Invasion of <i>Lotus japonicus root hairless 1</i> by <i>Mesorhizobium loti</i> Involves the Nodulation Factor-Dependent Induction of Root Hairs

Karas, Bogumil J.; Murray, J. D.; Gorzelak, M.; Smith, A.K.; Sato, Shusei; Tabata, Satoshi; Szczygłowski, Krzysztof

doi:10.1104/pp.104.057513

Cited by 63 publications

(77 citation statements)

References 54 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…This is unlike in L. japonicus plants carrying the wild-type Lhk1 gene, where empty or initially empty nodules readily develop in the presence of various mutations that affect infections (Karas et al, 2005;Yokota et al, 2009;Groth et al, 2010), including symRK-14 and arpc1-1 (Kosuta et al, 2011;Hossain et al, 2012).…”

Section: Lhk1 Mediates Signaling Without Bacterial Entry Into Rootsmentioning

confidence: 91%

Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation

et al. 2014

Self Cite

View full text Add to dashboard Cite

Previous analysis of the Lotus histidine kinase1 (Lhk1) cytokinin receptor gene has shown that it is required and also sufficient for nodule formation in Lotus japonicus. The L. japonicus mutant carrying the loss-of-function lhk1-1 allele is hyperinfected by its symbiotic partner, Mesorhizobium loti, in the initial absence of nodule organogenesis. At a later time point following bacterial infection, lhk1-1 develops a limited number of nodules, suggesting the presence of an Lhk1-independent mechanism. We have tested a hypothesis that other cytokinin receptors function in at least a partially redundant manner with LHK1 to mediate nodule organogenesis in L. japonicus. We show here that L. japonicus contains a small family of four cytokinin receptor genes, which all respond to M. loti infection. We show that within the root cortex, LHK1 performs an essential role but also works partially redundantly with LHK1A and LHK3 to mediate cell divisions for nodule primordium formation. The LHK1 receptor is also presumed to partake in mediating a feedback mechanism that negatively regulates bacterial infections at the root epidermis. Interestingly, the Arabidopsis thaliana AHK4 receptor gene can functionally replace Lhk1 in mediating nodule organogenesis, indicating that the ability to perform this developmental process is not determined by unique, legume-specific properties of LHK1.

show abstract

Section: Lhk1 Mediates Signaling Without Bacterial Entry Into Rootsmentioning

confidence: 91%

Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation

et al. 2014

Self Cite

View full text Add to dashboard Cite

show abstract

“…Later in the developmental process, patches of rhizobia were visible on top of the numerous empty nodules that formed on the mutant roots, from which colonization attempts similar to those observed in L. japonicus root-hairless mutant background (Karas et al, 2005) were occasionally launched ( Figure 3J). …”

Section: Root Hair Response and It Formation In Nap1 And Pir1 Mutantsmentioning

confidence: 96%

“…In vitro pollen germination experiments revealed about half the germination frequency in nap1-1, nap1-2, pir1-1, pir1-2, and pir1-3 mutant pollen (10 to 42%) compared with the wild type (57 to 82%). Likewise, when grown on the surface of vertically positioned agar plates (Karas et al, 2005), root hair formation appeared adversely affected in nap1-1, pir1-1, and pir1-1 nap1-1 double mutant roots when compared with wild-type control roots ( Figure 7A). Although consistent across all mutant genotypes and growth conditions tested, this phenotype was rather subtle.…”

Section: Expression Of the Nap1 And Pir1 Genesmentioning

confidence: 99%

See 1 more Smart Citation

Rearrangement of Actin Cytoskeleton Mediates Invasion ofLotus japonicusRoots byMesorhizobium loti

et al. 2009

Self Cite

View full text Add to dashboard Cite

Infection thread-dependent invasion of legume roots by rhizobia leads to internalization of bacteria into the plant cells, which is one of the salient features of root nodule symbiosis. We found that two genes, Nap1 (for Nck-associated protein 1) and Pir1 (for 121F-specific p53 inducible RNA), involved in actin rearrangements were essential for infection thread formation and colonization of Lotus japonicus roots by its natural microsymbiont, Mesorhizobium loti. nap1 and pir1 mutants developed an excess of uncolonized nodule primordia, indicating that these two genes were not essential for the initiation of nodule organogenesis per se. However, both the formation and subsequent progression of infection threads into the root cortex were significantly impaired in these mutants. We demonstrate that these infection defects were due to disturbed actin cytoskeleton organization. Short root hairs of the mutants had mostly transverse or web-like actin filaments, while bundles of actin filaments in wild-type root hairs were predominantly longitudinal. Corroborating these observations, temporal and spatial differences in actin filament organization between wild-type and mutant root hairs were also observed after Nod factor treatment, while calcium influx and spiking appeared unperturbed. Together with various effects on plant growth and seed formation, the nap1 and pir1 alleles also conferred a characteristic distorted trichome phenotype, suggesting a more general role for Nap1 and Pir1 in processes establishing cell polarity or polar growth in L. japonicus.

show abstract

“…Four mutations affecting the nodule symbiosis have been mapped on the lower part of chromosome 3, namely, HAR1, srh1, vrh1, and ccamk (Solaiman et al, 2000;Krusell et al, 2002;Nishimura et al, 2002;Karas et al, 2005;Sandal et al, 2006;Tirichine et al, 2006). However, the locations of these mutations and the phenotypes of the HAR1, srh1, and vrh1 mutants are different from the SL1795-4 mutant.…”

Section: Identification Of a Novel Mutation In L Japonicus Affectingmentioning

confidence: 99%

Lotus japonicusNodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume

Heckmann

Lombardo²,

Miwa³

et al. 2006

Plant Physiology

256

197

View full text Add to dashboard Cite

A new nodulation-defective mutant of Lotus japonicus does not initiate nodule cortical cell division in response to Mesorhizobium loti, but induces root hair deformation, Nod factor-induced calcium spiking, and mycorrhization. This phenotype, together with mapping data, suggested that the mutation could be in the ortholog of the Medicago truncatula NSP1 gene (MtNSP1). The sequence of the orthologous gene (LjNSP1) in the L. japonicus mutant (Ljnsp1-1) revealed a mutation causing a premature stop resulting in loss of the C-terminal 23 amino acids. We also sequenced the NSP2 gene from L. japonicus (LjNSP2). A mutant (Ljnsp2-3) with a premature stop codon was identified by TILLING showing a similar phenotype to Ljnsp1-1. Both LjNSP1 and LjNSP2 are predicted GRAS (GAI, RGA, SCR) domain transcriptional regulators. Transcript steady-state levels of LjNSP1 and LjNSP2 initially decreased and then increased following infection by M. loti. In hairy root transformations, LjNSP1 and MtNSP1 complemented both Mtnsp1-1 and Ljnsp1-1 mutants, demonstrating that these orthologous proteins have a conserved biochemical function. A Nicotiana benthamiana NSP1-like gene (NbNSP1) was shown to restore nodule formation in both Ljnsp1-1 and Mtnsp1-1 mutants, indicating that NSP1 regulators from legumes and non-legumes can propagate the Nod factor-induced signal, activating appropriate downstream targets. The L. japonicus nodules complemented with NbNSP1 contained some cells with abnormal bacteroids and could fix nitrogen. However, the NbNSP1-complemented M. truncatula nodules did not fix nitrogen and contained very few bacteria released from infection threads. These observations suggest that NSP1 is also involved in infection, bacterial release, and normal bacteroid formation in nodule cells.Legumes produce root nodules in response to Nod factors secreted by rhizobia. These Nod factor signals are essential for root hair deformation, induction of early nodulation genes, formation of nodule primordia, and infection by rhizobia. The earliest plant responses to Nod factors include an influx of calcium, plasmamembrane depolarizations, and then induction of cytosolic calcium spiking around the nucleus of epidermal root cells (Oldroyd and Downie, 2004). Purified Nod factors are sufficient to cause a range of early responses involved in the host developmental program (Hirsch and Fang, 1994;Schultze and Kondorosi, 1998;Downie and Walker, 1999). The Nod factors are the principle determinants by which legumes can be nodulated by specific rhizobia; the basis for this host specificity is the structure of the Nod factor, suggesting that highly specific plant receptors perceive Nod factor signals, thereby initiating the plant developmental response.Nod factor-induced root hair deformation is associated with reorganization of actin filaments in preparation for infection (Cardenas et al., 1998;Sieberer et al., 2005). The root hairs bend back, entrapping bacteria and thereby allowing infection foci to form as entrapped microcolonies. The infection thread, i...

show abstract

Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti Involves the Nodulation Factor-Dependent Induction of Root Hairs

Cited by 63 publications

References 54 publications

Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation

Lotus japonicus Cytokinin Receptors Work Partially Redundantly to Mediate Nodule Formation

Rearrangement of Actin Cytoskeleton Mediates Invasion ofLotus japonicusRoots byMesorhizobium loti

Lotus japonicusNodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume

Contact Info

Product

Resources

About