Radial gradient of the mitochondrial ultrastructure in Pisum sativum L. roots

TitleRadial gradient of the mitochondrial ultrastructure in Pisum sativum L. roots
Publication TypeJournal Article
Year of Publication2020
AuthorsBrykov, VO
Abbreviated Key TitleDopov. Nac. akad. nauk Ukr.
Date Published11/2020

Tissue hypoxia in roots of terrestrial plants in the environment saturated with oxygen is conditioned by the high tissue density and oxygen utilization during the cellular respiration, and it is followed by a gradual decrease in the oxygen concentration from the organ surface. We used this natural model on the example of the main roots of 5-day-old seedlings of Pisum sativum L. growing under well-aerated conditions to study the ultrastructure of mitochondria in tissue with reducing oxygen content. In the direction from the root surface to the endodermis, it was found a gradual increase in the size of mitochondria due to swelling and partial fusion of the organelles. The formation of one dominant invagination led to the appearance of cup-shaped organelles in inner cortex cell layers. Such successive changes in the structure of organelles were called the radial gradient of the mitochondrial ultrastructure under a gradual decrease in the cell oxygen content. It is suggested that the described transformations in the mitochondrial ultrastructure could be an unspecific response to conditions that limit their energy and / or metabolic functions.

Keywordscup-shaped mitochondria, low oxygen, mitochondrion, root cortex, ultrastructure

1. Van Dongen, J. T. & Licausi, F. (2015). Oxygen sensing and signaling. Annu. Rev. Plant Biol., 66, pp. 345-367. https://doi.org/10.1146/annurev-arplant-043014-114813
2. Wagner, S., Van Aken, O., Elsässer, M. & Schwarzländer, M. (2018). Mitochondrial energy signaling and its role in the low-oxygen stress response of plants. Plant Physiol., 176, pp. 1156-1170. https://doi.org/10.1104/pp.17.01387
3. Nakamura, M. & Noguchi, K. (2020). Tolerant mechanisms to O2 deficiency under submergence conditions in plants. J. Plant Res., 133, pp. 343-371. https://doi.org/10.1007/s10265-020-01176-1
4. Baker, N., Patel, J. & Khacho, M. (2019). Linking mitochondrial dynamics, cristae remodeling and supercomplex formation: How mitochondrial structure can regulate bioenergetics. Mitochondrion, 49, pp. 259-268. https://doi.org/10.1016/j.mito.2019.06.003
5. Armstrong, W. & Armstrong, J. (2014). Plant internal oxygen transport (diffusion and convection) and measuring and modelling oxygen gradients. In van Dongen, J., Licausi, F. (Eds.). Low-oxygen stress in plants (pp. 267-297). Plant Cell Monograpgs (Vol. 21). Vienna: Springer. https://doi.org/10.1007/978-3-7091-1254-0_14
6. Zabalza, A., Van Dongen, J. T., Froehlich, A., Oliver, S. N., Faix, B., Gupta, K. J., Schmälzlin, E., Igal, M., Orcaray, L., Royuela, M. & Geigenberger, P. (2009). Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol., 149, pp. 1087-1098. https://doi.org/10.1104/pp.108.129288
7. Gibbs, J., Turner, D. W., Armstrong, W., Darwent, M. J. & Greenway, H. (1998). Response to oxygen deficiency in primary roots of maize. I. Development of oxygen deficiency in the stele reduces radial solute transport to the xylem. Aust. J. Plant Physiol., 25, pp. 745-758. https://doi.org/10.1071/PP97135
8. Colmer, T. D., Winkel, A., Kotula, L., Armstrong, W., Revsbech, N. P. & Pedersen, O. (2020). Root O2 consumption, CO2 production and tissue concentration profiles in chickpea, as influenced by environmental hypoxia. New Phytol., 226, pp. 373-384. https://doi.org/10.1111/nph.16368
9. Van Gestel, K. & Verbelen, J. P. (2002). Giant mitochondria are a response to low oxygen pressure in cells of tobacco (Nicotiana tabacum L.). J. Exp. Bot., 53, pp. 1215-1218. https://doi.org/10.1093/jexbot/53.371.1215
10. Ramonell, K. M., Kuang, A., Porterfield, D. M., Crispi, M. L., Xiao, Y., Mclure, G. & Musgrave, M. E. (2001). Influence of atmospheric oxygen on leaf structure and starch deposition in Arabidopsis thaliana. Plant Cell Envir., 24, pp. 419-428. https://doi.org/10.1046/j.1365-3040.2001.00691.x
11. Rakhmatullina, D., Ponomareva, A., Gazizova, N. & Minibayeva, F. (2016). Mitochondrial morphology and dynamics in Triticum aestivum roots in response to rotenone and antimycin A. Protoplasma, 253, pp. 1299-1308. https://doi.org/10.1007/s00709-015-0888-0
12. Jaipargas, E.-A., Barton, K. A., Mathur, N. & Mathur, J. (2015). Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics. Front. Plant Sci., 6, pp. 783. https://doi.org/10.3389/fpls.2015.00783
13. Ponomareva, A. A. & Polygalova, O. O. (2012). Changes in mitochondrial shape in wheat root cells exposed to mitochondrial poisons. Russ. J. Plant Physiol., 59, pp. 428-433. https://doi.org/10.1134/S1021443712030144
14. Vella, N. G. F., Joss, T. V. & Roberts, T. H. (2012). Chilling-induced ultrastructural changes to mesophyll cells of Arabidopsis grown under short days are almost completely reversible by plant re-warming. Protoplasma, 249, pp. 1137-1149. https://doi.org/10.1007/s00709-011-0363-5
15. Xi, Y. X. (1995). NaCl-induced amoeboid plastids and mitochondria in meristematic cells of barley roots. Biol Plant., 37, pp. 363-369. https://doi.org/10.1007/BF02913979