Discerning of Rice Landraces (Oryza sativa L.) for Morpho-physiological, Antioxidant Enzyme Activity, and Molecular Markers’ Responses to Induced Salt Stress at the Seedling Stage

Abstract

Salinity has been identified as key abiotic stress factor limiting rice production in many countries around the globe, including Bangladesh. In the present study, we examined the effects of salt-induced toxicity on growth of rice landraces for screening salt-tolerant genotypes by assessing morpho-physiological, biochemical, and molecular responses. Screening of 28 rice genotypes at seedling stage was performed at 12 dS m−1 salinity level in hydroponic media. Most of the rice genotypes showed an apparent reduction in growth traits, while a fewer showed less reduction under salinity stress. Euclidean clustering and heatmap based on morpho-physiological parameters dissected rice genotypes into three major clusters, viz., susceptible, moderately tolerant, and tolerant. Results of cluster analysis revealed Nonabokra, Hogla, Ghunsi, Holdegotal, Nonabokra, and Kanchon as salt-tolerant rice genotypes. These genotypes also were grouped using three microsatellite markers, viz., RM493, RM3412b, and RM140 that were closely linked to saltol QTL showed Hogla, Ghunsi, Holdegotal, Nonabokra, Kanchon, BINA dhan-8, and BINA dhan-10 as salt-tolerant genotypes considering genetic similarity in dendrogram. The positive relationships of Na+/K+ ratio with hydrogen peroxide (H2O2) and malondialdehyde (MDA), and antioxidant enzymes’ activity in the tolerant rice genotypes indicated their importance for improving salinity tolerance. The salt-tolerant landraces showed lower Na+/K+ ratio, high proline accumulation, lower H2O2 accumulation and MDA content, and higher catalase and ascorbate peroxidase activities. Higher antioxidant enzymes’ activity and lower H2O2 accumulation in tolerant genotypes indicate their abilities to fight against oxidative stress. Based on all morpho-physiological clustering, biochemical response, and molecular dendrogram, Nonabokra, Hogla, Ghunsi, Holdegotal, and Kanchon were identified as the salt-tolerant landraces. Therefore, these identified salt-tolerant landraces could be useful to improve breeding program for the development of salt-tolerant high-yielding rice cultivars in future.

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References

  1. AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:276

    PubMed  PubMed Central  Google Scholar 

  2. Abeer AR, Fatma AF, Afaf MH (2013) Physiological and biochemical responses of salt-tolerant and salt-sensitive wheat and bean cultivars to salinity. J Biol Earth Sci 3:B72–B88

    Google Scholar 

  3. Abu-Muriefah SS (2015) Effect of sitosterol on growth, metabolism and protein pattern of pepper (Capsicum Annuum L.) plants grown under salt stress conditions. Int J Agric Crop Sci 8:94–106

    CAS  Google Scholar 

  4. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  Google Scholar 

  5. Ahmad P, Jhon R, Sarwat M, Umar S (2008) Responses of proline, lipid peroxidation and antioxidative enzymes in two varieties of Pisum sativum L. under salt stress. Int J Plant Prod 2:353–366

    CAS  Google Scholar 

  6. Ahmed MF, Haider MZ (2014) Impact of salinity on rice production in the south-west region of Bangladesh. Environ Sci Ind J 9:135–141

    Google Scholar 

  7. Akhzari D, Sepehry A, Pessarakli M, Barani H (2012) Studying the effects of salinity stress on the growth of various halophytic plant species (Agropyron elongatum, Kochia prostrata and Puccinellia distans). World Appl Sci J 16:998–1003

    Google Scholar 

  8. Akram S, Siddiqui MN, Nahid Hussain BM, Bari MA, Mosofa MG, Hossain MA, Tran LSP (2017) Exogenous glutathione modulates salinity tolerance of soybean [Glycine max (L.) Merrill] at reproductive stage. J Plant Growth Regul 36:877–888

    CAS  Google Scholar 

  9. Ali MN, Yeasmin L, Gantait S, Goswami R, Chakraborty S (2014) Screening of rice landraces for salinity tolerance at seedling stage through morphological and molecular markers. Physiol Mol Biol Plants 20:411–423

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Almeida DM, Oliveira MM, Saibo NJM (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genet Mol Biol 40:326–345

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Amirjani MR (2011) Effect of salt stress on growth, sugar content, pigment and enzyme activities in rice. Int J Bot 7:73–81

    CAS  Google Scholar 

  12. Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan EA, Kachhap K, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase-representative H2O2-detoxifying heme enzymes in plants. Environ Sci Pollut Res 23:19002–19029

    CAS  Google Scholar 

  13. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ashraf M, Foolad MR (2007) Roles of glycinebetaine and proline in improving plant abiotic stress tolerance. Environ Exp Bot 59:206–216

    CAS  Google Scholar 

  15. Ashraf M, Harris P (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    CAS  Google Scholar 

  16. Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Rev Plant Sci 23:157–174

    CAS  Google Scholar 

  17. Assaha DVM, Ueda A, Saneoka H, Yahyai RA, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:509

    PubMed  PubMed Central  Google Scholar 

  18. Azuma R, Ito N, Nakayama N, Suwa R, Nguyen NT, Larrinaga-Mayoral JA, Esaka M, Fujiyama H, Saneoka H (2010) Fruits are more sensitive to salinity than leaves and stems in pepper plants (Capsicum Annuum L.). Sci Hortic 125:171–178

    CAS  Google Scholar 

  19. Bangladesh Bureau of Statistics (BBS) (2016) Yearbook of agricultural statistics of Bangladesh 2015. Statistical division, Ministry of Planning, Government of the People’s Republic of Bangladesh, Dhaka

  20. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  21. Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Essah PA, Tester T, Ve´ry AA, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative dmage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Brown ID, Lilleland O (1946) Determination of potassium and sodium in plant material and soil extracts by flamephotometry. Proc Amer Soc Hort Sci 48:341–346

    CAS  Google Scholar 

  24. Chakravarthi BK, Naravaneni R (2006) SSR marker based DNA fingerprinting and diversity study in rice (Oryza sativa L). Afr J Biotechnol 5:684–688

    CAS  Google Scholar 

  25. Chattopadhyay K, Nath D, Mohanta RL, Bhattacharyya S, Marndi BC, Nayak AK, Singh DP, Sarkar RK, Singh ON (2014) Diversity and validation of microsatellite markers in Saltol QTL region in contrasting rice genotypes for salt tolerance at the early vegetative stage. Aust J Crop Sci 8:356–362

    CAS  Google Scholar 

  26. Cha-um S, Boriboonkaset T, Pichakum A, Kirdmanee C (2009) Multivariate physiological indices for salt tolerant classification in indica rice (Oryza sativa L. spp. indica). Gen Appl Plant Physiol 35:75–87

    CAS  Google Scholar 

  27. Cha-um S, Chuencharoen S, Mongkolsiriwatana C (2012) Screening sugarcane (Saccharum sp.) genotypes for salt tolerance using multivariate cluster analysis. Plant Cell Tissue Organ Cult 110:23–33

    CAS  Google Scholar 

  28. Chawla S, Jain S, Jain V (2013) Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). J Plant Biochem Biotechnol 22:27–34

    CAS  Google Scholar 

  29. Chen XQ, Yu BJ (2007) Ionic effects of Na+ and Cl on photosynthesis in Glycine max seedlings under iso osmotic salt stress. J Plant Physiol Mol Biol 33:294–300

    CAS  Google Scholar 

  30. Chong J, Soufan O, Li C, Caraus L, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46:486–494

    Google Scholar 

  31. Chowdhury AD, Haritha G, Sunitha T, Krishnamurthy SL, Divya B, Padmavathi G, Ram T, Sarla N (2016) Haplotyping of rice genotypes using simple sequence repeat markers associated with salt tolerance. Rice Sci 23:317–325

    Google Scholar 

  32. Chunthaburee S, Dongsansuk A, Sanitchon J, Pattanagul W, Theerakulpisut P (2016) Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi J Biol Sci 23:467–477

    CAS  PubMed  Google Scholar 

  33. Das P, Nutan KK, Singla-Pareek SL, Pareek A (2015) Understanding salinity responses and adopting ‘omics-based’ approaches to generate salinity tolerant cultivars of rice. Front Plant Sci 6:712

    PubMed  PubMed Central  Google Scholar 

  34. Datta JK, Nag S, Banerjee A, Mondal NK (2009) Impact of salt stress on five varieties of Wheat (Triticum aestivum L.) cultivars under laboratory condition. J Appl Sci Environ Manag 13:93–97

    Google Scholar 

  35. Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na + transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507

    CAS  PubMed  Google Scholar 

  36. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA mini preparation: version II. Plant Mol Biol Rep 1:19–21

    CAS  Google Scholar 

  38. Dogan M (2011) Antioxidative and proline potentials as a protective mechanism in soybean plants under salinity stress. Afr J Biotechnol 10:5972–5978

    CAS  Google Scholar 

  39. El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    CAS  PubMed  Google Scholar 

  40. Esfandiari E, Gohari G (2017) Response of ROS-scavenging systems to salinity stress in two different wheat (Triticum aestivum L.) cultivars. Not Bot Horti Agrobot 45:287–291

    CAS  Google Scholar 

  41. Fariduddin Q, Khalil RRAE, Mir BA, Yusuf M, Ahmad A (2013) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856

    CAS  PubMed  Google Scholar 

  42. Freed R, Einensmith SP, Gutez S, Reicosky D, Smail VW, Wolberg P (1989) Guide to MSTAT-C analysis of agronomic research experiments. Michigan State University, East Lansing

    Google Scholar 

  43. Ganie SA, Borgohain MJ, Kritika K, Talukdar A, Pani DR, Mondal TK (2016) Assessment of genetic diversity of Saltol QTL among the rice (Oryza sativa L.) genotypes. Physiol Mol Biol Plants 22:107–114

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8:55

    Google Scholar 

  45. Ghosh N, Adak MK, Ghosh PD, Gupta S, Sen Gupta DN, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5:89–103

    Google Scholar 

  46. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Gregorio GB, Senadhira D, Mendoza RD (1997) Screening rice for salinity tolerance. IRRI Discussion Paper Series no. 22. International Rice Research Institute, P.O. Box 933, Manila 1099, Philippines

  48. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596

    PubMed  PubMed Central  Google Scholar 

  49. Haq TU, Akhtar J, Nawaz S, Ahmad R (2009) Morpho-physiological response of rice (Oryza sativa L.) varieties to salinity stress. Pak J Bot 41:2943–2956

    Google Scholar 

  50. Haque SA (2006) Review article salinity problems and crop production in coastal regions of Bangladesh. Pak J Bot 38:1359–1365

    Google Scholar 

  51. Hassan MA, Chaura J, María P, Torres MPD, Boscaiu M, Vicente M (2017) Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima. AoB Plants 9:plx009

    PubMed  PubMed Central  Google Scholar 

  52. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signal Behav 7:1456–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Hoque MA, Okuma E, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561

    CAS  PubMed  Google Scholar 

  54. Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+ starved roots for growth. EMBO J 26:3003–3014

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Hossain M, Jaim WMH, Alam MS, Rahman ANMM (2013) Rice biodiversity in Bangladesh: adoption, diffusion and disappearance of varieties: a statistical report from farm Survey in 2005. BRAC Res Eval Forum, Dhaka

    Google Scholar 

  56. Hossain H, Rahman MA, Alam MS, Singh RK (2015) Mapping of quantitative trait loci associated with reproductive-stage salt tolerance in rice. J Agron Crop Sci 201:17–31

    CAS  Google Scholar 

  57. Ibrahim MAA, Rani MH, Begum SN, Akter MB, Islam MM (2016) Performance of rice landraces under salt stress at the reproductive stage using SSR markers. Int J Plant Soil Sci 13:1–11

    CAS  Google Scholar 

  58. International Rice Research Institute (IRRI) (1997) Rice Almanae. IRRI-WARDA-CIAT, Los Baños. Laguna, Philippines

  59. Islam MZ, Baset Mia MA (2007) Effect of different saline levels on growth and yield attributes of mutant rice. J Soil Nat 1:18–22

    Google Scholar 

  60. 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 166:1587–1597

    CAS  PubMed  Google Scholar 

  61. Islam MR, Salam MA, Hassan L, Collard BCY, Singh RK, Gregorio GB (2011) QTL mapping for salinity tolerance at seedling stage in rice. Emir J Food Agric 23:137–146

    Google Scholar 

  62. Islam F, Ali B, Wang J, Farooq MA, Gill RA, Ali S, Wang D, Zhou W (2016a) Combined herbicide and saline stress differentially modulates hormonal regulation and antioxidant defense system in Oryza sativa cultivars. Plant Physiol Biochem 107:82–95

    CAS  PubMed  Google Scholar 

  63. Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou W (2016b) Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul 80:23–36

    CAS  Google Scholar 

  64. Jamshidi A, Javanmard HR (2017) Evaluation of barley (Hordeum vulgare L.) genotypes for salinity tolerance under field conditions using the stress indices. Ain Shams Eng J. 9:2093–2099

    Google Scholar 

  65. Jenks MA, Hasegawa PM, Jain SM (2007) Advances in molecular breeding toward drought and salt tolerant crops. Springer, New York. https://doi.org/10.1007/978-1-4020-5578-2

    Google Scholar 

  66. Joseph B, Jini D, Sujatha S (2010) Biological and physiological perspectives of specificity in abiotic salt stress response from various rice plants. Asian J Agric Sci 2:99–105

    Google Scholar 

  67. Kabir MS, Salam MU, Chowdhury A, Rahman NMF, Iftekharuddaula KM, Rahman MS, Rashid MH, Dipti SS, Islam A, Latif MA, Islam AKMS, Hossain MM, Nessa B, Ansari TH, Ali MA, Biswas JK (2015) Rice vision for Bangladesh: 2050 and Beyond. Bangladesh Rice J 19:1–18

    Google Scholar 

  68. Kamruzzaman MD, Marjuk AL, Alam M (2017) Local rice varieties in climate vulnerable areas of Bangladesh: prospects and barriers. In: Proceedings of 7th international symposium, SEUSL, 7th and 8th December 2017

  69. Kanawapee N, Sanitchon J, Lontom A, Threerakulpisut P (2012) Evaluation of salt tolerance at the seedling stage in rice genotypes by growth performance, ion accumulation, proline and chlorophyll content. Plant Soil 358:235–249

    CAS  Google Scholar 

  70. Kavi Kishor PB, Hong Z, Miao G-H, Hu C-AA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108(4):1387–1394

    Google Scholar 

  71. Khafagy MA, Arafa AA, El-Banna MF (2009) Glycinebetaine and ascorbic acid can alleviate the harmful effects of NaCl salinity in sweet pepper. Aust J Crop Sci 5:257–267

    Google Scholar 

  72. Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30:81–89

    CAS  Google Scholar 

  73. Kibria MG, Hossain M, Murata Y, Hoque MA (2017) Antioxidant defense mechanisms of salinity tolerance in rice genotypes. Rice Sci 24:155–162

    Google Scholar 

  74. Koca H, Bor M, Özdemir F, Türkan I (2007) The effect of salinity stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351

    CAS  Google Scholar 

  75. Kordrostami M, Rabiei M, Kumleh HH (2017) Biochemical, physiological and molecular evaluation of rice cultivars differing in salt tolerance at the seedling stage. Physiol Mol Biol Plants 23:529–544

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537

    PubMed  PubMed Central  Google Scholar 

  77. Läuchli A, Grattan SR (2007) Plant growth and development under salinity Stress. Springer, Berlin, pp 1–32

    Google Scholar 

  78. Lo´pez-Aguilar R, Medina-Herna´ndez D, Ascencio-Valle F, Troyo-Dieguez E, Nieto-Garibay A, Arce-Montoya M, Larrinaga-Mayoral JA, Go´mez-Anduro GA (2012) Differential responses of chiltepin (Capsicum Annuum var. glabriusculum) and poblano (Capsicum Annuum var. annuum) hot peppers to salinity at the plantlet stage. Afr J Biotechnol 11:2642–2653

    Google Scholar 

  79. Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan M, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31(6):699–712

    CAS  PubMed  Google Scholar 

  80. Manzanilla DO, Paris TR, Vergara GV, Ismail AM, Pandey S (2011) Submergence risks and farmer’s preferences: implications for breeding sub1 rice in Southeast Asia. Agric Syst 104:335–347

    Google Scholar 

  81. Mekawy AMM, Assaha DV, Yahagi H, Tada Y, Ueda A, Saneoka H (2015) Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress. Plant Physiol Biochem 87:17–25

    CAS  PubMed  Google Scholar 

  82. Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    CAS  Google Scholar 

  83. Miller GAD, Suzuki N, Sultan CY, Mittler RON (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467

    CAS  Google Scholar 

  84. Motos JRA, Ortuño MF, Vicente AB, Vivancos PD, Blanco MJS, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18

    Google Scholar 

  85. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    CAS  PubMed  Google Scholar 

  86. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  87. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    CAS  PubMed  Google Scholar 

  88. Naumann JC, Young DR, Anderson JE (2008) Leaf chlorophyll fluorescence, reflectance, and physiological response to fresh-water and saltwater flooding in the evergreen shrub, Myrica cerifera. Environ Exp Bot 63:402–409

    CAS  Google Scholar 

  89. Nedjimi B (2014) Effects of salinity on growth, membrane permeability and root hydraulic conductivity in three saltbush species. Biochem Syst Ecol 52:4–13

    CAS  Google Scholar 

  90. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    CAS  PubMed  Google Scholar 

  91. Nejad M, Arzani A, Rezai AM, Singh RK, Gregorio GB (2008) Assessment of rice genotypes for salt tolerance using microsatellite markers associated with the saltol QTL G. Afr J Biotechnol 7:730–736

    Google Scholar 

  92. Nicholls RJ, Wong PP, Burkett VR, Codignotto JO, Hay JE, McLean RF, Ragoonaden S, Woodroffe CD (2007) Coastal systems and low-lying areas. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, Eds., Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 315–356

  93. Omisun T, Sahoo S, Saha B, Panda SK (2018) Relative salinity tolerance of rice cultivars native to North East India: a physiological, biochemical and molecular perspective. Protoplasma 255:193–202

    CAS  PubMed  Google Scholar 

  94. Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Poll Res 22:4056–4075

    CAS  Google Scholar 

  95. Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian J Exp Bot 46:736–742

    CAS  Google Scholar 

  96. Pons R, Cornejo MJ, Sanz A (2011) Differential salinity-induced variations in the activity of H+-pumps and Na+/H+ antiporters that are involved in cytoplasm ion homeostasis as a function of genotype and tolerance level in rice cell lines. Plant Physiol Biochem 49:1399–1409

    CAS  PubMed  Google Scholar 

  97. Reddy INBL, Kim BK, Yoon IS, Kim KH, Kwon TR (2017) Salt tolerance in rice: focus on mechanisms and approaches. Rice Sci 24:123–144

    Google Scholar 

  98. Roy PR, Tahjib-Ul-Arif M, Akter T (2016) Exogenous ascorbic acid and hydrogen peroxide alleviates salt-induced oxidative stress in rice (Oryza sativa L.) by enhancing antioxidant enzyme activities and proline content. Adv Environ Biol 10:148–215

    CAS  Google Scholar 

  99. Rubel MH, Hassan L, Islam MM, Robin AHK, Alam MJ (2014) Evaluation of rice genotypes under salt stress at the seedling and reproductive stages using phenotypic and molecular markers. Pak J Bot 46:423–432

    Google Scholar 

  100. Saha P, Chatterjee P, Biswas AK (2010) NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L. Wilczek). Indian J Exp Biol 48:593–600

    CAS  PubMed  Google Scholar 

  101. Santos VC (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic 130:93–99

    Google Scholar 

  102. Seetharam K, Thirumeni S, Paramasivam K (2009) Estimation of genetic diversity in rice (Oryza sativa L.) genotypes using SSR markers and morphological characters. Afr J Biotechnol 8:2050–2059

    CAS  Google Scholar 

  103. Senguttuvel P, Raju NS, Padmavathi G, Sundaram RM, Madhav S, Hariprasad AS, Kota S, Bhadana VP, Subrahmanyam D, Rao LVS, Brajendra R (2016) Identification and quantification of salinity tolerance through salt stress indices and variability studies in rice (Oryza sativa L.). SABRAO J Breed Genet 48:172–179

    Google Scholar 

  104. Shereen A, Mumtaz S, Raza S, Khan MA, Solangi S (2005) Salinity effects on seedling growth and yield components of different inbred rice lines. Pak J Bot 37:131–139

    Google Scholar 

  105. Siddiqui MN, Mostofa MG, Akter MM, Srivastava AK, Sayed MA, Hasan MS, Tran LSP (2017) Impact of salt-induced toxicity on growth and yield-potential of local wheat cultivars: oxidative stress and ion toxicity are among the major determinants of salt-tolerant capacity. Chemosphere 187:385–394

    CAS  PubMed  Google Scholar 

  106. Silva EN, Vieira SA, Ribeiro RV, Ponte LF, Ferreira-Silva SL, Silveira JA (2013) Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat. J Plant Growth Regul 32:159–169

    CAS  Google Scholar 

  107. Singh RK, Gregorio GB, Jain RK (2007) QTL mapping for salinity tolerance in rice. Physiol Mol Biol Plants 13:87–99

    CAS  Google Scholar 

  108. Singh VK, Singh BD, Kumar A, Maurya S, Krishnan SG, Vinod KK, Singh MP, Ellur RK, Bhowmick PK, Singh PK (2018) Marker-assisted introgression of Saltol QTL enhances seedling stage salt tolerance in the rice variety “Pusa Basmati”. Int J Genomics 2018:8319879

    PubMed  PubMed Central  Google Scholar 

  109. Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco, p 573

    Google Scholar 

  110. Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619

    CAS  Google Scholar 

  112. Summart J, Thanonkeo P, Panichajakul S, Prathepha P, Mcmanus M (2010) Effect of salt stress on growth, inorganic ion and proline accumulation in thai aromatic rice, Khao Dawk Mali 105, callus culture. Afr J Biotechnol 9:145–152

    CAS  Google Scholar 

  113. Sun J, Zou DT, Luan FS, Zhao HW, Wang JG, Liu HL, Liu ZL (2014) Dynamic QTL analysis of the Na+ content, K+ content, and Na+/K+ ratio in rice roots during the field growth under salt stress. Biol Plant 58:689–696

    CAS  Google Scholar 

  114. Surridge C (2004) Rice cultivation: feast or famine? Nature 428:360–361

    CAS  PubMed  Google Scholar 

  115. Tahjib-Ul-Arif M, Afrin S, Islam MM, Hossain MA (2017) Phenotypic parameters clustering based screening of rice (Oryza sativa L.) landraces for salt tolerance. Asian J Plant Sci 16:235–241

    CAS  Google Scholar 

  116. Tahjib-Ul-Arif M, Roy PR, Al Mamun Sohag A (2018a) Exogenous calcium supplementation improves salinity tolerance in brri dhan28; a salt-susceptible high-yielding Oryza sativa cultivar. J Crop Sci Biotechnol 21:383–394

    Google Scholar 

  117. Tahjib-Ul-Arif M, Sayed MM, Islam MM, Siddiqui MN, Begum SN, Hossain MA (2018b) Screening of rice landraces (Oryza sativa L.) for seedling stage salinity tolerance using morpho-physiological and molecular markers. Acta Physiol Plant 40:70

    Google Scholar 

  118. Tahjib-Ul-Arif M, Siddiqui MN, Sohag AAM (2018c) Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. J Plant Growth Regul 37:1318–1330

    CAS  Google Scholar 

  119. Taïbia K, Taïbia F, Abderrahima LA, Ennajahb A, Belkhodjac M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation andantioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312

    Google Scholar 

  120. Talat A, Nawaz K, Hussian K, Bhatti KH, Siddiqi EH, Khalid A, Anwer S, Sharif MU (2013) Foliar application of proline for salt tolerance of two wheat (Triticum aestivum L.) cultivars. World Appl Sci J 22:547–554

    CAS  Google Scholar 

  121. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Tatar O, Brueck H, Gevrek MN, Asch F (2010) Physiological responses of two Turkish rice (Oryza sativa L.) varieties to salinity. Turk J Agric For 34:451–459

    Google Scholar 

  123. Temizgul R, Kaplan M, Kara R, Yilmaz S (2016) Effects of salt concentrations on antioxidant enzyme activity of grain sorghum. Curr Trends Nat Sci 5:171–178

    Google Scholar 

  124. Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62:1–9

    CAS  Google Scholar 

  125. Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.) differential response in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418

    CAS  Google Scholar 

  126. Veylder D, Beeckman L, Inzé D (2007) The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 8:655–665

    PubMed  Google Scholar 

  127. Wi SG, Chung BY, Kim JH, Lee KS, Kim JS (2006) Deposition pattern of hydrogen peroxide in the leaf sheaths of rice under salt stress. Biol Plant 50:469–472

    CAS  Google Scholar 

  128. Willekens H, Inze D, Van Montagu M, Van Camp W (1995) Catalases in plants. Mol Bred 1:207–228

    CAS  Google Scholar 

  129. Zhai R, Feng Y, Wang H, Zhan X, Shen X, Wu W, Zhang Y, Chen D, Dai G, Yang Z, Cao L, Cheng S (2013) Transcriptome analysis of rice root heterosis by RNA-Seq. BMC Genomics 14:19

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot 85:1–9

    Google Scholar 

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Acknowledgements

The authors are grateful to the Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh, Bangladesh for providing rice seeds throughout the experimental work and also grateful to the Mirza Mofazzal Islam, Chief scientific officer, Plant breeding division, BINA, for help with laboratory work.

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LH conceived the project and planned the study. MR performed the experiments, analyzed the data, and wrote the first draft of the paper. MT-U-A guided the biochemical analysis and performed the critical revision of the data and wrote the final version of the paper. MAH contributed to the writing of the manuscript. MAS did the proof-reading of the final draft and edited.

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Correspondence to Md. Abu Sayed.

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Rasel, M., Tahjib-Ul-Arif, M., Hossain, M.A. et al. Discerning of Rice Landraces (Oryza sativa L.) for Morpho-physiological, Antioxidant Enzyme Activity, and Molecular Markers’ Responses to Induced Salt Stress at the Seedling Stage. J Plant Growth Regul 39, 41–59 (2020). https://doi.org/10.1007/s00344-019-09962-5

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Keywords

  • Antioxidant enzymes
  • Landraces
  • Rice
  • Salt stress
  • Seedling stage
  • SSR markers