A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

Anna Malolepszy; Simon Kelly; Kasper Kildegaard Sørensen; Euan Kevin James; Christina Kalisch; Zoltan Bozsoki; Michael Panting; Stig U Andersen; Shusei Sato; Ke Tao; Dorthe Bødker Jensen; Maria Vinther; Noor De Jong; Lene Heegaard Madsen; Yosuke Umehara; Kira Gysel; Mette U Berentsen; Mickael Blaise; Knud Jørgen Jensen; Mikkel B Thygesen; Niels Sandal; Kasper Røjkjær Andersen; Simona Radutoiu

doi:10.7554/eLife.38874

A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

Anna Malolepszy, Simon Kelly, Kasper Kildegaard Sørensen, Euan Kevin James, Christina Kalisch, Zoltan Bozsoki, Michael Panting, Stig U Andersen, Shusei Sato, Ke Tao, Dorthe Bødker Jensen, Maria Vinther, Noor De Jong, Lene Heegaard Madsen, Yosuke Umehara, Kira Gysel, Mette U Berentsen, Mickael Blaise, Knud Jørgen Jensen, Mikkel B ThygesenNiels Sandal, Kasper Røjkjær Andersen, Simona Radutoiu

Department of Chemistry

14 Citations (Scopus)

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Abstract

Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.

Original language	English
Article number	e38874
Journal	eLife
Volume	7
Pages (from-to)	1-17
Number of pages	17
ISSN	2050-084X
DOIs	https://doi.org/10.7554/eLife.38874
Publication status	Published - Oct 2018

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10.7554/eLife.38874Licence: CC BY

A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosisFinal published version, 4.34 MBLicence: CC BY

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Malolepszy, A., Kelly, S., Sørensen, K. K., James, E. K., Kalisch, C., Bozsoki, Z., Panting, M., Andersen, S. U., Sato, S., Tao, K., Jensen, D. B., Vinther, M., Jong, N. D., Madsen, L. H., Umehara, Y., Gysel, K., Berentsen, M. U., Blaise, M., Jensen, K. J., ... Radutoiu, S. (2018). A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis. eLife, 7, 1-17. Article e38874. https://doi.org/10.7554/eLife.38874

Malolepszy, A, Kelly, S, Sørensen, KK, James, EK, Kalisch, C, Bozsoki, Z, Panting, M, Andersen, SU, Sato, S, Tao, K, Jensen, DB, Vinther, M, Jong, ND, Madsen, LH, Umehara, Y, Gysel, K, Berentsen, MU, Blaise, M, Jensen, KJ , Thygesen, MB, Sandal, N, Andersen, KR & Radutoiu, S 2018, 'A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis', eLife, vol. 7, e38874, pp. 1-17. https://doi.org/10.7554/eLife.38874

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title = "A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis",

abstract = "Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.",

author = "Anna Malolepszy and Simon Kelly and S{\o}rensen, {Kasper Kildegaard} and James, {Euan Kevin} and Christina Kalisch and Zoltan Bozsoki and Michael Panting and Andersen, {Stig U} and Shusei Sato and Ke Tao and Jensen, {Dorthe B{\o}dker} and Maria Vinther and Jong, {Noor De} and Madsen, {Lene Heegaard} and Yosuke Umehara and Kira Gysel and Berentsen, {Mette U} and Mickael Blaise and Jensen, {Knud J{\o}rgen} and Thygesen, {Mikkel B} and Niels Sandal and Andersen, {Kasper R{\o}jkj{\ae}r} and Simona Radutoiu",

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AU - Malolepszy, Anna

AU - Kelly, Simon

AU - Sørensen, Kasper Kildegaard

AU - James, Euan Kevin

AU - Kalisch, Christina

AU - Bozsoki, Zoltan

AU - Panting, Michael

AU - Andersen, Stig U

AU - Sato, Shusei

AU - Tao, Ke

AU - Jensen, Dorthe Bødker

AU - Vinther, Maria

AU - Jong, Noor De

AU - Madsen, Lene Heegaard

AU - Umehara, Yosuke

AU - Gysel, Kira

AU - Berentsen, Mette U

AU - Blaise, Mickael

AU - Jensen, Knud Jørgen

AU - Thygesen, Mikkel B

AU - Sandal, Niels

AU - Andersen, Kasper Røjkjær

AU - Radutoiu, Simona

PY - 2018/10

Y1 - 2018/10

N2 - Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.

AB - Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.

U2 - 10.7554/eLife.38874

DO - 10.7554/eLife.38874

M3 - Journal article

C2 - 30284535

SN - 2050-084X

VL - 7

SP - 1

EP - 17

JO - eLife

JF - eLife

M1 - e38874

ER -

A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

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