Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress

Panagiota Filippou; Xavier Zarza; Chrystalla Antoniou; Toshihiro Obata; Carlos A. Villarroel; Ioannis Ganopoulos; Vaggelis Harokopos; Gholamreza Gohari; Vassilis Aidinis; Panagiotis Madesis; Anastasis Christou; Alisdair R. Fernie; Antonio F. Tiburcio; Vasileios Fotopoulos

doi:10.1016/j.csbj.2021.04.018

Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress

Panagiota Filippou, Xavier Zarza, Chrystalla Antoniou, Toshihiro Obata, Carlos A. Villarroel, Ioannis Ganopoulos, Vaggelis Harokopos, Gholamreza Gohari, Vassilis Aidinis, Panagiotis Madesis, Anastasis Christou, Alisdair R. Fernie, Antonio F. Tiburcio, Vasileios Fotopoulos

Centre for Biodiscovery

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Abstract

Salt stress is an important factor limiting plant productivity by affecting plant physiology and metabolism. To explore salt tolerance adaptive mechanisms in the model legume Medicago truncatula, we used three genotypes with differential salt-sensitivity: TN6.18 (highly sensitive), Jemalong A17 (moderately sensitive), and TN1.11 (tolerant). Cellular damage was monitored in roots and leaves 48 h after 200 mM NaCl treatment by measuring lipid peroxidation, nitric oxide, and hydrogen peroxide contents, further supported by leaf stomatal conductance and chlorophyll readings. The salt-tolerant genotype TN1.11 displayed the lowest level of oxidative damage, in contrast to the salt sensitive TN6.18, which showed the highest responses. Metabolite profiling was employed to explore the differential genotype-related responses to stress at the molecular level. The metabolic data in the salt tolerant TN1.11 roots revealed an accumulation of metabolites related to the raffinose pathway. To further investigate the sensitivity to salinity, global transcriptomic profiling using microarray analysis was carried out on the salt-stressed sensitive genotypes. In TN6.18, the transcriptomic analysis identified a lower expression of many genes related to stress signalling, not previously linked to salinity, and corresponding to the TIR-NBS-LRR gene class. Overall, this global approach contributes to gaining significant new insights into the complexity of stress adaptive mechanisms and to the identification of potential targets for crop improvement.

Original language	English
Pages (from-to)	2133-2147
Number of pages	15
Journal	Computational and Structural Biotechnology Journal
Volume	19
DOIs	https://doi.org/10.1016/j.csbj.2021.04.018
Publication status	Published - 8 Apr 2021

Bibliographical note

Funding Information:
We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F. P.F. and V.F. planned and designed the research; P.F. X.Z. C.A. T.O. A.C. and V.H. performed experiments; X.Z. T.O. C.A.V. G.G. and I.G. analyzed and interpreted the data; V.A. P.M. A.R.F. and A.F.T. were involved in discussions throughout the project; X.Z. P.F. and V.F. wrote the manuscript with contributions by all authors; V.F. supervised the project.

Funding Information:
We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F.

Publisher Copyright:
© 2021 The Author(s)

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Filippou, P., Zarza, X., Antoniou, C., Obata, T., Villarroel, C. A., Ganopoulos, I., Harokopos, V., Gohari, G., Aidinis, V., Madesis, P., Christou, A., Fernie, A. R., Tiburcio, A. F., & Fotopoulos, V. (2021). Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress. Computational and Structural Biotechnology Journal, 19, 2133-2147. https://doi.org/10.1016/j.csbj.2021.04.018

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title = "Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress",

abstract = "Salt stress is an important factor limiting plant productivity by affecting plant physiology and metabolism. To explore salt tolerance adaptive mechanisms in the model legume Medicago truncatula, we used three genotypes with differential salt-sensitivity: TN6.18 (highly sensitive), Jemalong A17 (moderately sensitive), and TN1.11 (tolerant). Cellular damage was monitored in roots and leaves 48 h after 200 mM NaCl treatment by measuring lipid peroxidation, nitric oxide, and hydrogen peroxide contents, further supported by leaf stomatal conductance and chlorophyll readings. The salt-tolerant genotype TN1.11 displayed the lowest level of oxidative damage, in contrast to the salt sensitive TN6.18, which showed the highest responses. Metabolite profiling was employed to explore the differential genotype-related responses to stress at the molecular level. The metabolic data in the salt tolerant TN1.11 roots revealed an accumulation of metabolites related to the raffinose pathway. To further investigate the sensitivity to salinity, global transcriptomic profiling using microarray analysis was carried out on the salt-stressed sensitive genotypes. In TN6.18, the transcriptomic analysis identified a lower expression of many genes related to stress signalling, not previously linked to salinity, and corresponding to the TIR-NBS-LRR gene class. Overall, this global approach contributes to gaining significant new insights into the complexity of stress adaptive mechanisms and to the identification of potential targets for crop improvement.",

author = "Panagiota Filippou and Xavier Zarza and Chrystalla Antoniou and Toshihiro Obata and Villarroel, {Carlos A.} and Ioannis Ganopoulos and Vaggelis Harokopos and Gholamreza Gohari and Vassilis Aidinis and Panagiotis Madesis and Anastasis Christou and Fernie, {Alisdair R.} and Tiburcio, {Antonio F.} and Vasileios Fotopoulos",

note = "Funding Information: We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F. P.F. and V.F. planned and designed the research; P.F. X.Z. C.A. T.O. A.C. and V.H. performed experiments; X.Z. T.O. C.A.V. G.G. and I.G. analyzed and interpreted the data; V.A. P.M. A.R.F. and A.F.T. were involved in discussions throughout the project; X.Z. P.F. and V.F. wrote the manuscript with contributions by all authors; V.F. supervised the project. Funding Information: We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F. Publisher Copyright: {\textcopyright} 2021 The Author(s)",

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language = "English",

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Filippou, P, Zarza, X, Antoniou, C, Obata, T, Villarroel, CA, Ganopoulos, I, Harokopos, V, Gohari, G, Aidinis, V, Madesis, P, Christou, A, Fernie, AR, Tiburcio, AF & Fotopoulos, V 2021, 'Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress', Computational and Structural Biotechnology Journal, vol. 19, pp. 2133-2147. https://doi.org/10.1016/j.csbj.2021.04.018

Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress. / Filippou, Panagiota; Zarza, Xavier; Antoniou, Chrystalla et al.
In: Computational and Structural Biotechnology Journal, Vol. 19, 08.04.2021, p. 2133-2147.

Research output: Contribution to journal › Article › peer-review

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T1 - Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress

AU - Filippou, Panagiota

AU - Zarza, Xavier

AU - Antoniou, Chrystalla

AU - Obata, Toshihiro

AU - Villarroel, Carlos A.

AU - Ganopoulos, Ioannis

AU - Harokopos, Vaggelis

AU - Gohari, Gholamreza

AU - Aidinis, Vassilis

AU - Madesis, Panagiotis

AU - Christou, Anastasis

AU - Fernie, Alisdair R.

AU - Tiburcio, Antonio F.

AU - Fotopoulos, Vasileios

N1 - Funding Information: We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F. P.F. and V.F. planned and designed the research; P.F. X.Z. C.A. T.O. A.C. and V.H. performed experiments; X.Z. T.O. C.A.V. G.G. and I.G. analyzed and interpreted the data; V.A. P.M. A.R.F. and A.F.T. were involved in discussions throughout the project; X.Z. P.F. and V.F. wrote the manuscript with contributions by all authors; V.F. supervised the project. Funding Information: We would like to thank Prof. Laurent Gentzbittel (ENSAT-Toulouse) for the kind provision of seeds of the Medicago genotypes. This work was supported by CUT Internal Start-up grant EX-32 to V.F. Publisher Copyright: © 2021 The Author(s)

PY - 2021/4/8

Y1 - 2021/4/8

N2 - Salt stress is an important factor limiting plant productivity by affecting plant physiology and metabolism. To explore salt tolerance adaptive mechanisms in the model legume Medicago truncatula, we used three genotypes with differential salt-sensitivity: TN6.18 (highly sensitive), Jemalong A17 (moderately sensitive), and TN1.11 (tolerant). Cellular damage was monitored in roots and leaves 48 h after 200 mM NaCl treatment by measuring lipid peroxidation, nitric oxide, and hydrogen peroxide contents, further supported by leaf stomatal conductance and chlorophyll readings. The salt-tolerant genotype TN1.11 displayed the lowest level of oxidative damage, in contrast to the salt sensitive TN6.18, which showed the highest responses. Metabolite profiling was employed to explore the differential genotype-related responses to stress at the molecular level. The metabolic data in the salt tolerant TN1.11 roots revealed an accumulation of metabolites related to the raffinose pathway. To further investigate the sensitivity to salinity, global transcriptomic profiling using microarray analysis was carried out on the salt-stressed sensitive genotypes. In TN6.18, the transcriptomic analysis identified a lower expression of many genes related to stress signalling, not previously linked to salinity, and corresponding to the TIR-NBS-LRR gene class. Overall, this global approach contributes to gaining significant new insights into the complexity of stress adaptive mechanisms and to the identification of potential targets for crop improvement.

AB - Salt stress is an important factor limiting plant productivity by affecting plant physiology and metabolism. To explore salt tolerance adaptive mechanisms in the model legume Medicago truncatula, we used three genotypes with differential salt-sensitivity: TN6.18 (highly sensitive), Jemalong A17 (moderately sensitive), and TN1.11 (tolerant). Cellular damage was monitored in roots and leaves 48 h after 200 mM NaCl treatment by measuring lipid peroxidation, nitric oxide, and hydrogen peroxide contents, further supported by leaf stomatal conductance and chlorophyll readings. The salt-tolerant genotype TN1.11 displayed the lowest level of oxidative damage, in contrast to the salt sensitive TN6.18, which showed the highest responses. Metabolite profiling was employed to explore the differential genotype-related responses to stress at the molecular level. The metabolic data in the salt tolerant TN1.11 roots revealed an accumulation of metabolites related to the raffinose pathway. To further investigate the sensitivity to salinity, global transcriptomic profiling using microarray analysis was carried out on the salt-stressed sensitive genotypes. In TN6.18, the transcriptomic analysis identified a lower expression of many genes related to stress signalling, not previously linked to salinity, and corresponding to the TIR-NBS-LRR gene class. Overall, this global approach contributes to gaining significant new insights into the complexity of stress adaptive mechanisms and to the identification of potential targets for crop improvement.

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U2 - 10.1016/j.csbj.2021.04.018

DO - 10.1016/j.csbj.2021.04.018

M3 - Article

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SN - 2001-0370

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EP - 2147

JO - Computational and Structural Biotechnology Journal

JF - Computational and Structural Biotechnology Journal

ER -

Systems biology reveals key tissue-specific metabolic and transcriptional signatures involved in the response of Medicago truncatula plant genotypes to salt stress

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