Abstract
Fimbristylis complanata manifests several biochemical and anatomical modifications to mitigate salinity-induced ionic disturbance. Three populations from salt-affected aquatic habitats were evaluated to assess degree of salinity tolerance and ion homeostasis. The collection sites were HR-Rasool headworks, LR-Lillah-Khewra foothills and SH-Sahianwala with ECe 19.45, 31.36 and 47.49 dS m−1, respectively. The populations were established in plastic containers and then three salt (NaCl) treatments (0, 200, 400 mM) were maintained. The experiment was laid in a completely randomized design (CRD) with three replicates. The SH population collected from hyper-saline habitat was the most salt tolerant mainly because of its capability to maintain root and shoot dry biomass accompanied by higher sequestration of Na+. Enhanced accumulation of Ca2+ and other key osmolytes in SH population played a key role in osmotic adjustments and maintenance of membrane integrity. The reduction in tissue K+ was observed in all populations due to the antagonistic effect of Na+. Anatomical traits like increased epidermal thickness and metaxylem area greatly contributed to ionic homeostasis in all three populations. The increase in anatomical traits was more pronounced in SH population. Increased leaf epidermal thickness in SH population was particularly helpful in tolerating low soil osmotic potentials by preventing water loss from the leaves. Increased aerenchyma in SH same population helped to store surplus water, salts and gases. These findings suggested that F. complanata exhibited enhanced salt tolerance by regulating the ion homeostasis and osmoregulation through a variety of morphological, biochemical and anatomical features.
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References
Adams E, Shin R (2014) Transport, signaling, and homeostasis of potassium and sodium in plants. J Integr Plant Biol 56:231–249. https://doi.org/10.1111/jipb.12159
Ahmed M, Fahad S, Ali MA, Hussain S, Tariq M, Ilyas F, Ahmad S, Saud S, Hammad HM, Nasim W, Wu C (2021) Hydrogen sulfide: a novel gaseous molecule for plant adaptation to stress. J Plant Growth Regul 40:2485–2501. https://doi.org/10.1007/s00344-020-10284-0
Akcin TA, Akcin A, Yalcın E (2017) Anatomical changes induced by salinity stress in Salicornia freitagii (Amaranthaceae). Brazil J Bot 40:1013–1018. https://doi.org/10.1007/s40415-017-0393-0
Bertazzini M, Sacchi GA, Forlani G (2018) A differential tolerance to mild salt stress conditions among six Italian rice genotypes does not rely on Na+ exclusion from shoots. J Plant Physiol 226:145–153. https://doi.org/10.1016/j.jplph.2018.04.011
Butt MA, Zafar M, Ahmad M, Sultana S, Ullah F, Jan G, Irfan A, Naqvi ZSA (2018) Morpho-palynological study of Cyperaceae from wetlands of Azad Jammu and Kashmir using SEM and LM. Microsc Res Tech 81:458–468. https://doi.org/10.1002/jemt.22999
Chakraborty K, Basak N, Bhaduri D, Ray S, Vijayan J, Chattopadhyay K, Sarkar RK (2018) Ionic basis of salt tolerance in plants: nutrient homeostasis and oxidative stress tolerance. In: Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B (eds) Plant nutrients and abiotic stress tolerance. Springer, pp 325–336. https://doi.org/10.1007/978-981-10-9044-8_14
Chaudhary DR (2019) Ion accumulation pattern of halophytes. In: Hasanuzzaman M, Shabala S, Fujita M (eds) Halophytes and climate change: adaptive mechanisms and potential uses. CABI, p 137. https://doi.org/10.1079/9781786394330.0137
de Bang TC, Husted S, Laursen KH, Persson DP, Schjoerring JK (2021) The molecular–Physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol 229:2446–2469. https://doi.org/10.1111/nph.17074
Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Phil Tran Royal Soc B: Biol Sci 367:547–555. https://doi.org/10.1098/rstb.2011.0272
Dubois M, Gilles K, Hamilton J, Rebers P, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167–167. https://doi.org/10.1038/168167a0
Durand M, Brendel O, Buré C, Le Thiec D (2020) Changes in irradiance and vapour pressure deficit under drought induce distinct stomatal dynamics between glasshouse and field-grown poplars. New Phytol 227:392–406. https://doi.org/10.1111/nph.16525
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115:327–331. https://doi.org/10.1093/aob/mcu267
Hameed M, Nawaz T, Ashraf M, Tufail A, Kanwal H, Ahmad MSA, Ahmad I (2012) Leaf anatomical adaptations of some halophytic and xerophytic sedges of the Punjab. Pak J Bot 44:159–164
Haque MI, Rathore MS, Gupta H, Jha B (2017) Inorganic solutes contribute more than organic solutes to the osmotic adjustment in Salicornia brachiata (Roxb.) under natural saline conditions. Aquat Bot 142:78–86. https://doi.org/10.1016/j.aquabot.2017.07.004
Hasanuzzaman M, Inafuku M, Nahar K, Fujita M, Oku H (2021) Nitric oxide regulates plant growth, physiology, antioxidant defense, and ion homeostasis to confer salt tolerance in the mangrove species Kandelia Obovata. Antioxidants 10:611. https://doi.org/10.3390/antiox10040611
Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80. https://doi.org/10.3389/fpls.2019.00080
Jacobsen AL, Ewers FW, Pratt RB, Paddock WA, Davis SD (2005) Do xylem fibers affect vessel cavitation resistance? Plant Physiol 139:546–556. https://doi.org/10.1104/pp.104.058404
Khan MA, Qaiser M (2006) Halophytes of Pakistan: characteristics, distribution and potential economic usages. In: Sabkha ecosystems. Springer, pp 129–153. https://doi.org/10.1007/978-1-4020-5072-5_11
Kowalenko C, Lowe L (1973) Determination of nitrates in soil extracts. Soil Sci Soc Am J 37:660–660
Kumari R, Kumar P, Meghawal D, Sharma V, Kumar H (2019) Salt-tolerance mechanisms in plants. In: Recent trends in tropical plant research. AkiNik Publications, New Delhi
Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495:286–291. https://doi.org/10.1016/j.bbrc.2017.11.043
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Mansour E, Moustafa ES, Desoky ESM, Ali M, Yasin MA, Attia A, Alsuhaibani N, Tahir MU, El-Hendawy S (2020) Multidimensional evaluation for detecting salt tolerance of bread wheat genotypes under actual saline field growing conditions. Plants 9:1324. https://doi.org/10.3390/plants9101324
Meychik NR, Nikolaeva YI, Yermakov IP (2013) Physiological response of halophyte (Suaeda altissima (L.) Pall.) and glycophyte (Spinacia oleracea L.) to salinity. Am J Plant Sci 4:427–435. https://doi.org/10.4236/ajps.2013.42A055
Mignolli F, Todaro JS, Vidoz ML (2020) Internal aeration and respiration of submerged tomato hypocotyls are enhanced by ethylene-mediated aerenchyma formation and hypertrophy. Physiol Plant 169:49–63. https://doi.org/10.1111/ppl.13044
Moore S, Stein WH (1948) Photometric nin-hydrin method for use in the ehromatography of amino acids. J Biol Chem 176:367–388
Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev 82:371–406. https://doi.org/10.1007/s12229-016-9173-y
Mumtaz S, Saleem MH, Hameed M, Batool F, Parveen A, Amjad SF, Mahmood A, Arfan M, Ahmed S, Yasmin H, Alsahli AA (2021) Anatomical adaptations and ionic homeostasis in aquatic halophyte Cyperus laevigatus L. under high salinities. Saudi J Biol Sci 28:2655–2666. https://doi.org/10.1016/j.sjbs.2021.03.002
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49. https://doi.org/10.1111/nph.12613
Phandee S, Hwan-air W, Soonthornkalump S, Jenke M, Buapet P (2022) Experimental flooding modifies rhizosphere conditions, induces photoacclimation and promotes antioxidant activities in Rhizophora mucronata seedlings. Bot Marina 65:1–12. https://doi.org/10.1515/bot-2021-0051
Pongrac P et al (2013) On the distribution and evaluation of Na, Mg and Cl in leaves of selected halophytes. Nuclear Inst Methods Phys Res Sect b Beam Int Mater Atom 306:144–149. https://doi.org/10.1016/j.nimb.2012.12.057
Rancic D, Pecinar I, Acic S, Stevanovic ZD (2019) 10 Morpho-anatomical traits of halophytic species. Halophytes and climate change: adaptive mechanisms and potential uses: CABI 152
Reef R, Lovelock CE (2015) Regulation of water balance in mangroves. Ann Bot 115:385–395. https://doi.org/10.1093/aob/mcu174
Safdar H, Amin A, Shafiq Y, Ali A, Yasin R, Shoukat A, Ul Hussan M, Sarwar MI (2019) A review: impact of salinity on plant growth. Nat Sci 17:34–40. https://doi.org/10.7537/marsnsj170119.06
Sims JR, Haby VA (1971) Simplified colorimetric determination of soil organic matter. Soil Sci 112:137–141
Singhal VP, Mehar SK (2020) Effect of limited nutrient availability on the development and relevance of root cortical aerenchyma. Plant Arch 20:1284–1288
Siwakoti M, Tiwari S (2007) Emerging needs of wetlands protection for the conservation of wild rice biodiversity in Nepal: A case study from Lumbini area Sci. World 5:95–99. https://doi.org/10.3126/sw.v5i5.2664
Sofy MR, Elhawat N, Alshaal T (2020) Glycine betaine counters salinity stress by maintaining high K+/Na+ ratio and antioxidant defense via limiting Na+ uptake in common bean (Phaseolus vulgaris L.). Ecotoxicol Environ Safety 200:110732. https://doi.org/10.1016/j.ecoenv.2020.110732
Surówka E, Hura T (2020) Osmoprotectants and nonenzymatic antioxidants in halophytes. In: Grigore MN (ed) Handbook of halophytes: from molecules to ecosystems towards Biosaline Agriculture. Springer, Cham, pp 1–31. https://doi.org/10.1007/978-3-030-57635-6_78
Tran DQ, Konishi A, Cushman JC, Morokuma M, Toyota M, Agarie S (2020) Ion accumulation and expression of ion homeostasis-related genes associated with halophilism, NaCl-promoted growth in a halophyte Mesembryanthemum crystallinum L. Plant Prod Sci 23:91–102. https://doi.org/10.1080/1343943X.2019.1647788
U.S. Salinity Laboratory Staff (1954) Diagnosis and improvement of saline and alkali soils. USDA agricultural handbook No 60. USDA, Washington DC, p 160
Volkov V (2015) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci 6:873. https://doi.org/10.3389/fpls.2015.00873
Wafa’a A, Gabr DG, (2017) Comparative morphological and anatomical characters of Cakile arabica from different habitat in eastern region of Saudi Arabia. Saudi J Biol Sci 24:226–233. https://doi.org/10.1016/j.sjbs.2016.04.009
Wolf B (1982) An improved universal extracting solution and its use for diagnosing soil fertility. Commun Soil Sci Plant Analysis 13:1005–1033. https://doi.org/10.1080/00103628209367331
Xu D et al (2017) Calcium alleviates decreases in photosynthesis under salt stress by enhancing antioxidant metabolism and adjusting solute accumulation in Calligonum mongolicum. Conserv Physiol 5:cox060. https://doi.org/10.1093/conphys/cox060
Yamada M, Kuroda C, Fujiyama H (2016) Function of sodium and potassium in growth of sodium-loving Amaranthaceae species. Soil Sci Plant Nutr 62:20–26. https://doi.org/10.1080/00380768.2015.1075365
Yoshida S, Forno DA, Cock JH (1971) Laboratory manual for physiological studies of rice. IRRI, Los Banos
Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci 7:977. https://doi.org/10.3389/fpls.2016.00977
Zahoor I, Ahmad MSA, Hameed M, Nawaz T, Tarteel A (2012) Comparative salinity tolerance of Fimbristylis dichotoma (L.) Vahl and Schoenoplectus juncoides (Roxb.) Palla, the candidate sedges for rehabilitation of saline wetlands. Pak J Bot 44:1–6
Zhang LX, Lai JH, Liang ZS, Ashraf M (2014) Interactive effects of sudden and gradual drought stress and foliar-applied glycinebetaine on growth, water relations, osmolyte accumulation and antioxidant defence system in two maize cultivars differing in drought tolerance. J Agron Crop Sci 200:425–433. https://doi.org/10.1111/jac.12081
Zhao C, Zhang H, Song C, Zhu JK, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. Innovation 1:100017
Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, Zhang X, Zhou Z, Dai S (2016) Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses. Sci Rep 6:32717. https://doi.org/10.1038/srep32717
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Kaleem, M., Hameed, M., Ahmad, F. et al. Anatomical and physiological features modulate ion homeostasis and osmoregulation in aquatic halophyte Fimbristylis complanata (Retz.) link. Acta Physiol Plant 44, 59 (2022). https://doi.org/10.1007/s11738-022-03400-y
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DOI: https://doi.org/10.1007/s11738-022-03400-y