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AtCBF1 Overexpression Confers Tolerance to High Light Conditions at Warm Temperatures in Potato Plants

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Abstract

We characterized transcriptional responses of potato plants to multiple abiotic stresses and used this information to identify potential mechanisms through which over-expression of the stress related transcription factor CBF1 from Arabidopsis thaliana (AtCBF1) confers multiple stress tolerance. Most transcriptional changes were specific to each condition, but genes involved in phenyl-propanoid biosynthesis were affected by all abiotic stresses evaluated. Interestingly, over-expression of AtCBF1 in potato plants not only conferred tolerance to low temperatures, as previously reported, but also to high-light conditions at 22 °C, suggesting that it confers multiple stress tolerance by enhancing the ability of plants to cope with an excess of radiant energy. Finally, we found that transcriptional changes triggered by abiotic stress were much larger than those resulting from AtCBF1 over-expression in potato, revealing that overexpression of an heterologous transcription factor causes minor alterations in the plant transcriptome in comparison to transcriptional changes triggered by abiotic stresses.

Resumen

Caracterizamos respuestas transcripcionales de plantas de papa a múltiples estreses abióticos y utilizamos esta información para identificar mecanismos potenciales a través de los cuales la sobreexpresión del factor de transcripción CBF1 relacionado con agobio de Arabidopsis thaliana (AtCBF1) confiere tolerancia múltiple al estrés. La mayoría de los cambios transcripcionales fueron específicos para cada condición, pero se afectaron los genes involucrados en la biosíntesis de fenil-propanoides por todos los estreses abióticos evaluados. Interesantemente, la sobreexpresión del AtCBF1 en plantas de papa no solo confirieron tolerancia a bajas temperaturas, como se ha reportado previamente, sino también a condiciones de alta luminosidad a 22 °C, lo que sugiere múltiple tolerancia al estrés mediante el aumento de la habilidad de las plantas para hacer frente a un exceso de energía radiante. Finalmente, encontramos que los cambios transcripcionales disparados por el agobio abiótico fueron mayores que aquellos que resultaron de la sobreexpresión de AtCBF1 en papa, revelando que la sobreexpresión de un factor heterólogo de transcripción causa alteraciones menores en el transcriptoma de la planta en comparación a cambios transcripcionales disparados por estreses abióticos.

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Acknowledgments

This work was supported by a fellowship from the Argentinean National Research Council to L.S., and by grants from Agencia Nacional de Promoción Científica y Tecnológica to M.J.Y.

Authors’ Contributions

LS performed most of the experiments in this study with technical assistance from EP, MLR, GGS. AC performed the statistical analysis. LS, CEH, RJS, JJC and MJY provided input in designing experiments and in the preparation of the manuscript and LS, CEH and MJY wrote the paper.

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Authors and Affiliations

  1. Instituto de Fisiología y Ecología Vinculado a la Agricultura, IFEVA, CONICET-UBA, Av. San Martín 4453, CPA1417DSE, Buenos Aires, Argentina

    Leonardo Storani, Edmundo Ploschuk, Matias L. Rugnone, Gustavo G. Striker, Jorge J. Casal & Marcelo J. Yanovsky

  2. Fundación Instituto Leloir - Instituto de Investigaciones Bioquímicas de Buenos Aires, Av. Patricias Argentinas 435, C1405BWE, Buenos Aires, Argentina

    Carlos E. Hernando, Roberto J. Staneloni, Jorge J. Casal, Ariel Chernomoretz & Marcelo J. Yanovsky

  3. Departamento de Física, FCEN, UBA, Pabellón 1, Ciudad Universitaria, 1428, Buenos Aires, Argentina

    Ariel Chernomoretz

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  1. Leonardo Storani
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  2. Carlos E. Hernando
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Correspondence to Marcelo J. Yanovsky.

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These experiments were funded by the Argentinean National Research Council (CONICET).

Electronic supplementary material

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ESM 1

Complete lists of genes regulated by drought, low temperature and high-light stress in potato plants. Tab1. Genes up-regulated under drought stress. Tab2. Genes down-regulated under drought stress. Tab3. Genes up-regulated under low temperature stress. Tab4. Genes down-regulated under low temperature stress. Tab5. Genes up-regulated under high light stress. Tab6. Genes down-regulated under high light stress. (XLS 1118 kb)

ESM 2

Examples of genes regulated under drought stress. (a) Up-regulated genes. (b) Down-regulated genes (GIF 35 kb)

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ESM 3

Examples of genes up-regulated under both drought and low temperature stresses (GIF 21 kb)

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ESM 4

Contrasting regulation of an aquaporin gene by drought and low temperatures (GIF 15 kb)

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ESM 5

Expression of circadian clock associated genes from the MYB family of transcription factors under low temperature, drought and high light (GIF 21 kb)

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ESM 6

Regulation of genes involved in redox homeostasis by high light stress (GIF 20 kb)

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ESM 7

Down regulation of genes associated with the control of cell elongation and leaf area in response to abiotic stress (GIF 23 kb)

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ESM 8

Regulation of CIB1 expression by abiotic stress in potato (GIF 13 kb)

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ESM 9

Phenotypic characterization of AtCBF1-OX transgenic potato plants. (a) Total height and 3rd internode length of two independent AtCBF1-OX transgenic lines compared to wild-type potato plants. (b) Tuber yield. In (a) data are mean ± S.E. of six replicates. In (b) data are mean ± S.E. of nine replicates. * indicates significant differences between treatments (p<0.05). (GIF 47 kb)

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ESM 10

Cold stress tolerance in AtCBF1-OX transgenic potato plants. (a) Fv/Fm measured in the leaves of WT and AtCBF1-OX transgenic plants under control and low temperature conditions. Data are mean ± S.E. of three replicates. Different letters indicate statistically significant differences (p<0.05). (b) Representative leaf of WT and AtCBF1-OX transgenic potato plants after prolonged cold exposure. (c) WT and AtCBF1-OX transgenic plants exposed for one week to low temperature conditions. (GIF 139 kb)

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Tolerance to drought stress in AtCBF1-OX transgenic potato plants. (a) Water loss in detached leaves of WT and AtCBF1-OX plants during three days. (b) Leaf transpiration rate during drought treatment. (c) Transpiration rate measured as water loss from plants grown in pots during a drought treatment. (d) Photograph of WT and AtCBF1OX transgenic potato plants after ten days of no water supply. (e) Fv/Fm after ten days of drought. (f) Photosynthesis rate and chlorophyll content of stress treated relative to control plants after 10 days of drought. Data in (a) are mean ± S.E. of twelve leaves. Data in (b), (c) and (d) are mean ± S.E. of three plants. Data in F are mean ± S.E. of four plants. * indicates significant differences between treatments (p<0.05). (GIF 114 kb)

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Genes regulated by AtCBF1 under control conditions and in WT plants under stress conditions. Tab1. Genes up-regulated by AtCBF1 under control growth conditions. Tab2. Genes down-regulated by AtCBF1 under control growth conditions. Tab3. Genes up-regulated by AtCBF1 under control growth conditions and under any of the abiotic stresses analyzed before. Tab4. Genes down-regulated by AtCBF1 under control growth conditions and by any of the abiotic stresses analyzed before. (XLS 149 kb)

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Expression of cold regulated genes in WT and AtCBF1-OX transgenic plants under control conditions (GIF 17 kb)

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Expression of PORB in WT and AtCBF1-OX transgenic plants in response to high light stress (GIF 18 kb)

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Template Matching Analysis. Number of genes significantly correlated to each one of these templates, as a function of the considered significance level. For any given statistical cutoff level, light stress treatments committed the largest set of genes (~20% bigger than the one induced by temperature stress, and up to 300% bigger than the one associated to genetic background differences). (GIF 35 kb)

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Multi Response Permutation Procedure for gene expression analysis. MRPP results obtained for the low temperature and high-light stress conditions are reported in the first and second row respectively. A, δ, <δ>, and pv, are the effect-size, the observed and expected weighted mean of intra group distances, and the associated p-value, respectively. (XLS 25 kb)

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Lists of genes regulated by AtCBF1-OX under control or abiotic stress conditions in potato plants. 1 indicates regulated by the treatment being evaluated, 0 indicates not regulated by the treatment being evaluated. Tab1. Genes regulated by temperature stress but not by light or genetic background. Tab2. Genes regulated by light but not by low temperature conditions or genetic background. Tab3. Genes regulated by genetic background but not by low temperatures or high-light stress. Tab4. Genes regulated by low temperatures and by high-light but not by genetic background. Tab5. Genes regulated by temperature stress and genetic background, but not by high-light. Tab6. Genes regulated by genetic background and by high-light, but not by low temperatures. Tab7. Genes regulated by genetic background, high-light and low temperatures. (XLS 1621 kb)

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Primers used for qRT-PCR validation of microarray data (XLS 24 kb)

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Storani, L., Hernando, C.E., Staneloni, R.J. et al. AtCBF1 Overexpression Confers Tolerance to High Light Conditions at Warm Temperatures in Potato Plants. Am. J. Potato Res. 92, 619–635 (2015). https://doi.org/10.1007/s12230-015-9476-2

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