Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides

Mingkee Achom; Proyash Roy; Beatriz Lagunas; Emma Picot; Luke Richards; Roxanna Bonyadi-Pour; Alonso J. Pardal; Laura Baxter; Bethany L. Richmond; Nadine Aschauer; Eleanor M. Fletcher; Monique Rowson; Joseph Blackwell; Charlotte Rich-Griffin; Kirankumar S Mysore; Jiangqi Wen; Sascha Ott; Isabelle A. Carré; Miriam L. Gifford

doi:10.1093/jxb/erab526

Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides

Mingkee Achom, Proyash Roy, Beatriz Lagunas, Emma Picot, Luke Richards, Roxanna Bonyadi-Pour, Alonso J. Pardal, Laura Baxter, Bethany L. Richmond, Nadine Aschauer, Eleanor M. Fletcher, Monique Rowson, Joseph Blackwell, Charlotte Rich-Griffin, Kirankumar S Mysore, Jiangqi Wen, Sascha Ott, Isabelle A. Carré, Miriam L. Gifford

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Abstract

Legumes house nitrogen-fixing endosymbiotic rhizobia in specialized polyploid cells within root nodules, which undergo tightly regulated metabolic activity. By carrying out expression analysis of transcripts over time in Medicago truncatula nodules, we found that the circadian clock enables coordinated control of metabolic and regulatory processes linked to nitrogen fixation. This involves the circadian clock-associated transcription factor LATE ELONGATED HYPOCOTYL (LHY), with lhy mutants being affected in nodulation. Rhythmic transcripts in root nodules include a subset of nodule-specific cysteine-rich peptides (NCRs) that have the LHY-bound conserved evening element in their promoters. Until now, studies have suggested that NCRs act to regulate bacteroid differentiation and keep the rhizobial population in check. However, these conclusions came from the study of a few members of this very large gene family that has complex diversified spatio-temporal expression. We suggest that rhythmic expression of NCRs may be important for temporal coordination of bacterial activity with the rhythms of the plant host, in order to ensure optimal symbiosis.

Original language	English
Pages (from-to)	2142–2156
Number of pages	15
Journal	Journal of Experimental Botany
Volume	73
Issue number	3
Early online date	1 Dec 2021
DOIs	https://doi.org/10.1093/jxb/erab526
Publication status	Published - 5 Apr 2022
Externally published	Yes

Bibliographical note

The raw RNA-seq data that support the findings of this study are openly available in the NCBI SRA database (PRJNA634620). The datasets associated with this paper are openly available at the Dryad Digital Repository https://doi.org/10.5061/dryad.9s4mw6mgg; Achom et al., 2022).

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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Achom, M., Roy, P., Lagunas, B., Picot, E., Richards, L., Bonyadi-Pour, R., Pardal, A. J., Baxter, L., Richmond, B. L., Aschauer, N., Fletcher, E. M., Rowson, M., Blackwell, J., Rich-Griffin, C., Mysore, K. S., Wen, J., Ott, S., Carré, I. A., & Gifford, M. L. (2022). Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides. Journal of Experimental Botany, 73(3), 2142–2156. https://doi.org/10.1093/jxb/erab526

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title = "Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides",

abstract = "Legumes house nitrogen-fixing endosymbiotic rhizobia in specialized polyploid cells within root nodules, which undergo tightly regulated metabolic activity. By carrying out expression analysis of transcripts over time in Medicago truncatula nodules, we found that the circadian clock enables coordinated control of metabolic and regulatory processes linked to nitrogen fixation. This involves the circadian clock-associated transcription factor LATE ELONGATED HYPOCOTYL (LHY), with lhy mutants being affected in nodulation. Rhythmic transcripts in root nodules include a subset of nodule-specific cysteine-rich peptides (NCRs) that have the LHY-bound conserved evening element in their promoters. Until now, studies have suggested that NCRs act to regulate bacteroid differentiation and keep the rhizobial population in check. However, these conclusions came from the study of a few members of this very large gene family that has complex diversified spatio-temporal expression. We suggest that rhythmic expression of NCRs may be important for temporal coordination of bacterial activity with the rhythms of the plant host, in order to ensure optimal symbiosis.",

author = "Mingkee Achom and Proyash Roy and Beatriz Lagunas and Emma Picot and Luke Richards and Roxanna Bonyadi-Pour and Pardal, {Alonso J.} and Laura Baxter and Richmond, {Bethany L.} and Nadine Aschauer and Fletcher, {Eleanor M.} and Monique Rowson and Joseph Blackwell and Charlotte Rich-Griffin and Mysore, {Kirankumar S} and Jiangqi Wen and Sascha Ott and Carr{\'e}, {Isabelle A.} and Gifford, {Miriam L.}",

note = "The raw RNA-seq data that support the findings of this study are openly available in the NCBI SRA database (PRJNA634620). The datasets associated with this paper are openly available at the Dryad Digital Repository https://doi.org/10.5061/dryad.9s4mw6mgg; Achom et al., 2022). {\textcopyright} The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.",

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doi = "10.1093/jxb/erab526",

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Achom, M, Roy, P, Lagunas, B, Picot, E, Richards, L, Bonyadi-Pour, R, Pardal, AJ, Baxter, L, Richmond, BL, Aschauer, N, Fletcher, EM, Rowson, M, Blackwell, J, Rich-Griffin, C, Mysore, KS, Wen, J, Ott, S, Carré, IA & Gifford, ML 2022, 'Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides', Journal of Experimental Botany, vol. 73, no. 3, pp. 2142–2156. https://doi.org/10.1093/jxb/erab526

TY - JOUR

T1 - Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides

AU - Achom, Mingkee

AU - Roy, Proyash

AU - Lagunas, Beatriz

AU - Picot, Emma

AU - Richards, Luke

AU - Bonyadi-Pour, Roxanna

AU - Pardal, Alonso J.

AU - Baxter, Laura

AU - Richmond, Bethany L.

AU - Aschauer, Nadine

AU - Fletcher, Eleanor M.

AU - Rowson, Monique

AU - Blackwell, Joseph

AU - Rich-Griffin, Charlotte

AU - Mysore, Kirankumar S

AU - Wen, Jiangqi

AU - Ott, Sascha

AU - Carré, Isabelle A.

AU - Gifford, Miriam L.

N1 - The raw RNA-seq data that support the findings of this study are openly available in the NCBI SRA database (PRJNA634620). The datasets associated with this paper are openly available at the Dryad Digital Repository https://doi.org/10.5061/dryad.9s4mw6mgg; Achom et al., 2022). © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

PY - 2022/4/5

Y1 - 2022/4/5

N2 - Legumes house nitrogen-fixing endosymbiotic rhizobia in specialized polyploid cells within root nodules, which undergo tightly regulated metabolic activity. By carrying out expression analysis of transcripts over time in Medicago truncatula nodules, we found that the circadian clock enables coordinated control of metabolic and regulatory processes linked to nitrogen fixation. This involves the circadian clock-associated transcription factor LATE ELONGATED HYPOCOTYL (LHY), with lhy mutants being affected in nodulation. Rhythmic transcripts in root nodules include a subset of nodule-specific cysteine-rich peptides (NCRs) that have the LHY-bound conserved evening element in their promoters. Until now, studies have suggested that NCRs act to regulate bacteroid differentiation and keep the rhizobial population in check. However, these conclusions came from the study of a few members of this very large gene family that has complex diversified spatio-temporal expression. We suggest that rhythmic expression of NCRs may be important for temporal coordination of bacterial activity with the rhythms of the plant host, in order to ensure optimal symbiosis.

AB - Legumes house nitrogen-fixing endosymbiotic rhizobia in specialized polyploid cells within root nodules, which undergo tightly regulated metabolic activity. By carrying out expression analysis of transcripts over time in Medicago truncatula nodules, we found that the circadian clock enables coordinated control of metabolic and regulatory processes linked to nitrogen fixation. This involves the circadian clock-associated transcription factor LATE ELONGATED HYPOCOTYL (LHY), with lhy mutants being affected in nodulation. Rhythmic transcripts in root nodules include a subset of nodule-specific cysteine-rich peptides (NCRs) that have the LHY-bound conserved evening element in their promoters. Until now, studies have suggested that NCRs act to regulate bacteroid differentiation and keep the rhizobial population in check. However, these conclusions came from the study of a few members of this very large gene family that has complex diversified spatio-temporal expression. We suggest that rhythmic expression of NCRs may be important for temporal coordination of bacterial activity with the rhythms of the plant host, in order to ensure optimal symbiosis.

UR - https://academic.oup.com/jxb/article/73/7/2142/6447273

U2 - 10.1093/jxb/erab526

DO - 10.1093/jxb/erab526

M3 - Article

SN - 0022-0957

VL - 73

SP - 2142

EP - 2156

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

IS - 3

ER -

Plant circadian clock control of Medicago truncatula nodulation via regulation of nodule cysteine-rich peptides

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