Abstract
For the first time, the effect of 5- and 10-day soil flooding on the ultrastructure of the leaf mesophyll cells of the psammophyte desert madwort (Alyssum desertorum L.) was investigated. The seeds for the experiments were collected from plants of dry sandy areas of the gully slopes of the ravine forest in the steppe zone of the Dnipropetrovsk oblast. It is shown that a characteristic feature of the leaf photosynthetic cells of this species is the presence of single and large, up to 6 pm, peroxisomes, which are in close contact with chloroplasts and mitochondria, playing a key role in photorespiration. The general organization of palisade parenchyma cells on days 5 and 10 of soil flooding is similar to that in the control. A slight decrease in the size of peroxisomes on day 5 of flooding and its increase on day 10 and more often formation of multivesicular structures (assembly of endomembranes) in the vacuole, which is considered as an autophagy enhancement of the cytoplasm under hypoxia, were noted. Differences in the ultrastructure of chloroplasts under the influence of soil flooding consisted in a significant, almost twofold increase in transient starch, the size and number of plastoglobules, especially on day 10, and swelling of granal and stroma thylakoids on day 10. Changes in the ultrastructure of desert madwort chloroplasts under the influence of soil flooding coincide with those of mesophytes studied in this respect. The obtained data on the chloroplast ultrastructure of desert madwort psammophyte prove the functioning of the photosynthetic apparatus in conditions of short-term soil flooding, which contributes to the survival of seedlings. The subsequent yellowing of leaves and death of plants indicates, as is assumed, the lack of systemic adaptation, primarily metabolic, that is, the transition to anaerobic metabolism, in this species to long-term hypoxia.
Similar content being viewed by others
REFERENCES
Akyol, Y., Kocabas, O., Bozdag, B., Minareci, E., and Ozdemir, C., Vascular anatomy of Alyssum alyssoides and A. desertorum (Brassicaceae) from Eastern Anatolia, Turkey, Phytol. Canica, 2017, vol. 23, pp. 3–6.
Bailey-Serres, J. and Voesenek, L., Flooding stress: acclimations and genetic diversity, Ann. Rev. Plant Biol., 2008, vol. 59, pp. 313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752
Bailey-Serres, J., Lee, S., and Brinton, E., Waterproofing crops: effective flooding survival strategies, Plant Physiol., 2012, vol. 160, pp. 1698–1709. https://doi.org/10.1104/pp.112.208173
Gravatt, D.A. and Kirby, C.J., Patterns of photosynthesis and starch allocation in seedlings of four bottomland hardwood tree species subjected to flooding, Tree Physiol., 1998, vol. 18, pp. 411–417. https://doi.org/10.1093/treephys/18.6.411
Gu, L., Grodzinski, B., Han, J., et al., Granal thylakoid structure and function: explaining an enduring mystery of higher plants, New Phytol., 2022, vol. 236, pp. 319–329. https://doi.org/10.1111/nph.18371
Hirabayashi, Y., Mahendran, R., Koirala, S., et al., Global flood risk under climate change, Nat. Clim. Change, 2013, vol. 3, pp. 816–821. https://doi.org/10.1038/nclimate1911
Hu, J., Baker, A., Bartel, B., et al., Plant peroxisomes: biogenesis and function, Plant Cell, 2012, vol. 24, no. 6, pp. 2279–2303. https://doi.org/10.1105/tpc.112.096586
Iljinska, A.P., Species of the genus Alyssum L. (sect. Alyssum) in the flora of Ukraine, Ukr. Bot. J., 2005, vol. 62, no. 2, pp. 223–234.
Jansen, R.L.M., Santana-Molina, C., van den Noort, M., Devos, D.P., and van der Klei, I.J., Comparative genomics of peroxisome biogenesis proteins: making sense of the PEX proteins, Front. Cell Dev. Biol., 2021, vol. 9, p. 654163. https://doi.org/10.3389/fcell.2021.654163
Kanai, M., Higuchi, K., Hagihara, T., et al., Common reed produces starch granules at the shoot base in response to salt stress, New Phytol., 2007, vol. 176, pp. 572–580.
Kao, Y.T., Gonzalez, K.L., and Bartel, B., Peroxisome function, biogenesis, and dynamics in plants, Plant Physiol., 2018, vol. 176, pp. 162–177. https://doi.org/10.1104/pp.17.01050
Kirchhoff, H., Chloroplast ultrastructure in plants, New Phytol., 2019, vol. 223, pp. 565–574. https://doi.org/10.1111/nph.15730
Klymchuk, D.O., Brown, C.S., Chapman, D.K., Vorobyova, T.V., and Martyn, G.M., Cytochemical localization of calcium in soybean root cap cells in microgravity, Adv. Space Res., 2001, vol. 27, pp. 967–972.
Kreuzwieser, J. and Rennenberg, H., Molecular and physiological responses of trees to waterlogging stress, Plant Cell Environ., 2014, vol. 37, pp. 2245–2259. https://doi.org/10.1111/pce.12310
Liu, Z., Cheng, R., Xiao, W., et al., Effect of off-season flooding on growth, photosynthesis, carbohydrate partitioning, and nutrient uptake in Distylium chinense, PLoS One, 2014, vol. 9, p. e107636. https://doi.org/10.1371/journal.pone.0107636
Merchant, A., Peuke, A.D., Keitel, C., et al., Phloem sap and leaf δ13C-carbohydrates and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment, J. Exp. Bot., 2010, vol. 61, pp. 1785–1793. https://doi.org/10.1093/jxb/erq045
Morris, J. and Brewin, P., The impact of seasonal flooding on agriculture: the spring 2012 floods in Somerset, England, J. Flood Risk Manage., 2014, vol. 7, pp. 128–140. https://doi.org/10.1111/jfr3.12041
Nasrullah, A.S., Umar, M., et al., Flooding tolerance in plants: from physiological and molecular perspectives, Braz. J. Bot., 2022, vol. 45, pp. 1161–1176. https://doi.org/10.1007/s40415-022-00841-0
Oikawa, K., Hayashi, M., Hayashi, Y., and Nishimura, M., Re-evaluation of physical interaction between plant peroxisomes and other organelles using live-cell imaging techniques, J. Integr. Plant Biol., 2019, vol. 61, pp. 836–852. https://doi.org/10.1111/jipb.12805
Pan, R., Jun, L., Saisai, W., and Jianping, H., Peroxisomes: versatile organelles with diverse roles in plants, New Phytol., 2020, vol. 225, pp. 1410–1427. https://doi.org/10.1111/nph.16134
Patel, P., Singh, A., Tripathi, N., et al., Flooding: abiotic constraint limiting vegetable productivity, Adv. Plants Agric. Res., 2014, vol. 1, pp. 96–103. https://doi.org/10.15406/apar.2014.01.00016
Pshybytko, E., Kruk, J., Lysenko, E., et al., Environ. Exp. Bot., 2022, vol. 206. https://doi.org/10.1016/j.envexpbot.2022.105151
Ren, B., Zhang, J., Dong, S., Liu, P., and Zhao, B., Effects of waterlogging on leaf mesophyll cell ultrastructure and photosynthetic characteristics of summer maize, PloS One, 2016, vol. 11, p. e0161424
Reumann, S. and Bartel, B., Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics, Curr. Opin. Plant B-iol., 2016, vol. 34, pp. 17–26. https://doi.org/10.1016/j.pbi.2016.07.008
Sharma, U., Bhatt, J., Sharma, H.M., et al., Ultrastructure, adaptability, and alleviation mechanisms of photosynthetic apparatus in plants under waterlogging: A review, Photosynthetica, 2022, vol. 60, pp. 430–444. https://doi.org/10.32615/ps.2022.033
Shi, F., Pan, Z., Dai, P., et al., Effect of waterlogging stress on leaf anatomical structure and ultrastructure of Phoebe sheareri seedlings, Forests, 2023, vol. 14, no. 7, p. 1294. https://doi.org/10.3390/f14071294
Takahashi, S. and Badger, M.R., Photoprotection in plants: a new light on photosystem II damage, Trends Plant Sci., 2011, vol. 16, pp. 53–60. https://doi.org/10.1016/j.tplants.2010.10.001
Thalmann, M. and Santelia, D., Starch as a determinant of plant fitness under abiotic stress, New Phytol., 2017, vol. 214, no. 3, pp. 943–951. https://doi.org/10.1111/nph.14491
Todorova, D., Katerova, Z., Shopova, E., et al., The physiological responses of wheat and maize seedlings grown under water deficit are modulated by pre-application of auxin-type plant growth regulators, Plants, 2022, vol. 11, p. 3251. https://doi.org/10.3390/plants11233251
Topa, M.A. and Cheeseman, J.M., Carbon and phosphorus partitioning in Pinus serotina seedlings growing under hypoxic and low-phosphorus conditions, Tree Physiol., 1992, vol. 10, pp. 195–207.
Utrillas, M.J. and Alegre, L., Impact of water stress on leaf anatomy and ultrastructure in Cynodon dactylon (L.) Pers. under natural conditions, Int. J. Plant Sci., 1997, vol. 158, pp. 313–324.
Van Wijk, K.J. and Kessler, F., Plastoglobuli: plastid microcompartments with integrated functions in metabolism, plastid developmental transitions, and environmental adaptation, Ann. Rev. Plant Biol., 2017, vol. 68, pp. 253–389.
Vu, C.V. and Yelenosky, G., Photosnythetic responses of rough lemon and sour orange to soil flooding, chilling, and short-term temperature fluctuations during growth, Environ. Exp. Bot., 1992, vol. 32, pp. 471–477. https://doi.org/10.1016/0098-8472(92)90060-F
Wample, R.L. and Davis, R.W., Effect of flooding on starch accumulation in chloroplasts of sunflower (Helianthus annus L), Plant Physiol., 1983, vol. 73, pp. 195–198.
Yan, L., Guanghui, L., Xueming, H., and Xueni, Z., Complete chloroplast genome of a spring ephemeral plant Alyssum desertorum and its implications for the phylogenetic position of the tribe Alysseae within the Brassicaceae Nordic, J. Bot., 2017, vol. 35, pp. 644–652. https://doi.org/10.1111/njb.01531
Yoshioka-Nishimura, M., Close relationships between the PSII repair cycle and thylakoid membrane dynamics, Plant Cell Physiol., 2016, vol. 57, pp. 1115–1122. https://doi.org/10.1093/pcp/pcw050
Zhang, R.D., Zhou, Y.F., Yue, Z.X., et al., Changes in photosynthesis, chloroplast ultrastructure, and antioxidant metabolism in leaves of sorghum under waterlogging stress, Photosynthetica, 2019, vol. 57, pp. 1076–1083.
Zhou, J., Wan, S.W., Li, G., and Qin, P., et al., Ultrastructure changes of seedlings of Kosteletzkya virginica under waterlogging conditions, Biol. Plant., 2011, vol. 55, pp. 493–498. https://doi.org/10.1007/s10535-011-0115-6
Funding
The financing of the work was carried out within the framework of the topic of the Department of Anatomy and Cell Biology of Kholodny Institute of Botany, no. 467 “Cellular and molecular Aspects of Phenotypic Plasticity of Heliophytes, Psammophytes, and Lithophytes under Contrasting Conditions of the Water Regime.”
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This work does not contain any studies involving human and animal subjects.
CONFLICT OF INTEREST
The authors of this work declare that they have no conflicts of interest.
Additional information
Publisher’s Note.
Allerton Press remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Akimov, Y.M., Vorob’ova, T.V. Ultrastructure of Leaf Mesophyll Cells of Alyssum desertorum L. under Soil Flooding. Cytol. Genet. 58, 92–98 (2024). https://doi.org/10.3103/S0095452724020026
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3103/S0095452724020026