Abstract
When exposed to dry conditions, plants become cognizant of desiccation signal and transfer it to cellular machinery to activate responses for adaptation. For protection against the injurious effects of desiccation inside the cells, lower plants have typical defense mechanism. Although bryophyte possesses capability to tolerate desiccation, yet unfavourable environmental conditions may be the reason for irreversible dryness of these miniature plants. Hence, the genera which are tolerant to desiccation have to be compelled to be recognised and propagated to conserve some precursor colonisers of ecosystem naturally. This study explores the effect of different desiccation levels in plants of Semibarbula orientalis collected from two locations. The two populations showed difference in the expression of antioxidative enzymes as well as photosynthetic pigments in their respective controls. Maximum increment in peroxidase activity was observed in 72 h desiccated plants, which was 59% higher in site 1, and 484% in site 2, than their respective controls. In the plants of site 2, maximum value (about 105% higher than control) of superoxide dismutase was seen at 48 h desiccation. However, a gradual decrement was observed in catalase, as the duration of desiccation increased. Highest value of chlorophyll content was seen at 48 h desiccation which was about 294% higher for chl a, 387% for chl b and 372% for total chl in site 1, whereas plants of site 2 revealed 269% increment in chl a, 1042% in chl b and 803% in total chl, than their respective controls. Our results are often explained on the premise of relationship between desiccation tolerance and atmospheric moisture (relative humidity), as the rate of desiccation has been reported to be faster at lower relative humidity and vice versa. Hence it is suggested that, desiccation and rehydration are not merely indicative of removal and addition of water, but also include a sequence of physiological and biochemical events, and the efficiency of such changes in different populations, under different environmental conditions highlights variation in the inducible response strategy.
Similar content being viewed by others
References
Alberte, R. S., Mcclure, P. R., & Thornber, J. P. (1976). Photosynthesis in trees: Organization of chlorophyll and photosynthetic unit size in isolated gymnosperm chloroplasts. Plant Physiology, 59, 351–353.
Alpert, P. (2005). The limits and frontiers of desiccation-tolerant life. Integrative and Comparative Biology, 45, 85–695.
Alpert, P. (2006). Constraints of tolerance: Why are desiccation-tolerant organisms so small or rare? Journal of Experimental Biology, 209, 1575–1584.
Alpert, P., & Oechel, W. C. (1987). Comparative patterns of net photosynthesis in an assemblage of mosses with contrasting micro distributions. American Journal of Botany, 74, 1787–1796.
Alpert, P., & Oliver, M. J. (2002). Drying without dying. In M. Black & H. W. Pritchard (Eds.), Desiccation and survival in plants: Drying without dying (pp. 3–43). Wallingford: CABI Publishing.
Arnon, D. I. (1949). Copper enzyme polyphenoloxides in isolated chloroplast in Beta vulgaris. Plant Physiology, 24, 1–15.
Ashraf, M., & Harris, P. J. C. (2013). Photosynthesis under stressful environments: An overview. Photosynthetica, 51, 163–190.
Bansal, P., & Srivastava, A. (2017). Desiccation-related responses of antioxidative enzymes and photosynthetic pigments in Brachythecium procumbens (Mitt.) A. Jaeger. Acta Physiologiae Plantarum, 39, 154.
Beauchamp, C., & Fridovich, I. (1971). Superoxide Dismutase: Improved assay and an application to acrylamide gels. Analytical Biochemistry, 44, 276–287.
Beckett, R. P. (1999). Partial dehydration and ABA induce tolerance to desiccation-induced ion leakage in the moss Atrichum androgynum. South African Journal of Botany, 65, 1–6.
Beckett, R. P., & Minibayeva, F. V. (2007). Rapid breakdown of exogenous extracellular hydrogen peroxide by lichens. Physiologia Plantarum, 129, 588–596.
Bramley-Alves, J., King, D. H., Robinson, S. A., & Miller, R. E. (2014). Dominating the Antarctic environment: Bryophytes in a time of change. Advances in Photosynthesis and Respiration, 37, 309–324.
Brinda, J. C., Stark, L. R., Clark, T. A., & Greenwood, J. L. (2016). Embryos of a moss can be hardened to desiccation tolerance: Effects of rate of drying on the timeline of recovery and dehardening in Aloina ambigua (Pottiaceae). Annals of Botany, 117, 153–163.
Castillo, F. J. (1996). Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery. Oecologia, 107, 469–477.
Cruz de Carvalho, R., Branquinho, C., & Marques da Silva, J. (2011). Physiological consequences of desiccation in the aquatic bryophyte Fontinalis antipyretica. Planta, 234, 195–205.
Cruz de Carvalho, R., Branquinho, C., & Marques da Silva, J. (2019). Desiccation rate affects chlorophyll and carotenoid content and the recovery of the aquatic moss Fontinalis antipyretica (Fontinalaceae). Hattoria, 10, 53–60.
Cruz de Carvalho, R., Catalá, M., Branquinho, C., Marques da Silva, J., & Barreno, E. (2017). Dehydration rate determines the degree of membrane damage and desiccation tolerance in bryophytes. Physiologia Plantarum, 159, 277–289.
Cruz de Carvalho, R., Silva, A. B., Soares, R., Almeida, A., Coelho, A. V., Marques da Silva, J., et al. (2014). Differential proteomics of dehydration and rehydration in bryophytes: Evidence towards a common desiccation tolerance mechanism. Plant, Cell and Environment, 37, 1499–1515.
Dhindsa, R. S. (1987). Glutathione status and protein synthesis during drought and subsequent rehydration of Tortula ruralis. Plant Physiology, 83, 816–819.
Du, H., Wang, N. L., Cui, F., Li, X. H., Xiao, J. H., & Xiong, L. Z. (2010). Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiology, 154, 1304–1318.
Euler, H. V., & Josephson, K. (1927). Uber katalase. I. Justus Liebigs Annalen der Chemie, 452, 158–181.
Francini, A., Galleschi, L., Saviozzi, F., Pinzino, C., Izzo, R., Sgherri, C., et al. (2006). Enzymatic and non-enzymatic protective mechanisms in recalcitrant seeds of Araucaria bidwillii subjected to desiccation. Plant Physiology and Biochemistry, 44, 556–563.
Glime, J. M. (2017a). Adaptive Strategies: Growth and Life Forms. In J. M. Glime (Ed.), Bryophyte Ecology (Vol. 1, pp. 1–21). Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists.
Glime, J. M. (2017b). Water relations: Biochemical adaptations to drying. In J. M. Glime (Ed.), Bryophyte ecology (Vol. 1, pp. 1–14). Physiological ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists.
Grieco, M., Jain, A., Ebersberger, I., & Teige, M. (2016). An evolutionary view on thylakoid protein phosphorylation uncovers novel phosphorylation hotspots with potential functional implications. Journal of Experimental Botany, 67, 3883–3896.
Horsley, K., Stark, L. R., & McLetchie, D. N. (2011). Does the silver moss Bryum argenteum exhibit sex-specific patterns in vegetative growth rate, asexual fitness or prezygotic reproductive investment? Annals of Botany, 107, 897–907.
Hörtensteiner, S. (2006). Chlorophyll degradation during senescence. Annual Review of Plant Biology, 57, 55–77.
Hutsemekers, V., Hardy, O. J., Mardulyn, P., Shaw, A. J., & Vanderpoorten, A. (2010). Macroecological patterns of genetic structure and diversity in the aquatic moss Platyhypnidium riparioides. New Phytologist, 185, 852–864.
Kholová, J., Hash, C. T., Kočova, M., & Vadez, V. (2011). Does a terminal drought tolerance QTL contribute to differences in ROS scavenging enzymes and photosynthetic pigments in pearl millet exposed to drought? Environmental and Experimental Botany, 71, 99–106.
Lubaina, A. S., Meenu Krishnan, V. G., & Murugan, K. (2013). Induction of oxidative stress and antioxidative response mechanisms in Octoblepharum albidum Hedw. a bryophyte under desiccation-rehydration stress. Indian Journal of Plant Sciences, 2, 12–22.
Luck, M. (1963). Peroxidase. In H. V. Bergmeyer (Ed.), Methods of enzymic analysis (pp. 895–897). New York: Academic Press.
Martin, C. E. (1980). Chlorophyll a/b ratios of eleven North Carolina mosses. Bryologist, 83, 84–87.
Masoumi, H., Darvish, F., Daneshian, J., Ghorban, N., & Habibi, D. (2011). Effects of water deficit stress on seed yield and antioxidants content in soybean (Glycine max L.) cultivars. African Journal of Agricultural Research, 6, 1209–1218.
Mayaba, N., & Beckett, R. (2003). Increased activities of superoxide dismutase and catalase are not the mechanism of desiccation tolerance induced by hardening in the moss Atrichum androgynum. Journal of Bryology, 25, 281–286.
Mayaba, N., Beckett, R. P., Csintalan, Z., & Tuba, Z. (2001). ABA increases the desiccation tolerance of photosynthesis in the afromontane understory moss Atrichum androgynum. Annals of Botany, 86, 1093–1100.
Mikulášková, E., Hájek, M., Veleba, A., Johnson, M. G., Hájek, T., & Shaw, J. A. (2015). Local adaptations in bryophytes revisited: The genetic structure of the calcium-tolerant peatmoss Sphagnum warnstorfii along geographic and pH gradients. Ecology and Evolution, 5, 229–242.
Millan-Almaraz, J. R., Guevara-Gonzalez, R. G., Romero-Troncoso, R., Osornio-Rios, R. A., & Torres-Pacheco, I. (2009). Advantages and disadvantages on photosynthesis measurement techniques: A review. African Journal of Biotechnology, 8, 7340–7349.
Minibayeva, F., & Beckett, R. P. (2001). High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation. New Phytologist, 152, 333–341.
Núñez-Olivera, E., Otero, S., Tomás, R., & Martínez-Abaigar, J. (2009). Seasonal variations in UV-absorbing compounds and physiological characteristics in the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia over a 3-year period. Physiologia Plantarum, 136, 73–85.
Oliver, M. J. (1996). Desiccation-tolerance in vegetative plant cells. Physiologia Plantarum, 97, 779–787.
Platt, K. A., Oliver, M. J., & Thomson, W. W. (1994). Membranes and organelles of dehydrated Selaginella and Tortula retain their normal configuration and structural integrity: Freeze fracture evidence. Protoplasma, 178, 57–65.
Pressel, S., & Duckett, J. G. (2010). Cytological insights into the desiccation biology of a model system: Moss protonemata. New Phytol, 185, 944–963.
Pressel, S., Ligrone, R., & Duckett, J. G. (2006). Effects of de- and rehydration on food-conducting cells in the moss Polytrichum formosum: A cytological study. Annals of Botany, 98, 67–76.
Proctor, M. C. F. (2001). Patterns of desiccation tolerance and recovery in bryophytes. Plant Growth Regulation, 35, 147–156.
Proctor, M. C. F. (2004). How long must a desiccation-tolerant moss tolerate desiccation? Some results of 2 years’ data logging on Grimmia pulvinata. Physiologia Plantarum, 122, 21–27.
Proctor, M. C. F., Ligrone, R., & Duckett, J. G. (2007a). Desiccation tolerance in the moss Polytrichum formosum: Physiological and fine-structural changes during desiccation and recovery. Annals of Botany, 99, 75–93.
Proctor, M. C. F., Oliver, M. J., Wood, A. J., Alpert, P., Stark, L. R., Cleavitt, N. L., et al. (2007b). Desiccation-tolerance in bryophytes: A review. Bryologist, 110, 595–621.
Proctor, M. C. F., & Pence, V. C. (2002). Vegetative tissues: Bryophytes, vascular resurrection plants and vegetative propagules. In H. Pritchard & M. Black (Eds.), Desiccation and plant survival (pp. 207–237). Wallingford: CABI Publishing.
Sairam, R. K., Shukla, D. S., & Saxena, D. C. (1997). Stress induced injury and antioxidant enzymes in relation to drought tolerance in wheat genotypes. Biological Plantarum, 40, 357–364.
Schlensog, M., Green, T. G. A., & Schroeter, B. (2013). Life form and water source interact to determine active time and environment in cryptogams: An example from the maritime Antarctic. Oecologia, 173, 59–72.
Schonbeck, M. W., & Bewley, J. D. (1981a). Responses of the moss Tortula ruralis to desiccation treatments. I. Effects of minimum water content and rates of dehydration and rehydration. Canadian Journal of Botany, 59, 2698–2706.
Schonbeck, M. W., & Bewley, J. D. (1981b). Responses of the moss Tortula ruralis to desiccation treatments. II. Variations in desiccation tolerance. Canadian Journal of Botany, 59, 2707–2712.
Seel, W. E., Hendry, G. A. F., & Lee, J. A. (1992). Effects of desiccation on some activated oxygen processing enzymes and antioxidants in mosses. Journal of Experimental Botany, 43, 1031–1037.
Shaw, B., Thomas, T. H., & Cooke, D. T. (2002). Responses of sugar beet (Beta vulgaris L.) to drought and nutrient deficiency stress. Plant Growth Regulation, 37, 77–83.
Soltys-Kalina, D., Plich, J., Strzelczyk-Żyta, D., Śliwka, J., & Marczewski, W. (2016). The effect of drought stress on the leaf relative water content and tuber yield of a half-sib family of Katahdin-derived potato cultivars. Breeding Science, 66, 328–331.
Stark, L. R. (2005). Phenology of patch hydration, patch temperature and sexual reproductive output over a four-year period in the desert moss Crossidium crassinerve. Journal of Bryology, 27, 231–240.
Stark, L. R. (2017). Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology. Bryologist, 120, 130–165.
Stark, L. R., & Brinda, J. C. (2015). Developing sporophytes transition from an inducible to a constitutive ecological strategy of desiccation tolerance in the moss Aloina ambigua: Effects of desiccation on fitness. Annals of Botany, 115, 593–603.
Stark, L. R., Greenwood, J. L., & Brinda, J. C. (2017). Desiccated Syntrichia ruralis shoots regenerate after 20 years in the herbarium. Journal of Bryology, 39, 85–93.
Stark, L. R., Greenwood, J. L., Brinda, J. C., & Oliver, M. J. (2013). The desert moss Pterygoneurum lamellatum exhibits inducible desiccation tolerance: Effects of rate of drying on shoot damage and regeneration. American Journal of Botany, 100, 1522–1531.
Stark, L. R., Greenwood, J. L., Brinda, J. C., & Oliver, M. J. (2014). Physiological history may mask the inherent inducible desiccation tolerance strategy of the desert moss Crossidium crassinerve. Plant Biology, 16, 935–946.
Toldi, O., Tuba, Z., & Scott, P. (2009). Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops? Plant Science, 176, 187–199.
Tuba, Z., Csintalan, Z., & Proctor, M. C. F. (1996). Photosynthetic responses of a moss, Tortula ruralis ssp. ruralis, and the lichens Cladonia convoluta and C. furcata to water deficit and short periods of desiccation, and their ecophysiological significance: A baseline study at present-day CO2 concentration. New Phytologist, 133, 353–361.
Türkan, İ., Bor, M., Özdemir, F., & Koca, H. (2005). Differential responses of lipid peroxidation and antioxidants in the leaves of drought tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science, 168, 223–231.
Wang, X., Liu, Z., & He, Y. (2008). Responses and tolerance to salt stress in bryophytes. Plant Signaling & Behavior, 3, 516–518.
Werner, O., Espin, R. M. R., Bopp, M., & Atzorn, R. (1991). Abscisic acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta, 186, 99–103.
Wood, A. J. (2007). The nature and distribution of vegetative desiccation tolerance in hornworts, liverworts and mosses. Bryologist, 110, 163–177.
Acknowledgements
Both the authors thank the University Grants Commission (U.G.C.), New Delhi for financial assistance [F.4-2/2006(BSR)/BL/13-14/0375].
Author information
Authors and Affiliations
Contributions
PB executed the experiments, and prepared first draft of the manuscript. AS outlined the experiment and monitored its proper execution, and helped in final preparation of manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bansal, P., Srivastava, A. An adaptive inducible ecological tolerance strategy of Semibarbula orientalis (Web.) Wijk. & Marg. to desiccation stress. Plant Physiol. Rep. 25, 460–471 (2020). https://doi.org/10.1007/s40502-020-00530-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40502-020-00530-8