The Ethylene Responsive Factor Required for Nodulation 1 (ERN1) Transcription Factor Is Required for Infection-Thread Formation in Lotus japonicus

Several hundred genes are transcriptionally regulated during infection-thread formation and development of nitrogen-fixing root nodules. We have characterized a set of Lotus japonicus mutants impaired in root-nodule formation and found that the causative gene, Ern1, encodes a protein with a characteristic APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription-factor domain. Phenotypic characterization of four ern1 alleles shows that infection pockets are formed but root-hair infection threads are absent. Formation of root-nodule primordia is delayed and no normal transcellular infection threads are found in the infected nodules. Corroborating the role of ERN1 (ERF Required for Nodulation1) in nodule organogenesis, spontaneous nodulation induced by an autoactive CCaMK and cytokinin–induced nodule primordia were not observed in ern1 mutants. Expression of Ern1 is induced in the susceptible zone by Nod factor treatment or rhizobial inoculation. At the cellular level, the pErn1:GUS reporter is highly expressed in root epidermal cells of the susceptible zone and in the cortical cells that form nodule primordia. The genetic regulation of this cellular expression pattern was further investigated in symbiotic mutants. Nod factor induction of Ern1 in epidermal cells was found to depend on Nfr1, Cyclops, and Nsp2 but was independent of Nin and Nf-ya1. These results suggest that ERN1 functions as a transcriptional regulator involved in the formation of infection threads and development of nodule primordia and may coordinate these two processes.

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The Mesorhizobium loti purB Gene Is Involved in Infection Thread Formation and Nodule Development in Lotus japonicus

Journal of Bacteriology ◽

10.1128/jb.00788-07 ◽

2007 ◽

Vol 189 (22) ◽

pp. 8347-8352 ◽

Cited By ~ 18

Author(s):

Shin Okazaki ◽

Yoshiyuki Hattori ◽

Kazuhiko Saeki

Keyword(s):

Lotus Japonicus ◽

Infection Thread ◽

Nodule Development ◽

Nodule Formation ◽

Mesorhizobium Loti ◽

Infection Threads ◽

Thread Formation ◽

Infection Thread Formation

ABSTRACT The purB and purH mutants of Mesorhizobium loti exhibited purine auxotrophy and nodulation deficiency on Lotus japonicus. In the presence of adenine, only the purH mutant induced nodule formation and the purB mutant produced few infection threads, suggesting that 5-aminoimidazole-4-carboxamide ribonucleotide biosynthesis catalyzed by PurB is required for the establishment of symbiosis.

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Restriction of Infection Threads in Nodulation of Clover and Lucerne

Australian Journal of Biological Sciences ◽

10.1071/bi9580155 ◽

1958 ◽

Vol 11 (2) ◽

pp. 155 ◽

Cited By ~ 8

Author(s):

Hilary F Purchase

Keyword(s):

Trifolium Pratense ◽

Infection Thread ◽

Tube Culture ◽

Nodule Number ◽

Infection Threads ◽

Thread Formation ◽

Trifolium Pratense L ◽

Infection Thread Formation

Clover and lucerne roots from plants grown in tube culture were examined for infection thread formation and nodule number. The number of infection threads was about equal to the number of nodules in Trifolium pratense L.; this relation was shown to hold for abundantly and sparsely nodulating plants and for bacterial inocula.nts producing large and small numbers of nodules.

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Endoplasmic reticulum-targeted GFP reveals ER remodeling in Mesorhizobium-treated Lotus japonicus root hairs during root hair curling and infection thread formation

PROTOPLASMA ◽

10.1007/s00709-013-0584-x ◽

2013 ◽

Vol 251 (4) ◽

pp. 817-826 ◽

Cited By ~ 5

Author(s):

F. M. Perrine-Walker ◽

H. Kouchi ◽

R.W. Ridge

Keyword(s):

Endoplasmic Reticulum ◽

Root Hair ◽

Lotus Japonicus ◽

Root Hairs ◽

Infection Thread ◽

Thread Formation ◽

Hair Curling ◽

Root Hair Curling ◽

Infection Thread Formation

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Infection thread formation as a basis of nodulation specificity in Rhizobium – strawberry clover associations

Canadian Journal of Microbiology ◽

10.1139/m69-206 ◽

1969 ◽

Vol 15 (10) ◽

pp. 1133-1136 ◽

Cited By ~ 27

Author(s):

Diana Li ◽

D. H. Hubbell

Keyword(s):

Characteristic Root ◽

Root Hairs ◽

Infection Thread ◽

Root Hair Deformation ◽

Infection Threads ◽

Specific Substance ◽

Thread Formation ◽

Nodulation Specificity ◽

Infection Thread Formation

The basis for determination of nodulating specificity in Rhizobium–clover associations was investigated. Thirteen strains of rhizobia from eight different cross-inoculation groups were used to inoculate aseptically grown strawberry clover seedlings in slide culture. Microscopic observation revealed that each strain produced characteristic root hair deformation but infection threads and nodules were observed only in the homologous combination. It is concluded that, in rhizobia–clover combinations which nodulate via infection threads, specificity is determined at or before infection thread initiation. Observations of other workers that rhizobia produce a strain-specific substance affecting growth and morphology of legume root hairs were confirmed by results of this study.

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Exopolysaccharide Structure Is Not a Determinant of Host-Plant Specificity in Nodulation of Vicia sativa Roots

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-18-1123 ◽

2005 ◽

Vol 18 (11) ◽

pp. 1123-1129 ◽

Cited By ~ 16

Author(s):

Marc C. Laus ◽

Anton A. N. van Brussel ◽

Jan W. Kijne

Keyword(s):

Host Plant ◽

Rhizobium Leguminosarum ◽

Infection Thread ◽

Vicia Sativa ◽

Bacterial Growth Rate ◽

Successful Infection ◽

Infection Threads ◽

Thread Formation ◽

Host Plant Specificity ◽

Infection Thread Formation

Exopolysaccharide (EPS)-deficient strains of the root nodule symbiote Rhizobium leguminosarum induce formation of abortive infection threads in Vicia sativa subsp. nigra roots. As a result, the nodule tissue remains uninfected. Formation of an infection thread can be restored by coinoculation of the EPS-deficient mutant with a Nod factor-deficient strain, which produces a similar EPS structure. This suggests that EPS contributes to host-plant specificity of nodulation. Here, a comparison was made of i) coinoculation with heterologous strains with different EPS structures, and ii) introduction of the pRL1JI Sym plasmid or a nod gene-encoding fragment in the same heterologous strains. Most strains not complementing in coinoculation experiments were able to nodulate V. sativa roots as transconjugants. Apparently, coinoculation is a delicate approach in which differences in root colonization ability or bacterial growth rate easily affect successful infection-thread formation. Obviously, lack of infection-thread formation in coinoculation studies is not solely determined by EPS structure. Transconjugation data show that different EPS structures can allow infection-thread formation and subsequent nodulation of V. sativa roots.

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Plant genes involved in root-nodule development on legumes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1995.0144 ◽

1995 ◽

Vol 350 (1331) ◽

pp. 101-107 ◽

Cited By ~ 9

Keyword(s):

Root Nodule ◽

Nodule Development ◽

Nodule Formation ◽

Atmospheric Nitrogen ◽

Cortical Cells ◽

Nod Factor ◽

Plant Genes ◽

Thread Formation ◽

Nodulin Genes ◽

Infection Thread Formation

Rhizobium is able to induce the formation of a new organ on roots of leguminous plants, the root nodule, in which the penetrated bacteria fix atmospheric nitrogen. This process is initiated by specific lipo-oligosaccharides, called Nod factors, secreted by the bacterium. Nodule formation proceeds through distinct steps like infection thread formation and activation of mitotic activity in cortical cells. During these steps specific plant genes, nodulin genes, are induced and several of these have been identified and characterized. Nodulin genes are used now as markers to study Nod factor perception and signal transduction.

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Transcriptomic Analysis With the Progress of Symbiosis in ‘Crack-Entry’ Legume Arachis hypogaea Highlights Its Contrast With ‘Infection Thread’ Adapted Legumes

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-06-18-0174-r ◽

2019 ◽

Vol 32 (3) ◽

pp. 271-285 ◽

Cited By ~ 8

Author(s):

Kanchan Karmakar ◽

Anindya Kundu ◽

Ahsan Z Rizvi ◽

Emeric Dubois ◽

Dany Severac ◽

...

Keyword(s):

Arachis Hypogaea ◽

Root Nodule ◽

Infection Thread ◽

Cortical Cells ◽

Nod Factor ◽

Transcriptional Dynamics ◽

Infection Threads ◽

Spread Of Infection ◽

Molecular Framework ◽

Nodule Symbiosis

In root-nodule symbiosis, rhizobial invasion and nodule organogenesis is host controlled. In most legumes, rhizobia enter through infection threads and nodule primordium in the cortex is induced from a distance. But in dalbergoid legumes like Arachis hypogaea, rhizobia directly invade cortical cells through epidermal cracks to generate the primordia. Herein, we report the transcriptional dynamics with the progress of symbiosis in A. hypogaea at 1 day postinfection (dpi) (invasion), 4 dpi (nodule primordia), 8 dpi (spread of infection in nodule-like structure), 12 dpi (immature nodules containing rod-shaped rhizobia), and 21 dpi (mature nodules with spherical symbiosomes). Expression of putative ortholog of symbiotic genes in ‘crack entry’ legume A. hypogaea was compared with infection thread–adapted model legumes. The contrasting features were i) higher expression of receptors like LYR3 and EPR3 as compared with canonical Nod factor receptors, ii) late induction of transcription factors like NIN and NSP2 and constitutive high expression of ERF1, EIN2, bHLH476, and iii) induction of divergent pathogenesis-responsive PR-1 genes. Additionally, symbiotic orthologs of SymCRK, ROP6, RR9, SEN1, and DNF2 were not detectable and microsynteny analysis indicated the absence of a RPG homolog in diploid parental genomes of A. hypogaea. The implications are discussed and a molecular framework that guides crack-entry symbiosis in A. hypogaea is proposed.

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IPD3 Controls the Formation of Nitrogen-Fixing Symbiosomes in Pea and Medicago Spp.

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-01-11-0013 ◽

2011 ◽

Vol 24 (11) ◽

pp. 1333-1344 ◽

Cited By ~ 82

Author(s):

Evgenia Ovchinnikova ◽

Etienne-Pascal Journet ◽

Mireille Chabaud ◽

Viviane Cosson ◽

Pascal Ratet ◽

...

Keyword(s):

Pisum Sativum ◽

Lotus Japonicus ◽

Infection Thread ◽

Nodule Formation ◽

Nitrogen Fixing ◽

Cytokinin Signaling ◽

Interacting Protein ◽

Thread Formation ◽

The Common ◽

Infection Thread Formation

A successful nitrogen-fixing symbiosis requires the accommodation of rhizobial bacteria as new organelle-like structures, called symbiosomes, inside the cells of their legume hosts. Two legume mutants that are most strongly impaired in their ability to form symbiosomes are sym1/TE7 in Medicago truncatula and sym33 in Pisum sativum. We have cloned both MtSYM1 and PsSYM33 and show that both encode the recently identified interacting protein of DMI3 (IPD3), an ortholog of Lotus japonicus (Lotus) CYCLOPS. IPD3 and CYCLOPS were shown to interact with DMI3/CCaMK, which encodes a calcium- and calmodulin-dependent kinase that is an essential component of the common symbiotic signaling pathway for both rhizobial and mycorrhizal symbioses. Our data reveal a novel, key role for IPD3 in symbiosome formation and development. We show that MtIPD3 participates in but is not essential for infection thread formation and that MtIPD3 also affects DMI3-induced spontaneous nodule formation upstream of cytokinin signaling. Further, MtIPD3 appears to be required for the expression of a nodule-specific remorin, which controls proper infection thread growth and is essential for symbiosome formation.

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Nodulation Gene Mutants of Mesorhizobium loti R7A—nodZ and nolL Mutants Have Host-Specific Phenotypes on Lotus spp.

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-12-1546 ◽

2009 ◽

Vol 22 (12) ◽

pp. 1546-1554 ◽

Cited By ~ 30

Author(s):

Patsarin Rodpothong ◽

John T. Sullivan ◽

Kriangsak Songsrirote ◽

David Sumpton ◽

Kenneth W. J.-T. Cheung ◽

...

Keyword(s):

Factor Structure ◽

Infection Thread ◽

Plant Responses ◽

Nod Factors ◽

Nod Factor ◽

Mesorhizobium Loti ◽

Terminal Residue ◽

Nodulation Genes ◽

Thread Formation ◽

Infection Thread Formation

Rhizobial Nod factors induce plant responses and facilitate bacterial infection, leading to the development of nitrogen-fixing root nodules on host legumes. Nodule initiation is highly dependent on Nod-factor structure and, hence, on at least some of the nodulation genes that encode Nod-factor production. Here, we report the effects of mutations in Mesorhizobium loti R7A nodulation genes on nodulation of four Lotus spp. and on Nod-factor structure. Most mutants, including a ΔnodSΔnolO double mutant that produced Nod factors lacking the carbamoyl and possibly N-methyl groups on the nonreducing terminal residue, were unaffected for nodulation. R7AΔnodZ and R7AΔnolL mutants that produced Nod factors without the (acetyl)fucose on the reducing terminal residue had a host-specific phenotype, forming mainly uninfected nodule primordia on Lotus filicaulis and L. corniculatus and effective nodules with a delay on L. japonicus. The mutants also showed significantly reduced infection thread formation and Nin gene induction. In planta complementation experiments further suggested that the acetylfucose was important for balanced signaling in response to Nod factor by the L. japonicus NFR1/NFR5 receptors. Overall the results reveal differences in the sensitivity of plant perception with respect to signaling leading to root hair deformation and nodule primordium development versus infection thread formation and rhizobial entry.

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