Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Sebastián Acosta-Jurado; Dulce Nombre Rodríguez-Navarro; Yasuyuki Kawaharada; Miguel A. Rodríguez-Carvajal; Antonio Gil-Serrano; María E. Soria-Díaz; Francisco Pérez-Montaño; Juan Fernández-Perea; Yanbo Niu; Cynthia Alias-Villegas; Irene Jiménez-Guerrero; Pilar Navarro-Gómez; Francisco Javier López-Baena; Simon Kelly; Niels Sandal; Jens Stougaard; José E. Ruiz-Sainz; José María Vinardell

doi:10.1111/1462-2920.14584

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

Sebastián Acosta-Jurado, Dulce Nombre Rodríguez-Navarro, Yasuyuki Kawaharada, Miguel A. Rodríguez-Carvajal, Antonio Gil-Serrano, María E. Soria-Díaz, Francisco Pérez-Montaño, Juan Fernández-Perea, Yanbo Niu, Cynthia Alias-Villegas, Irene Jiménez-Guerrero, Pilar Navarro-Gómez, Francisco Javier López-Baena, Simon Kelly, Niels Sandal, Jens Stougaard, José E. Ruiz-Sainz, José María Vinardell^*

^*Corresponding author for this work

Department of Molecular Biology and Genetics - Plant Molecular Biology

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

27 Citations (Scopus)

Abstract

Sinorhizobium fredii HH103 Rif ^R , a broad-host-range rhizobial strain, forms ineffective nodules with Lotus japonicus but induces nitrogen-fixing nodules in Lotus burttii roots that are infected by intercellular entry. Here we show that HH103 Rif ^R nolR or nodD2 mutants gain the ability to induce infection thread formation and to form nitrogen-fixing nodules in L. japonicus Gifu. Microscopy studies showed that the mode of infection of L. burttii roots by the nodD2 and nolR mutants switched from intercellular entry to infection threads (ITs). In the presence of the isoflavone genistein, both mutants overproduced Nod-factors. Transcriptomic analyses showed that, in the presence of Lotus japonicus Gifu root exudates, genes related to Nod factors production were overexpressed in both mutants in comparison to HH103 Rif ^R . Complementation of the nodD2 and nolR mutants provoked a decrease in Nod-factor production, the incapacity to form nitrogen-fixing nodules with L. japonicus Gifu and restored the intercellular way of infection in L. burttii. Thus, the capacity of S. fredii HH103 Rif ^R nodD2 and nolR mutants to infect L. burttii and L. japonicus Gifu by ITs and fix nitrogen L. japonicus Gifu might be correlated with Nod-factor overproduction, although other bacterial symbiotic signals could also be involved.

Original language	English
Journal	Environmental Microbiology
Volume	21
Issue	5
Pages (from-to)	1718-1739
Number of pages	22
ISSN	1462-2912
DOIs	https://doi.org/10.1111/1462-2920.14584
Publication status	Published - 1 May 2019

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Acosta-Jurado, S., Rodríguez-Navarro, D. N., Kawaharada, Y., Rodríguez-Carvajal, M. A., Gil-Serrano, A., Soria-Díaz, M. E., Pérez-Montaño, F., Fernández-Perea, J., Niu, Y., Alias-Villegas, C., Jiménez-Guerrero, I., Navarro-Gómez, P., López-Baena, F. J., Kelly, S., Sandal, N., Stougaard, J., Ruiz-Sainz, J. E., & Vinardell, J. M. (2019). Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii. Environmental Microbiology, 21(5), 1718-1739. https://doi.org/10.1111/1462-2920.14584

@article{a8cba7082dd844d089ecd9ad6aac9de0,

title = "Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii",

abstract = " Sinorhizobium fredii HH103 Rif R , a broad-host-range rhizobial strain, forms ineffective nodules with Lotus japonicus but induces nitrogen-fixing nodules in Lotus burttii roots that are infected by intercellular entry. Here we show that HH103 Rif R nolR or nodD2 mutants gain the ability to induce infection thread formation and to form nitrogen-fixing nodules in L. japonicus Gifu. Microscopy studies showed that the mode of infection of L. burttii roots by the nodD2 and nolR mutants switched from intercellular entry to infection threads (ITs). In the presence of the isoflavone genistein, both mutants overproduced Nod-factors. Transcriptomic analyses showed that, in the presence of Lotus japonicus Gifu root exudates, genes related to Nod factors production were overexpressed in both mutants in comparison to HH103 Rif R . Complementation of the nodD2 and nolR mutants provoked a decrease in Nod-factor production, the incapacity to form nitrogen-fixing nodules with L. japonicus Gifu and restored the intercellular way of infection in L. burttii. Thus, the capacity of S. fredii HH103 Rif R nodD2 and nolR mutants to infect L. burttii and L. japonicus Gifu by ITs and fix nitrogen L. japonicus Gifu might be correlated with Nod-factor overproduction, although other bacterial symbiotic signals could also be involved. ",

author = "Sebasti{\'a}n Acosta-Jurado and Rodr{\'i}guez-Navarro, {Dulce Nombre} and Yasuyuki Kawaharada and Rodr{\'i}guez-Carvajal, {Miguel A.} and Antonio Gil-Serrano and Soria-D{\'i}az, {Mar{\'i}a E.} and Francisco P{\'e}rez-Monta{\~n}o and Juan Fern{\'a}ndez-Perea and Yanbo Niu and Cynthia Alias-Villegas and Irene Jim{\'e}nez-Guerrero and Pilar Navarro-G{\'o}mez and L{\'o}pez-Baena, {Francisco Javier} and Simon Kelly and Niels Sandal and Jens Stougaard and Ruiz-Sainz, {Jos{\'e} E.} and Vinardell, {Jos{\'e} Mar{\'i}a}",

year = "2019",

month = may,

day = "1",

doi = "10.1111/1462-2920.14584",

language = "English",

volume = "21",

pages = "1718--1739",

journal = "Environmental Microbiology",

issn = "1462-2912",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "5",

}

Acosta-Jurado, S, Rodríguez-Navarro, DN, Kawaharada, Y, Rodríguez-Carvajal, MA, Gil-Serrano, A, Soria-Díaz, ME, Pérez-Montaño, F, Fernández-Perea, J, Niu, Y, Alias-Villegas, C, Jiménez-Guerrero, I, Navarro-Gómez, P, López-Baena, FJ, Kelly, S, Sandal, N , Stougaard, J, Ruiz-Sainz, JE & Vinardell, JM 2019, 'Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii', Environmental Microbiology, vol. 21, no. 5, pp. 1718-1739. https://doi.org/10.1111/1462-2920.14584

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii. / Acosta-Jurado, Sebastián; Rodríguez-Navarro, Dulce Nombre; Kawaharada, Yasuyuki et al.
In: Environmental Microbiology, Vol. 21, No. 5, 01.05.2019, p. 1718-1739.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

AU - Acosta-Jurado, Sebastián

AU - Rodríguez-Navarro, Dulce Nombre

AU - Kawaharada, Yasuyuki

AU - Rodríguez-Carvajal, Miguel A.

AU - Gil-Serrano, Antonio

AU - Soria-Díaz, María E.

AU - Pérez-Montaño, Francisco

AU - Fernández-Perea, Juan

AU - Niu, Yanbo

AU - Alias-Villegas, Cynthia

AU - Jiménez-Guerrero, Irene

AU - Navarro-Gómez, Pilar

AU - López-Baena, Francisco Javier

AU - Kelly, Simon

AU - Sandal, Niels

AU - Stougaard, Jens

AU - Ruiz-Sainz, José E.

AU - Vinardell, José María

PY - 2019/5/1

Y1 - 2019/5/1

N2 - Sinorhizobium fredii HH103 Rif R , a broad-host-range rhizobial strain, forms ineffective nodules with Lotus japonicus but induces nitrogen-fixing nodules in Lotus burttii roots that are infected by intercellular entry. Here we show that HH103 Rif R nolR or nodD2 mutants gain the ability to induce infection thread formation and to form nitrogen-fixing nodules in L. japonicus Gifu. Microscopy studies showed that the mode of infection of L. burttii roots by the nodD2 and nolR mutants switched from intercellular entry to infection threads (ITs). In the presence of the isoflavone genistein, both mutants overproduced Nod-factors. Transcriptomic analyses showed that, in the presence of Lotus japonicus Gifu root exudates, genes related to Nod factors production were overexpressed in both mutants in comparison to HH103 Rif R . Complementation of the nodD2 and nolR mutants provoked a decrease in Nod-factor production, the incapacity to form nitrogen-fixing nodules with L. japonicus Gifu and restored the intercellular way of infection in L. burttii. Thus, the capacity of S. fredii HH103 Rif R nodD2 and nolR mutants to infect L. burttii and L. japonicus Gifu by ITs and fix nitrogen L. japonicus Gifu might be correlated with Nod-factor overproduction, although other bacterial symbiotic signals could also be involved.

AB - Sinorhizobium fredii HH103 Rif R , a broad-host-range rhizobial strain, forms ineffective nodules with Lotus japonicus but induces nitrogen-fixing nodules in Lotus burttii roots that are infected by intercellular entry. Here we show that HH103 Rif R nolR or nodD2 mutants gain the ability to induce infection thread formation and to form nitrogen-fixing nodules in L. japonicus Gifu. Microscopy studies showed that the mode of infection of L. burttii roots by the nodD2 and nolR mutants switched from intercellular entry to infection threads (ITs). In the presence of the isoflavone genistein, both mutants overproduced Nod-factors. Transcriptomic analyses showed that, in the presence of Lotus japonicus Gifu root exudates, genes related to Nod factors production were overexpressed in both mutants in comparison to HH103 Rif R . Complementation of the nodD2 and nolR mutants provoked a decrease in Nod-factor production, the incapacity to form nitrogen-fixing nodules with L. japonicus Gifu and restored the intercellular way of infection in L. burttii. Thus, the capacity of S. fredii HH103 Rif R nodD2 and nolR mutants to infect L. burttii and L. japonicus Gifu by ITs and fix nitrogen L. japonicus Gifu might be correlated with Nod-factor overproduction, although other bacterial symbiotic signals could also be involved.

UR - http://www.scopus.com/inward/record.url?scp=85065022824&partnerID=8YFLogxK

U2 - 10.1111/1462-2920.14584

DO - 10.1111/1462-2920.14584

M3 - Journal article

C2 - 30839140

AN - SCOPUS:85065022824

SN - 1462-2912

VL - 21

SP - 1718

EP - 1739

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 5

ER -

Sinorhizobium fredii HH103 nolR and nodD2 mutants gain capacity for infection thread invasion of Lotus japonicus Gifu and Lotus burttii

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