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At the core of salinity: convergent and divergent transcriptome response pathways to neutral and alkaline salinity in natural populations of Arabidopsis thaliana

View ORCID ProfileMaria Almira-Casellas, View ORCID ProfileSílvia Busoms, View ORCID ProfileLaura Pérez-Martín, View ORCID ProfileGlòria Escolà, View ORCID ProfileÁlvaro López-Valiñas, View ORCID ProfileAntoni Garcia-Molina, View ORCID ProfileMercè Llugany, View ORCID ProfileCharlotte Poschenrieder
doi: https://doi.org/10.1101/2023.02.05.527167
Maria Almira-Casellas
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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  • ORCID record for Maria Almira-Casellas
Sílvia Busoms
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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  • For correspondence: merce.llugany@uab.cat silvia.busoms@uab.cat
Laura Pérez-Martín
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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Glòria Escolà
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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Álvaro López-Valiñas
2Unitat Mixta d’Investigació IRTA-UAB en Sanitat Animal, Centre de Recerca en Sanitat Animal (CReSA), Campus UAB, 08193 Bellaterra, Spain
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Antoni Garcia-Molina
3Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Barcelona, Spain
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  • ORCID record for Antoni Garcia-Molina
Mercè Llugany
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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  • For correspondence: merce.llugany@uab.cat silvia.busoms@uab.cat
Charlotte Poschenrieder
1Plant Physiology Unit, Biosciences Faculty, Universitat Autònoma de Barcelona (UAB), 08193 Bellaterra, Spain
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Abstract

More than 70% of land’s cultivated area is affected by alkaline salinity stress. As 98% of plants are glycophytes – unable to successfully reproduce under salinity – our previous research focused on comparative studies of Arabidopsis thaliana demes with differential performance under neutral and alkaline salinity (neuSAL and alkSAL) due to local adaptation processes. Here, an integrated analysis on leaf tissue was performed, including physiological indicators, nutritional status, endogenous phytohormonal concentration and transcriptome profiling, to further understand differences in molecular mechanisms underlying neuSAL and alkSAL responses. The results support that alkSAL is more detrimental to plant performance than neuSAL and indicate higher sensitivity to alkSAL in demes locally adapted to coastal siliceous soils. A decreased internal Fe use efficiency in coastal demes under alkSAL is proposed to be the driver of their enhanced sensitivity, and sequence variation at β-CA1 and α-CA1 locus is hypothesized to contribute to the imbalance of Fe homeostasis. Dissection on the down-regulated transcripts shared by neuSAL and alkSAL confirmed enhanced inhibition of central features on primary and secondary metabolism in coastal individuals under alkSAL. The cell wall and vacuolar β-galactosidase BGAL4 was revealed as a candidate for conferring tolerance to neuSAL by favoring stress-regulated cell wall rearrangement, but not to alkSAL, probably due to pH-restricted enzymatic activity. In addition, differential modulation of endogenous phytohormonal cues was reported among salinity types and demes, by which higher alteration of the auxinic, ethylene and jasmonic acid signaling pathways was exerted by alkSAL but sustained ABA biosynthesis was detected only in coastal plants under neuSAL. Weighted correlation network analysis (WGCNA) confirmed the involvement of the identified candidate genes in co-expression modules significantly correlating with favorable responses to neuSAL and alkSAL. Overall, the present study provides useful insights into key targets for breeding improvement in alkaline saline soils.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Submitting author: ORCID and e-mail of all authors: Maria José Almira Casellas; 0000-0002-4035-8766; mariajose.almira{at}uab.cat, Sílvia Busoms; 0000-0002-9917-7118; silvia.busoms{at}uab.cat, Laura Pérez-Martín; 0000-0001-6066-3939; laura.perezmartin{at}unige.ch, Glòria Escolà; 0000-0003-4231-4334; gloria.escola{at}uab.cat, Álvaro López-Valiñas; 0000-0002-7492-5108; alvaro.lopezv{at}irta.cat, Antoni Garcia; 0000-0002-7790-9736; antoni.garcia{at}cragenomica.es, Mercè Llugany: 0000-0002-9940-0383; merce.llugany{at}uab.cat, Charlotte Poschenrieder: ORCID 0000-0002-3818-0874; charlotte.poschentrieder{at}uab.es

  • As suggested, we have included new physiological data (relative leaf water content) and increased the number of replicates for the growth, nutrition, chlorophyll fluorescence and hormone concentration (n=6). Initially, we showed the data for the particular plants that were used for the transcriptome analysis (n=3). However, all the plants from the experiment (n=6) were monitored, harvested, and keept at −80 C and have been included now. However, no new experimental setups were implemented in order that the transcriptomic data would remain comparable. New figures, supplementary datasets and discussion are provided in this re-submission, which further address the long term plant responses to salinity at the physiological and transcriptomic level.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 19, 2023.
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At the core of salinity: convergent and divergent transcriptome response pathways to neutral and alkaline salinity in natural populations of Arabidopsis thaliana
Maria Almira-Casellas, Sílvia Busoms, Laura Pérez-Martín, Glòria Escolà, Álvaro López-Valiñas, Antoni Garcia-Molina, Mercè Llugany, Charlotte Poschenrieder
bioRxiv 2023.02.05.527167; doi: https://doi.org/10.1101/2023.02.05.527167
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At the core of salinity: convergent and divergent transcriptome response pathways to neutral and alkaline salinity in natural populations of Arabidopsis thaliana
Maria Almira-Casellas, Sílvia Busoms, Laura Pérez-Martín, Glòria Escolà, Álvaro López-Valiñas, Antoni Garcia-Molina, Mercè Llugany, Charlotte Poschenrieder
bioRxiv 2023.02.05.527167; doi: https://doi.org/10.1101/2023.02.05.527167

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