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Structure, ultrastructure and cation accumulation in quinoa epidermal bladder cell complex under high saline stress

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Abstract

Quinoa is a facultative halophyte with excellent tolerance to salinity. In this study, the epidermal bladder cell complex (EBCc) of quinoa leaves was studied to determine their cellular characteristics and involvement in salt tolerance. We used light microscopy, confocal RAMAN microscopy, confocal fluorescence microscopy, transmission electron microscopy, and environmental scanning electron microscopy complemented by energy dispersive X-ray analysis. Ionic content was quantified with flame atomic absorption spectroscopy and with flame emission photometry. Results show that: (i) the number of EBCcs remains constant but their density and area vary with leaf age; (ii) stalk cells store lipids and exhibit thick walls, bladder cells present carotenes in small vesicles, oxalate crystals in vacuoles and lignin in their walls and both stalk and bladder cells have cuticles that differ in wax and cutin content; (iii) chloroplasts containing starch can be found on both stalk and bladder cells, and the latter also presents grana; (iv) plasmodesmata are observed between the stalk cell and the bladder cell, and between the epidermal cell and the stalk cell, and ectodesmata-like structures are observed on the bladder cell. Under high salinity conditions, (v) there is a clear tendency to accumulate greater amounts of K+ with respect to Na+ in the bladder cell; (vi) stalk cells accumulate similar amounts of K+ and Na+; (vii) Na+ accumulates mainly in the medullary parenchyma of the stem. These results add knowledge about the structure, content, and role of EBCc under salt stress, and surprisingly present the parenchyma of the stem as the main area of Na+ accumulation.

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Acknowledgements

We express our gratitude to Dr. María Victoria Repetto for technical assistance in confocal fluorescence microscopy.

Funding

Funding for this work was provided by grants from the Agencia Nacional de Investigaciones Científicas y Tecnologicas (ANyCT, Argentina) to Sara Maldonado and Hernán Pablo Burrieza (PICT-2015–3527) and University of Buenos Aires (20020170200265BA) to Hernán Pablo Burrieza. María Belén Palacios, Axel Joel Rizzo, and Tatiana Belén Heredia thank the Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Argentina, for their fellowships.

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Authors and Affiliations

  1. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    María Belén Palacios, Axel Joel Rizzo, Sara Maldonado & Hernán Pablo Burrieza

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    María Belén Palacios, Axel Joel Rizzo, Tatiana Belén Heredia, Sara Maldonado, Daniel Horacio Murgida & Hernán Pablo Burrieza

  3. Estación Experimental Agropecuaria San Juan, Instituto Nacional de Tecnología Agropecuaria (INTA), San Juan, Argentina

    Tatiana Belén Heredia & Gonzalo Roqueiro

  4. Departamento de Química Inorgánica, Analítica y Química Física and INQUIMAE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    Daniel Horacio Murgida

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  1. María Belén Palacios
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Contributions

María Belén Palacios: research design, preparation of biological material, carrying out the main experiments (EBCcs, LM, TEM, ESEM-EDX, CLSM, CRM analysis), statistics and writing. Hernán Pablo Burrieza: original idea, conceptualization, research design, validation, critical supervision of the work, writing and acquisition of funds. Sara Maldonado: original idea, research design and acquisition of funds. Axel Joel Rizzo: technical assistance in microscopy, statistics and writing. Daniel Horacio Murgida: image acquisition and analysis of confocal RAMAN microscopy. Tatiana Belén Heredia: cation quantification. Gonzalo Roqueiro: cation quantification. All authors read and approved the manuscript.

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Correspondence to Hernán Pablo Burrieza.

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Palacios, M.B., Rizzo, A.J., Heredia, T.B. et al. Structure, ultrastructure and cation accumulation in quinoa epidermal bladder cell complex under high saline stress. Protoplasma (2024). https://doi.org/10.1007/s00709-023-01922-x

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