localized to multiple subcellular locations including the nuclei and plasma membrane, where the SIE3-SymRK interaction took place. Overexpression of SIE3 promoted nodulation in transgenic hairy roots, whereas downregulation of SIE3 transcripts by RNA interference inhibited infection thread development and nodule organogenesis. These results suggest that SIE3 represents a new class of E3 ubiquitin ligase, acts as a regulator of SymRK, and is involved in rhizobial infection and nodulation in L. japonicus.

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The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus

Cited by 434 publications

References 55 publications

Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade

Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade

Experimental evolution of nodule intracellular infection in legume symbionts

A Ubiquitin Ligase of Symbiosis Receptor Kinase Involved in Nodule Organogenesis

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