Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti

Keisuke Yokota; Eigo Fukai; Lene H Madsen; Anna Jurkiewicz; Paloma Rueda; Simona Radutoiu; Mark Held; Md Shakhawat Hossain; Krzysztof Szczyglowski; Giulia Morieri; Giles E D Oldroyd; J Allan Downie; Mette W Nielsen; Anna Maria Rusek; Shusei Sato; Satoshi Tabata; Euan K James; Hiroshi Oyaizu; Niels Sandal; Jens Stougaard

doi:10.1105/tpc.108.063693

Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti

Keisuke Yokota, Eigo Fukai, Lene H Madsen, Anna Jurkiewicz, Paloma Rueda, Simona Radutoiu, Mark Held, Md Shakhawat Hossain, Krzysztof Szczyglowski, Giulia Morieri, Giles E D Oldroyd, J Allan Downie, Mette W Nielsen, Anna Maria Rusek, Shusei Sato, Satoshi Tabata, Euan K James, Hiroshi Oyaizu, Niels Sandal, Jens Stougaard

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Abstract

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.

Original language	English
Journal	Plant Cell
ISSN	1040-4651
DOIs	https://doi.org/10.1105/tpc.108.063693
Publication status	Published - 2009

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Yokota, K., Fukai, E., Madsen, L. H., Jurkiewicz, A., Rueda, P., Radutoiu, S., Held, M., Hossain, M. S., Szczyglowski, K., Morieri, G., Oldroyd, G. E. D., Downie, J. A., Nielsen, M. W., Rusek, A. M., Sato, S., Tabata, S., James, E. K., Oyaizu, H., Sandal, N., & Stougaard, J. (2009). Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti. Plant Cell. https://doi.org/10.1105/tpc.108.063693

@article{4db3d36008bf11de8317000ea68e967b,

title = "Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti",

abstract = "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.",

author = "Keisuke Yokota and Eigo Fukai and Madsen, {Lene H} and Anna Jurkiewicz and Paloma Rueda and Simona Radutoiu and Mark Held and Hossain, {Md Shakhawat} and Krzysztof Szczyglowski and Giulia Morieri and Oldroyd, {Giles E D} and Downie, {J Allan} and Nielsen, {Mette W} and Rusek, {Anna Maria} and Shusei Sato and Satoshi Tabata and James, {Euan K} and Hiroshi Oyaizu and Niels Sandal and Jens Stougaard",

year = "2009",

doi = "10.1105/tpc.108.063693",

language = "English",

journal = "Plant Cell",

issn = "1040-4651",

publisher = "American Society of Plant Biologists",

}

Yokota, K, Fukai, E, Madsen, LH, Jurkiewicz, A, Rueda, P, Radutoiu, S, Held, M, Hossain, MS, Szczyglowski, K, Morieri, G, Oldroyd, GED, Downie, JA, Nielsen, MW, Rusek, AM, Sato, S, Tabata, S, James, EK, Oyaizu, H, Sandal, N & Stougaard, J 2009, 'Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti', Plant Cell. https://doi.org/10.1105/tpc.108.063693

TY - JOUR

T1 - Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti

AU - Yokota, Keisuke

AU - Fukai, Eigo

AU - Madsen, Lene H

AU - Jurkiewicz, Anna

AU - Rueda, Paloma

AU - Radutoiu, Simona

AU - Held, Mark

AU - Hossain, Md Shakhawat

AU - Szczyglowski, Krzysztof

AU - Morieri, Giulia

AU - Oldroyd, Giles E D

AU - Downie, J Allan

AU - Nielsen, Mette W

AU - Rusek, Anna Maria

AU - Sato, Shusei

AU - Tabata, Satoshi

AU - James, Euan K

AU - Oyaizu, Hiroshi

AU - Sandal, Niels

AU - Stougaard, Jens

PY - 2009

Y1 - 2009

N2 - 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.

AB - 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.

U2 - 10.1105/tpc.108.063693

DO - 10.1105/tpc.108.063693

M3 - Journal article

C2 - 19136645

SN - 1040-4651

JO - Plant Cell

JF - Plant Cell

ER -

Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti

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