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Deciphering the regulatory networks involved in mild and severe salt stress responses in the roots of wild grapevine Vitis vinifera spp. sylvestris

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Abstract

Transcriptional regulatory networks are pivotal components of plant’s response to salt stress. However, plant adaptation strategies varied as a function of stress intensity, which is mainly modulated by climate change. Here, we determined the gene regulatory networks based on transcription factor (TF) TF_gene co-expression, using two transcriptomic data sets generated from the salt-tolerant “Tebaba” roots either treated with 50 mM NaCl (mild stress) or 150 mM NaCl (severe stress). The analysis of these regulatory networks identified specific TFs as key regulatory hubs as evidenced by their multiple interactions with different target genes related to stress response. Indeed, under mild stress, NAC and bHLH TFs were identified as central hubs regulating nitrogen storage process. Moreover, HSF TFs were revealed as a regulatory hub regulating various aspects of cellular metabolism including flavonoid biosynthesis, protein processing, phenylpropanoid metabolism, galactose metabolism, and heat shock proteins. These processes are essentially linked to short-term acclimatization under mild salt stress. This was further consolidated by the protein–protein interaction (PPI) network analysis showing structural and plant growth adjustment. Conversely, under severe salt stress, dramatic metabolic changes were observed leading to novel TF members including MYB family as regulatory hubs controlling isoflavonoid biosynthesis, oxidative stress response, abscisic acid signaling pathway, and proteolysis. The PPI network analysis also revealed deeper stress defense changes aiming to restore plant metabolic homeostasis when facing severe salt stress. Overall, both the gene co-expression and PPI network provided valuable insights on key transcription factor hubs that can be employed as candidates for future genetic crop engineering programs.

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Data availability

The RNA-seq datasets by using the Illumina-Hiseq platform are available from the NCBI Sequence Read Archive database (SRA; http://www.ncbi.nlm.nih.gov/sra) under project number accession PRJNA507974. The cDNA libraries were obtained from the controls and their respective salt-stress of 50 mM NaCl and 150 mM NaCl for 24 h with two biological replicates, respectively.

Abbreviations

ABA:

Abscisic acid

HSP:

Heat shock protein

ER:

Endoplasmic reticulum

TF:

Transcription factor

ROS:

Reactive oxygen species

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Funding

This research was carried out as part of the Tunisian National Research Program (CP2019-2022) of the Laboratory of Plant Molecular Physiology at the Centre of Biotechnology of Borj-Cedria, funded by the Tunisian Ministry of Higher Education and Scientific Research.

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Authors and Affiliations

  1. Laboratory of Plant Molecular Physiology, Centre of Biotechnology of Borj-Cedria, BP. 901, Hammam-Lif, Tunisia

    Samia Daldoul, Faouzia Hanzouli, Ahmed Mliki & Mahmoud Gargouri

  2. Faculty of Sciences of Tunis, University Tunis El-Manar, El Manar II, 2092, Tunis, Tunisia

    Faouzia Hanzouli

  3. Laboratory of Legumes and Sustainable Agrosystems, Centre of Biotechnology of Borj-Cedria, B.P 901, 2050, Hammam-Lif, Tunisia

    Hatem Boubakri

  4. Molecular Cell Biology, Botanical Institute, Karlsruhe Institute of Technology, Karlsruhe, Germany

    Peter Nick

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  1. Samia Daldoul
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  4. Peter Nick
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  6. Mahmoud Gargouri
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Contributions

S.D. and M.G. conceived and designed the study. F.H. and S.D performed the physiological analyses. S.D. performed the molecular analyses. M.G. performed the bioinformatic and statistical analyses. H.B. performed PPI interaction networks. S.D. and M.G wrote the original draft of the manuscript. All authors read and contribute to the review and editing of the final manuscript.

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Correspondence to Samia Daldoul or Mahmoud Gargouri.

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Daldoul, S., Hanzouli, F., Boubakri, H. et al. Deciphering the regulatory networks involved in mild and severe salt stress responses in the roots of wild grapevine Vitis vinifera spp. sylvestris. Protoplasma 261, 447–462 (2024). https://doi.org/10.1007/s00709-023-01908-9

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  • DOI: https://doi.org/10.1007/s00709-023-01908-9

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