Skip to main content

Advertisement

Log in

Structural and Functional Determinants of Physiological Pliability in Kyllinga brevifolia Rottb. for Survival in Hyper-Saline Saltmarshes

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The role of morpho-anatomical adaptations of six Kyllinga brevifolia populations in successfully invading hyper-saline environments was investigated. Physiological and anatomical characteristics showed a high degree of plasticity indicating its adaptability potential to a variety of environmental conditions. The population from hyper-saline saltmarsh Sahianwala was exposed to physiological drought for a long time and its survival relied on the prevention of water loss attained by decreased stomatal density and area, lignin deposition in the inner and outer cortical region, especially outside vascular tissue. Larger cells of cortical storage parenchyma aided in water storage and wide metaxylem vessels in better conduction of solutes. Higher accumulation of shoot Ca2+ in this habitat protected neutralized the impact of the enhanced shoot and root Na+ ion uptake. Organic osmoprotectants like total free amino acid, proline, soluble proteins, and sugars accumulated in a higher quantity that contributed towards an osmotic adjustment in Sahianwala population. Population from seasonal inundation (Treemu Headworks) showed larger root aerenchyma to supply sufficient oxygen for respiration, broader xylem vessels for better water and nutrient conduction, and greater density of leaf stomata for better transpiration. Maximum shoot and root length, total leaf area, and water potential were observed in the least saline Chinyot population indicating its best growth potential in a slightly saline aquatic environment. Each population showed specific physiological and anatomical modifications to colonize their respective habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

The herbarium samples used for identification of plant species deposited to the Herbarium Collection of the Department of Botany, University of Agriculture Faisalabad.

References

  • Abulfatih, H. A. (2003). Ecological anatomy of xerophytic leaves from Qatar. Journal of King Saud University, 16, 19–29.

    Google Scholar 

  • Ahmad, I., & Maathuis, F. J. (2014). Cellular and tissue distribution of potassium: Physiological relevance, mechanisms and regulation. Journal of Plant Physiology, 171, 708–714.

    Article  CAS  Google Scholar 

  • Alam, M. A., Juraimi, A. S., Rafii, M. Y., & Hamid, A. A. (2015). Effect of salinity on biomass yield and physiological and stem-root anatomical characteristics of purslane (Portulaca oleracea L.) accessions. BioMed Research Internatinal, 2015, 105695.

    Google Scholar 

  • Alvarez, J. M., Rocha, J. F., & Machado, S. R. (2008). Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): Structure in relation to function. Brazilian Archives of Biology and Technology, 51, 113–119.

    Article  Google Scholar 

  • Atreya, A., Vartak, V., & Bhargava, S. (2009). Salt priming improves tolerance to desiccation stress and to extreme salt stress in Bruguiera cylindrica. International Journal of Integrative Biology, 6, 68–73.

    CAS  Google Scholar 

  • Barrett-Lennard, E. G. (2003). The interaction between waterlogging and salinity in higher plants: Causes, consequences and implications. Plant and Soil, 253, 35–54.

    Article  CAS  Google Scholar 

  • Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207.

    Article  CAS  Google Scholar 

  • Batool, R., Hameed, M., & Ashraf, M. (2013). Photosynthetic response of three aquatic species of Schoenoplectus (Reichenb.) Palla under salt stress. Wetlands, 27, 2–11.

    Google Scholar 

  • Bell, H. L., & O’Leary, J. W. (2003). Effects of salinity on growth and cation accumulation of Sporobolus virginicus (Poaceae). American Journal of Botany, 90, 1416–1424.

    Article  Google Scholar 

  • Benz, B. R., Rhode, J. M., & Cruzan, M. B. (2007). Aerenchyma development and elevated alcohol dehydrogenase activity as alternative responses to hypoxic soils in the Piriqueta caroliniana complex. American Journal of Botany, 94, 542–550.

    Article  CAS  Google Scholar 

  • Benzarti, M., Rejeb, K. B., Messedi, D., Mna, A. B., Hessini, K., Ksontini, M., Abdelly, C., & Debez, A. (2014). Effect of high salinity on Atriplex portulacoides: Growth, leaf water relations and solute accumulation in relation with osmotic adjustment. South African Journal of Botany, 95, 70–77.

    Article  CAS  Google Scholar 

  • Bernhardt, K. G., & Kropf, M. (2006). Schoenus nigricans (Cyperaceae) xerophytic grasslands on the NE Adriatic islands Cres and Krk (Croatia). Acta Botanica Croatica, 65, 127–136.

    Google Scholar 

  • Bonomelli, C., Gil, P. M., & Schaffer, B. (2019). Effect of soil type on calcium absorption and partitioning in young avocado (Persea americana Mill.) trees. Agronomy, 9, 837–849.

    Article  CAS  Google Scholar 

  • Bray, S., & Reid, D. M. (2002). The effect of salinity and CO2 enrichment on the growth and anatomy of the second trifoliate leaf of Phaseolus vulgaris. Canadian Journal of Botany, 80, 349–359.

    Article  Google Scholar 

  • Camargo, M. A. B., & Marenco, R. A. (2011). Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia. Acta Amazonica, 41, 205–212.

    Article  Google Scholar 

  • Carignato, A., Piqué, J. V., Tapias, R., Ruiz, F., & Fernández, M. (2019). Variability and plasticity in cuticular transpiration and leaf permeability allow differentiation of Eucalyptus clones at an early age. Forests, 6, 23–31.

    Google Scholar 

  • Dítě, D., Dítě, Z., Hájková, P., & Šuvada, R. (2019). Vegetation and ecological characteristics of the northernmost salt marshes of the European continent. Nordic Journal of Botany, 3. https://doi.org/10.1111/njb.023347.

  • Farooq, M., Kobayashi, N., & Fujita, D. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable Development, 29, 185–212.

    Article  Google Scholar 

  • Field, R., Hawkins, B. A., Cornell, H. V., Currie, D. J., Alexandre, J., Diniz-Filho, F., Guégan, J. F., Dawn Kaufman, M., Kerr, J. T., Mittelbach, G. G., Eileen, T. O., O’Brien, M., & Turner, J. R. G. (2009). Spatial species-richness gradients across scales: A metaanalysis. Journal of Biogeography, 36, 132–147.

    Article  Google Scholar 

  • Grigore, M. N., & Toma, C. (2007). Histo-anatomical strategies of Chenopodiaceae halophytes: Adaptive, ecological and evolutionary implications. WSEAS Transactions on. Biology and Biomedicine, 4, 204–218.

    Google Scholar 

  • Grigore, M. N., Ivanescu, L., & Toma, C. (2014). Halophytes. An integrative anatomical study. Springer.

    Book  Google Scholar 

  • Hameed, M., Ashraf, M., & Naz, N. (2009). Anatomical adaptations to salinity in cogon grass [Imperata cylindrica (L.) Raeuschel] from the Salt Range, Pakistan. Plant and Soil, 322, 229–238.

    Article  CAS  Google Scholar 

  • Hanif, U., Syed, S. H., Ahmad, R., & Malik, K. (2010). Economic impact of climate change on the agricultural sector of Punjab. The Pakistan Development Review, 49, 771–798.

    Article  Google Scholar 

  • Hanson, D. T., Stutz, S., & Boyer, J. S. (2016). Why small fluxes matter: The case and approaches for improving measurements of photosynthesis and (photo)respiration. Journal of Experimental Botany, 67, 3027–3039.

    Article  CAS  Google Scholar 

  • Hoque, M. I. U., Uddin, M. N., Fakir, M. S. A., & Rasel, M. (2018). Drought and salinity affect leaf and root anatomical structures in three maize genotypes. Journal of Bangladesh Agriculture University, 16, 47–55.

    Article  Google Scholar 

  • Hayat, S., Hasan, S. A., Fariduddin, Q., & Ahmad, A. (2011). Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. Journal of Plant Interaction, 3, 297–304.

    Article  CAS  Google Scholar 

  • Hussain, K., Majeed, A., Nawaz, K., Khizar, H. B., & Nisar, M. F. (2009). Effect of different levels of salinity on growth and ion contents of black seeds (Nigella sativa L.). Current Research Journal of Biological Sciences, 1, 135–138.

    CAS  Google Scholar 

  • Jiang, Z., Zhu, S., Ye, R., Xue, Y., Chen, A., An, L., & Pei, Z. M. (2013). Relationship between NaCl- and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis. PLoS ONE, 8, e76130.

    Article  CAS  Google Scholar 

  • Kafi, M., Nabati, J., Ahmadi-Lahijani, M. J., & Oskoueian, A. (2021). Silicon compounds and potassium sulfate improve salinity tolerance of potato plants through instigating the defense mechanisms, cell membrane stability, and accumulation of osmolytes. Communication in Soil Science and Plant Analysis, 52,. https://doi.org/10.1080/00103624.2020.1869768

  • Kokkonen, M., Jestoi, M., & Rizzo, A. (2005). Determination of selected mycotoxins in mould cheeses with liquid chromatography coupled to tandem with mass spectrometry. Food Additives and Contaminants, 22, 449–456.

    Article  CAS  Google Scholar 

  • Les, D. H. (2020). Aquatic monocotyledons of North America: Ecology, life history, and systematics. CRC Press.

    Book  Google Scholar 

  • Liu, Y., Li, X., Chen, G., Li, M., Liu, M., & Liu, D. (2015). Epidermal micromorphology and mesophyll structure of Populus euphratica heteromorphic leaves at different development stages. PLoS One, 10, e0141578.

    Article  CAS  Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin Phenol reagent. Journal of Biological Chemistry, 193, 265–275.

  • Mishra, S., Tripathi, A., Tripathi, D. K., & Chauhan, D. K. (2015). Role of sedges (Cyperaceae) in wetlands, environmental cleaning and as food material: Possibilities and future perspectives. Journal of Experimental Botany, 62, 42–53.

    Google Scholar 

  • Moller, I. S., Gilliham, M., Jha, D., Mayo, G. M., Roy, S. J., Coates, J. C., Haseloff, J., & Tester, M. (2009). Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. The Plant Cell, 21, 2163–2178.

    Article  CAS  Google Scholar 

  • Muhlenbock, P., Plaszczyca, M., Plaszczyca, M., Mellerowicz, E., & Karpinski, S. (2007). Lysigenous aerenchyma formation in Arabidopsis is controlled by lesion simulating disease. The Plant Cell, 19, 3819–3830.

    Article  CAS  Google Scholar 

  • Nawaz, T., Hameed, M., Waqar-U-Nisa, A., & M. S. A., Younis, A., & Kanwal, H. . (2012). Comparative anatomy of root and stem of some native and exotic Asparagus L. species. Pakistan Journal of Botany, 44, 153–158.

    Google Scholar 

  • Omamt, E. N., Hammes, P. S., & Robbertse, P. J. (2006). Differences in salinity tolerance for growth and water-use efficiency in some amaranth (Amaranthus spp.) genotypes. New Zealand Journal of Crop and Horticultural Science, 34, 11–22.

    Article  Google Scholar 

  • Piwpuan, N., Zhai, X., & Brix, H. (2013). Nitrogen nutrition of Cyperus laevigatus and Phormium tenax: Effects of ammonium versus nitrate on growth, nitrate reductase activity and N uptake kinetics. Aquatic Botany, 106, 42–51.

    Article  CAS  Google Scholar 

  • Qados, A. M. S. A. (2015). Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). Journal of the Saudi Society of Agricultural Sciences, 1, 7–15.

    Google Scholar 

  • Ruzin, S. E. (1999). Plant microtechnique and microscopy. Oxford University Press.

    Google Scholar 

  • Shimamura, S., Yamamoto, R., Nakamura, T., Shimada, S., & Komatsu, S. (2010). Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Annals of Botany, 106, 277–284.

    Article  Google Scholar 

  • Smith, M. S., Fridley, J. D., Yin, J., & Bauerle, T. L. (2013). Contrasting xylem vessel constraints on hydraulic conductivity between native and non-native woody understory species. Frontiers in Plant Sciences, 4, 1–12.

    Google Scholar 

  • Stoeva, N., & Kaymakanova, M. (2008). Effect of salt stress on the growth and photosynthesis rate of bean plants (Phaseolus vulgaris L.). Journal of Central European Agriculture, 9, 385–391.

    Google Scholar 

  • Takahashi, H., Yamauchi, T., Colmer, T. D., & Nakazono, M. (2014). Aerenchyma formation in plant. In: Low-oxygen stress in plants, oxygen sensing and adaptive responses to hypoxia. van Dongen, J.T., Licausi, F. (Eds.), Plant Cell Monographs (Vol. 21, 247−265). Springer.

  • Tavakkoli, E., Rengasamy, P., & McDonald, G. K. (2012). High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. Journal of Experimental Botany, 61, 4449–4459.

    Article  CAS  Google Scholar 

  • Uddin, S. J., Mondal, K., Shilpi, J. A., & Rahnan, M. T. (2006). Antidiarrhoeal activity of Cyperus rotundus. Fitoterapia, 77, 134–143.

    Article  CAS  Google Scholar 

  • Wolf, B. (1982). A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Communications in Soil Science and Plant Analysis, 13, 1035–1059.

    Article  CAS  Google Scholar 

  • Xu, Z., & Zhou, G. (2008). Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany, 59, 3317–3325.

    Article  CAS  Google Scholar 

  • Yemm, E. W., & Willis, A. J. (1954). The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal, 57, 508–514.

    Article  CAS  Google Scholar 

  • Younis, A., Riaz, A., Ahmed, I., Siddique, M. I., Tariq, U., Hameed, M., & Nadeem, M. (2014). Anatomical changes induced by NaCl stress in root and stem of Gazania harlequin L. Agricultural Communications, 2, 8–14.

    Google Scholar 

Download references

Acknowledgements

This manuscript is a part of the Ph. D. research of Sahar Mumtaz submitted to the Department of Botany, University of Agriculture, Faisalabad.

Author information

Authors and Affiliations

Authors

Contributions

Sahar Mumtaz conducted the experiment. Mansoor Hameed and Farooq Ahmad supervised the research work. Muhammad Sajid Aqeel Ahmad analyzed the data statistically and performed the multivariate analysis. Iftikhar Ahmad and Muhammad Hamzah Saleem were involved in the preparation of the manuscript. Muhammad Ashraf proofread is the group leader and finally edited the scientific and English language.

Corresponding author

Correspondence to Mansoor Hameed.

Ethics declarations

Ethics Approval

The manuscript was submitted solely to Water, Air and Soil Pollution and no part was published or submitted elsewhere. All ethical guidelines set by parent institution(s) were observed during sampling and analysis.

Consent to Participate and Publish

All authors equally participated in the execution of the experiment and unanimously agreed to publish in Environmental Science and Pollution Research.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mumtaz, S., Hameed, M., Ahmad, F. et al. Structural and Functional Determinants of Physiological Pliability in Kyllinga brevifolia Rottb. for Survival in Hyper-Saline Saltmarshes. Water Air Soil Pollut 232, 424 (2021). https://doi.org/10.1007/s11270-021-05391-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-05391-x

Keywords

Navigation