Abstract
Finger millet is an important cereal that is grown in semi-arid and arid regions of East-Africa. Salinity stress is a major environmental impediment for the crop growth and production. This study aimed to understand the physiological and biochemical responses to salinity stress of six Kenyan finger millet varieties (GBK043137, GBK043128, GBK043124, GBK043122, GBK043094, GBK043050) grown across different agroecological zones under NaCl-induced salinity stress (100, 200 and 300 mM NaCl). Seeds were germinated on the sterile soil and treated using various concentrations of NaCl for 2 weeks. Early-seedling stage of germinated plants were irrigated with the same salt concentrations for 60 days. The results indicated depression in germination percentage, shoot and root growth rate, leaf relative water content, chlorophyll content, leaf K+ concentration, and leaf K+/Na+ ratios with increased salt levels and the degree of increment differed among the varieties. On the contrary, the content of proline, malonaldehyde, leaf total proteins, and reduced sugar increased with increasing salinity. At the same time, the leaf Na+ and Cl− amounts of all plants increased substantially with increasing stress levels. Clustering analysis placed GBK043094 and GBK043137 together and these varieties were identified as salt-tolerant based on their performance. Taken together, our findings indicated a significant varietal variability for most of the parameters analysed. The superior varieties identified could be used as promising genetic resources in future breeding programmes directed towards development of salt-tolerant finger millet hybrids. Further analysis at genomic level needs to be undertaken to better understand the genetic factors that promote salinity tolerance in finger millet.
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Ahmed S, Ahmed S, Roy SK, Woo SH, Sonawane KD, Shohael AM (2019) Effect of salinity on the morphological, physiological and biochemical properties of lettuce (Lactuca sativa L.) in Bangladesh. Open Agric 4(1):361–373. https://doi.org/10.1515/opag-2019-0033
Al-Hassan M, del Pilar LM, Boscaiu M, Vicente O (2016) Stress tolerance mechanisms in Juncus: responses to salinity and drought in three Juncus species adapted to different natural environments. Funct Plant Biol 43:949–960. https://doi.org/10.1071/FP16007
Ali Y, Aslam Z, Ashraf MY, Tahir GR (2004) Effect of salinity on chlorophyll concentration, leaf area, yield and yield components of rice genotypes grown under saline environment. Int J Environ Sci Technol 1(3):221–225
Anuradha S, Rao SSR (2001) Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regul 33:151–153. https://doi.org/10.1023/A:1017590108484
Arnon D (1949) Copper enzyme in isolated chloroplast and chlorophyll expressed in terms of mg per gram. Plant Physiol 24:1–15
Asfaw E, Suryabhagavan KV, Argaw M (2018) Soil salinity modeling and mapping using remote sensing and GIS: the case of Wonji sugar cane irrigation farm, Ethiopia. J Saudi Soc Agric Sci 17(3):250–258. https://doi.org/10.1016/j.jssas.2016.05.003
Ashraf MY (1998) Effect of salinity on growth, chlorophyll content, and flag leaf area of rice (Oryza sativa L.) genotypes. Int Rice Res Notes 2:33–35
Ashraf MPJC, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16. https://doi.org/10.1016/j.plantsci.2003.10.024
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190
Ashraf M, Shahbaz M (2003) Assessment of genotypic variation in salt tolerance of early CIMMYT hexaploid wheat germplasm using photosynthetic capacity and water relations as selection criteria. Photosynthetica 41(2):273–280
Awana M, Yadav K, Rani K, Gaikwad K, Praveen S, Kumar S, Singh A (2019) Insights into salt stress-induced biochemical, molecular and epigenetic regulation of spatial responses in Pigeonpea (Cajanus cajan L.). Plant Growth Regul. https://doi.org/10.1007/s00344-019-09955-4
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
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. Plant Physiol 226:145–153. https://doi.org/10.1016/j.jplph.2018.04.011
Carillo P, Cirillo C, De Micco V, Arena C, de Pascale S, Rouphael Y (2019) Morpho-anatomical, physiological and biochemical adaptive responses to saline water of Bougainvillea spectabilis Willd. trained to different canopy shapes. Agric Water Manag 212:12–22. https://doi.org/10.1016/j.agwat.2018.08.037
Chen J, Zong J, Li D, Chen Y, Wang Y, Guo H, Li J, Li L, Guo A, Liu J (2019) Growth response and ion homeostasis in two bermudagrass (Cynodon dactylon) cultivars differing in salinity tolerance under salinity stress. Soil Sci Plant Nutr 65:419–429. https://doi.org/10.1080/00380768.2019.1631125
Cheng W, Zhang G, Yao H, Dominy P, Wu W, Wang R (2004) Possibility of predicting heavy-metal contents in rice grains based on DTPA-extracted levels in soil. Commun Soil Sci Plant Anal 35:2731–2745. https://doi.org/10.1081/CSS-200036424
Chivenge P, Mabhaudhi T, Modi A, Mafongoya P (2015) The potential role of neglected and underutilised crop species as future crops under water scarce conditions in Sub-Saharan Africa. Int J Environ Res Public Health 12:5685–5711. https://doi.org/10.3390/ijerph120605685
Cirillo C, De Micco V, Arena C, Carillo P, Pannico A, De Pascale S, Rouphael Y (2019) Biochemical, physiological and anatomical mechanisms of adaptation of callistemon citrinus and viburnum lucidum to NaCl and CaCl2 salinization. Front Plant Sci 10:742
Colla G, Rouphael Y, Rea E, Cardarelli M (2012) Grafting cucumber plants enhance tolerance to sodium chloride and sulfate salinization. Sci Hortic 135:177–185
Damerval C, de Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54. https://doi.org/10.1002/elps.1150070108
Dugasa MT, Cao F, Ibrahim W, Wu F (2019) Differences in physiological and biochemical characteristics in response to single and combined drought and salinity stresses between wheat genotypes differing in salt tolerance. Physiol Plant 165:134–143. https://doi.org/10.1111/ppl.12743
Eaton AD, Clesceri LS, Greenberg AE (1995) Standard methods for the examination of water and wastewater. American Public Health Association, Washington
Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Funct Plant Biol 13(1):75–91. https://doi.org/10.1071/PP9860075
Ganie SA, Molla KA, Henry RJ, Bhat KV, Mondal TK (2019) Advances in understanding salt tolerance in rice. Theor Appl Genet 132:851–870. https://doi.org/10.1007/s00122-019-03301-8
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hema R, Vemanna RS, Sreeramulu S, Reddy CP, Senthil KM, Udayakumar M (2014) Stable expression of mtlD gene imparts multiple stress tolerance in finger millet. PLoS ONE 9(6):e99110. https://doi.org/10.1371/journal.pone.0099110
Hussain MI, Al-Dakheel AJ, Reigosa MJ (2018) Genotypic differences in agro-physiological, biochemical and isotopic responses to salinity stress in quinoa (Chenopodium quinoa Willd.) plants: prospects for salinity tolerance and yield stability. Plant Physiol Biochem 129:411–420. https://doi.org/10.1016/j.plaphy.2018.06.023
Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46. https://doi.org/10.1016/j.jplph.2015.12.011
Ishikawa T, Shabala S (2019) Control of xylem Na+ loading and transport to the shoot in rice and barley as a determinant of differential salinity stress tolerance. Physiol Plant 165:619–631. https://doi.org/10.1111/ppl.12758
Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166(15):1587–1597
Johnson G, Lambert C, Johnson DKD, Sunderwirth SG (1964) Colorimetric determination of glucose, fructose, and sucrose in plant materials using a combination of enzymatic and chemical methods. J Agric Food Chem 12:216–219. https://doi.org/10.1021/jf60133a007
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487. https://doi.org/10.2135/cropsci2000.402482x
Kumar V, Khare T (2016) Differential growth and yield responses of salt-tolerant and susceptible rice cultivars to individual (Na+ and Cl−) and additive stress effects of NaCl. Acta Physiol Plant 38:1–9. https://doi.org/10.1007/s11738-016-2191-x
Kumar A, Metwal M, Kaur S, Gupta AK, Puranik S, Singh S, Singh M, Gupta S, Babu BK, Sood S, Yadav R (2016) Nutraceutical value of finger millet [Eleusine coracana (L.) Gaertn.], and their improvement using omics approaches. Front Plant Sci 7:934
Laghmouchi Y, Belmehdi O, Bouyahya A, Senhaji NS, Abrini J (2017) Effect of temperature, salt stress and pH on seed germination of medicinal plant Origanum compactum. Biocatal Agric Biotechnol 10:156–160. https://doi.org/10.1016/j.bcab.2017.03.002
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J stat softw 25(1):1–18
Li Y, Zhang T, Zhang Z, He K (2019) The physiological and biochemical photosynthetic properties of Lycium ruthenicum Murr in response to salinity and drought. Sci Hortic 256:1–9. https://doi.org/10.1016/j.scienta.2019.05.057
Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3(30):2–13. https://doi.org/10.3390/horticulturae3020030
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nawaz K, Ashraf M (2010) Exogenous application of glycinebetaine modulates activities of antioxidants in maize plants subjected to salt stress. J Agron Crop Sci 196(1):28–37
Neocleous D, Ntatsi G, Savvas D (2017) Physiological, nutritional and growth responses of melon (Cucumis melo L.) to a gradual salinity built-up in recirculating nutrient solution. J Plant Nutr 40(15):2168–2180. https://doi.org/10.1080/01904167.2017.1346673
Nxele X, Klein A, Ndimba BK (2017) Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. S Afr J Bot 108:261–266. https://doi.org/10.1016/j.sajb.2016.11.003
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. ESPR 22:4056–4075. https://doi.org/10.1007/s11356-014-3739-1
Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38:282–295. https://doi.org/10.1111/1477-8947.12054
Rao ES, Kadirvel P, Symonds RC, Ebert AW (2013) Relationship between survival and yield related traits in Solanum pimpinellifolium under salt stress. Euphytica 190(2):215–228
Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiologiae Plant 35(4):1039–1050
Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91. https://doi.org/10.1007/s10535-005-5091-2
Sandhu D, Cornacchione MV, Ferreira JF, Suarez DL (2017) Variable salinity responses of 12 alfalfa genotypes and comparative expression analyses of salt-response genes. Sci Rep 7:1–18. https://doi.org/10.1038/srep42958
Sarabi B, Bolandnazar S, Ghaderi N, Ghashghaie J (2017) Genotypic differences in physiological and biochemical responses to salinity stress in melon (Cucumis melo L.) plants: prospects for selection of salt tolerant landraces. Plant Physiol Biochem 119:294–311. https://doi.org/10.1016/j.plaphy.2017.09.006
Shabala S, Hariadi Y, Jacobsen SE (2013) Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. J Plant Physiol 170:906–914. https://doi.org/10.1016/j.jplph.2013.01.014
Soares AC, Geilfus CM, Carpentier SC (2018) Genotype-specific growth and proteomic responses of maize towards salt stress. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00661
Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte arabidopsis and the halophyte thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149(2):1154–1165
Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312. https://doi.org/10.1016/j.sajb.2016.03.011
Tounsi S, Feki K, Hmidi D, Masmoudi K, Brini F (2017) Salt stress reveals differential physiological, biochemical and molecular responses in T. monococcum and T. durum wheat genotypes. Physiol Mol Biol Plants 23:517–528. https://doi.org/10.1007/s12298-017-0457-4
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35(4):753–759
von Alvensleben N, Stookey K, Magnusson M, Heimann K (2013) Salinity tolerance of Picochlorum atomus and the use of salinity for contamination control by the freshwater cyanobacterium Pseudanabaena limnetica. PLoS ONE 8:e63569. https://doi.org/10.1371/journal.pone.0063569
Yang C, Shahidi F, Tsao R (2018) Biomarkers of oxidative stress and cellular-based assays of indirect antioxidant measurement. Meas Antioxid Act Capacity. https://doi.org/10.1002/9781119135388.ch9
Yeo AR, Lee λS, Izard P, Boursier PJ, Flowers TJ (1991) Short- and long-term effects of salinity on leaf growth in rice (Oryza sativa L.). J Exp Bot 42(7):881–889
Acknowledgements
This project was funded by The World Academy of Sciences grant (Ref. No. 17-357 RG/BIO/AF/AC_I—FR3240297745) through the generous contribution of the Swedish International Development Cooperation Agency. The authors thank the Kenyatta University and Pwani University for providing laboratory facilities. The authors gratefully acknowledge Kenya Agricultural and Livestock Research Organization, Gene Bank, for providing the finger millet seeds.
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AM, AN, WM designed and did the experiments performed data analyses. AM, WM wrote the draft manuscript. ES and RO revised and corrected the draft manuscript. WM conceptualized the idea and design, supervised the work and made critical review of the article.
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Mukami, A., Ng’etich, A., Syombua, E. et al. Varietal differences in physiological and biochemical responses to salinity stress in six finger millet plants. Physiol Mol Biol Plants 26, 1569–1582 (2020). https://doi.org/10.1007/s12298-020-00853-8
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DOI: https://doi.org/10.1007/s12298-020-00853-8