Abstract
Exposure to low, non-freezing temperatures develops freezing tolerance in many plant species. Such process is called cold acclimation. Molecular changes undergone during cold acclimation are orchestrated by signalling networks including MAP kinases. Structure and function of chloroplasts are affected by low temperatures. The aim of this work was to study how the MAP kinases MPK3 and MPK6 are involved in the chloroplast performance upon a long period of cold acclimation. We used Arabidopsis thaliana wild type and mpk3 and mpk6 mutants. Adult plants were acclimated during 7 days at 4 °C and then measurements of PSII performance and chloroplast ultrastructure were carried out. Only the mpk6 acclimated plants showed a high freezing sensitivity. No differences in the PSII function were observed in the plants from the three genotypes exposed to non-acclimated or acclimated conditions. The acclimation of wild-type plants produced severe alterations in the ultrastructure of chloroplast and thylakoids, which was more accentuated in the mpk plants. However, only the mpk6 mutant was unable to internalize the damaged chloroplasts into the vacuole. These results indicate that cold acclimation induces alterations in the chloroplast architecture leading to preserve an optimal performance of PSII. MPK3 and MPK6 are necessary to regulate these morphological changes, but besides, MPK6 is needed to the vacuolization of the damaged chloroplasts, suggesting a role in the chloroplast recycling during cold acclimation. The latter could be quite relevant, since it could explain why this mutant is the only one showing an extremely low freezing tolerance.
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taken from 18 different plants from every genotype in three independent experiments. Different letters denote significant differences based on Tukey’s test (p < 0.05)
taken from plants exposed to NA (upper panel) or AC conditions (lower panel). Bars = 2 μm in all images. b Chloroplast length/width ratio. This was calculated from fifteen chloroplasts measured from four cells for each genotype and acclimation condition using ImageJ. c Ultrastructure of thylakoid membranes. Representative cross-sections of chloroplasts are shown for NA and AC wild type, mpk3 and mpk6. Bars = 500 nm in all images. d Scattered plot of the average grana diameter and height values (n = 75) from six chloroplasts measured by ImageJ in the three genotypes. Bars represent the respective standard errors of the mean (SEM). Different letters denote significant differences based on Tukey’s test (p < 0.05)
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Abbreviations
- AC:
-
Acclimated
- Atg :
-
Autophagy-defective mutant
- CBF:
-
C-repeat binding factor
- FB1:
-
Fumonisin B1
- MAPK:
-
Mitogen-activated protein kinase
- MAPKK:
-
Mitogen-activated protein kinase kinase
- MAPKKK:
-
Mitogen-activated protein kinase kinase kinase
- MKK2:
-
Upstream MAPKK of MPK4/MPK6
- MPK3, MPK4 or MPK6:
-
Mitogen-activated protein kinase 3, 4 or 6, respectively
- NA:
-
Non-acclimated
- PAMPs:
-
Pathogen-associated molecular patterns
- SEM:
-
Standard error of the mean
- TEM:
-
Transmission electron microscopy
- UV-B:
-
Ultraviolet B rays
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Acknowledgements
The authors thank Dr. Laura Carmona-Salazar and Dr. Rodolfo Paredes for the transmission electron microscopy work.
Funding
This work was financed by Dirección General de Asuntos del Personal Académico (DGAPA), UNAM (grants: PAPIIT IN222815 and IN220618), Consejo Nacional de Ciencia y Tecnología (CONACYT) (CB-2015 and 255265 to M.S.-G; CB-2014-01 and 238368 to M.G.-R) and Facultad de Química, UNAM (5000 9115).
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CDGC, IGPP, DCR, FRC and EAP performed the experiments; MSG, AZ and MGR analysed the data; DCR, MSG, AZ and MGR conceived the project; MSG, AZ and MGR wrote the article with contributions of all the authors.
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Alonso Zavafer is a guest Editor in this special issue in honour to Wah Soon Chow. Despite this relationship, he did not at any stage have editor-level access to this manuscript whilst in peer review, as is the standard practice when handling manuscripts submitted by an editor to this journal. The authors have no further conflicts of interest to declare. Alonso Zavafer declares that Zavafer is a pseudonym and his legal name is Alonso Zavaleta Fernandez de Cordova.
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Saucedo-García, M., González-Córdova, C.D., Ponce-Pineda, I.G. et al. Effects of MPK3 and MPK6 kinases on the chloroplast architecture and function induced by cold acclimation in Arabidopsis. Photosynth Res 149, 201–212 (2021). https://doi.org/10.1007/s11120-021-00852-0
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DOI: https://doi.org/10.1007/s11120-021-00852-0