The genus Portulaca as a suitable model to study the mechanisms of plant tolerance to drought and salinity

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Abstract

Drought and soil salinity are at present the major factors responsible for the global reduction of crop yields, and the problem will become more severe in the coming decades because of climate change effects. The most promising strategy to achieve the increased agricultural production that will be required to meet food demands worldwide will be based on the enhancement of crop stress tolerance, by both, traditional breeding and genetic engineering. This, in turn, requires a deep understanding of the mechanisms of tolerance which, although based on a conserved set of basic responses, vary widely among plant species. Therefore, the use of different plant models to investigate these mechanisms appears to be a sensible approach. The genus Portulaca could be a suitable model to carry out these studies, as some of its taxa have been described as tolerant to drought and/or salinity. Information on relevant mechanisms of tolerance to salt and water stress can be obtained by correlating the activation of specific defence pathways with the relative stress resistance of the investigated species. Also, species of the genus could be economically attractive as ‘new’ crops for ‘saline’ and ‘arid’, sustainable agriculture, as medicinal plants, highly nutritious vegetable crops and ornamentals.

1. IPCC (WGI). Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change, JT Houghton and Ding Yihu, eds. Cambridge: Cambridge University Press, 2001.

2. IPCC (WGII). Climate Change 2001: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate Change. JJ McCarthy, OF Canziani, NA Leary, DJ Dokken, and KS White, eds. Cambridge: Cambridge University Press, 2001b.

3. Warrick RA. The possible impacts on wheat product on of a recurrence of the 1930s drought in the U.S. Great Plans. Climatic Change 1984; 6: 5-26.

4. Boyer JS: Plant productivity and environment. Science 1982; 218(4571): 443-448.

5. Bray EA, Bailey-Serres J, Weretilnyk E. Responses to abiotic stress. In: Buchanan B, Gruissem W, Jones R eds. Biochemistry and molecular biology of plants. American Society of Plant Physiology 2000; Rockville, pp 1158-1203.

6. FAO. FAO land and plant nutrition management service 2008. Available at http://www.fao.org/ag/agl/agll/spush

7. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003; 218(1): 1-14.

8. Flowers TJ, Hajibagheri MA, Clipson NJW. Halophytes. Quat Rev Biol 1986; 61: 313-337. doi: 10.1086/415032

9. Zhu JK. Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 2000; 124: 941-948.

10. Reddy IN, Kim BK, Yoon IS, Kim KH, Kwon TR. Salt tolerance in rice: Focus on mechanisms and approaches. Rice Sci 2017; 24(3): 123-144.

11. Zhang J, Zhang Y, Du Y, Chen S, Tang H. Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 2011; 10(4): 1904-1914.

12. Cruz V, Cuartero J. Effects of salinity at several developmental stages of six genotypes of tomato (Lycopersicon spp.). In: Proceedings of the XIth Eucarpia meeting on tomato genetics and breeding 1990: 81-86.

13. Xiong L, Zhu JK. Salt-stress signal transduction. In: Scheel D, Wasternack C, eds. Plant Signal Transduction, Frontiers in Molecular Biology Series 2002. Oxford UK: Oxford University Press, pp 165-197.

14. Zhu JK. Plant salt tolerance. Trends Plant Sci 2001; 6: 66-71.

15. Barnes RF, Baylor JE. Forages in a changing world. In: Forages, Vol 1: An introduction to Grassland Agriculture, Barnes RF, Miller DA, Nelson CJ, eds. 5th ed. Iowa State University Press, Iowa 1995.

16. Rozema J, Flowers T. Crops for a salinized world. Science 2008; 322: 1478-1480.

17. Lokhande VH, Suprasanna P. Prospects of halophytes in understanding and managing abiotic stress tolerance in environmental adaptations and stress tolerance of plants in the era of climate change, Ahmad P, Prasad MNV, eds., pp. 29-56, Springer, New York, NY, USA, 2012.

18. Ma J, Zhang M, Xiao X, You J, Wang J, Wang T, ... Tian C. Global transcriptome profiling of Salicornia europaea L. shoots under NaCl treatment. PloS ONE 20013; 8(6): e65877.

19. Ramani B, Reeck T, Debez A, Stelzer R, Huchzermeyer B, Schmidt A, Papenbrock J. Aster tripolium L. and Sesuvium portulacastrum L.: two halophytes, two strategies to survive in saline habitats. Plant Physiol Biochem 2006; 44(5): 395-408.

20. Zurayk RA, Baalbaki R. Inula crithmoides: a candidate plant for saline agriculture. Arid Land Res Manag 1996; 10(3): 213-223.

21. Al Hassan M, Chaura J, López-Gresa MP, Borsai O, Daniso E, Donat-Torres MP, ... Boscaiu M. Native-invasive plants vs. halophytes in Mediterranean salt marshes: Stress tolerance mechanisms in two related species. Front Plant Sci 2016; 7: 473.

22. Fita A, Rodríguez-Burruezo A, Boscaiu M, Prohens J and Vicente O. Breeding and domesticating crops adapted to drought and salinity: A new paradigm for increasing food production. Front Plant Sci 2015; 6: 978.

23. Glenn EP, Anday T, Chaturvedi R, Martinez-Garcia R, Pearlstein S, Soliz D, ... Felger RS. Three halophytes for saline-water agriculture: An oilseed, a forage and a grain crop. Environ Exp Bot 2013; 92: 110-121.

24. Glenn EP, O’leary JW, Watson MC, Thompson TL, Kuehl RO. Salicornia bigelovii Torr: An oilseed halophyte for seawater irrigation. Science 1991; 251: 1065-1067. doi:10.1126/science.251.4997.1065

25. Weber DJ, Ansarib R, Gul B, Khan MA. Potential of halophytes as source of edible oil. J Arid Environ 2007; 68: 315-321. doi: 10.1016/j.jaridenv.2006.05.010

26. Ma C, Zhou D, Wang H, Han D, Wang Y, Yan X. Elicitation of Jerusalem artichoke (Helianthus tuberosus L.) cell suspension culture for enhancement of inulin production and altered degree of polymerisation. J Sci Food Agric 2017; 97(1): 88-94.

27. Khan MA, Qaiser M. Halophytes of Pakistan: characteristics, distribution and potential economic usages. Sabkha ecosystems 2006: 129-53.

28. Jin R, Wang Y, Liu R, Gou J, Chan Z. Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front Plant Sci 2016; 6: 1123.

29. von Poellnitz K. Versuch eine Monographie der Gattung Portulaca L. Fedde Rep 1934; 37: 240-320.

30. Legrand D. Las especies americanas de Portulaca. Mus Hist Nat 1962; 2a Ser. 7, 1-147.

31. Geesink R. An account of the genus Portulaca in Indo-Australia and the Pacific. Blumea 1969; 17: 275-301.

32. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7: 214. doi:10.1186/1471-2148-7-214.

33. Ocampo G, Columbus JT. Molecular phylogenetics, historical biogeography, and chromosome number evolution of Portulaca (Portulacaceae). Mol Phylogenetics Evol 2016; 63(1): 97-112.

34. Teixeira M, Carvalho IS. Effects of salt stress on purslane (Portulaca oleracea) nutrition. Ann App Bio 2009; 154(1): 77-86.

35. Alam MA, Juraimi AS, Rafii MY, Abdul Hamid A, Aslani F. Screening of purslane (Portulaca oleracea L.) accessions for high salt tolerance. Sci World J 2014; 9.

36. Grieve CM, Suarez DL. Purslane (Portulaca oleracea L.): a halophytic crop for drainage water reuse systems. Plant and Soil 1997; 192(2): 277-283.

37. Ren S, Weeda S, Akande O, Guo Y, Rutto L, Mebrahtu T. Drought tolerance and AFLP-based genetic diversity in purslane (Portulaca oleracea L.). J Biotech Res 2011; 3: 51-61.

38. Liu L, Howe P, Zhou YF, Hocart C, Zhang R. Fatty acid profiles of leaves of nine edible wild plants: an Australian study. J Food Lipids 2002; 9: 65-71.

39. Zheng ZH, Dong ZH, Yu J. Modern study of traditional Chinese medicine, Xue Yuan Press, Beijing University of Traditional Chinese Medicine, Beijing, 1997.

40. Simpoulos AP. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 1991; 54: 438-463.

41. Alam MA, Juraimi AS, Rafii MY, Hamid AA, Aslani F, Alam MZ. Effects of salinity and salinity-induced augmented bioactive compounds in purslane (Portulaca oleracea L.) for possible economical use. Food Chem 2015; 169: 439-447.

42. Mulry KR, Hanson BA, Dudle DA. Alternative strategies in response to saline stress in two varieties of Portulaca oleracea (purslane). PloS ONE 2015; 10(9): e0138723.

43. Crane TA, Roncoli C, Hoogenboom G. Adaptation to climate change and climate variability: the importance of understanding agriculture as performance. NJAS –Wag. J Life Sci 2011; 57: 179-185. doi: 10.1016/j.njas.2010.11.002

44. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010; 48(12): 909-930.

45. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003; 218(1): 1-14.

46. Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S … Kopka J. Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 2015; 91: 1118-1133. doi: 10.1111/brv.12215

47. Vicente O, Boscaiu M, Naranjo MA, Estrelles E, Bellés JM, Soriano P. Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). J Arid Environ 2004; 58: 463-481.

48. Rahdari P, Tavakoli S, Hosseini SM. Studying of salinity stress effect on germination, proline, sugar, protein, lipid and chlorophyll content in purslane (Portulaca oleracea L.) leaves. J Stress Physiol Biochem 2012; 8(1): 182-193.

49. Borsai O, Al Hassan M, Boscaiu M, Vicente O, Sestras A, Sestras R. Effects of salt on seed germination and seedling growth of three Portulaca species. Bulletin USAMV Cluj-Napoca. Horticulture 2015; 72(2): 450-451.

50. Franco JA, Cros V, Vicente MJ, Martínez-Sánchez JJ. Effects of salinity on the germination, growth, and nitrate contents of purslane (Portulaca oleracea L.) cultivated under different climatic conditions. J Hortic Sci Biotechnol 2011; 86(1): 1-6.

51. Rahimi Z, Kafi M. Effects of drought stress on germination characteristics of purslane (Portulaca oleracea L.). Environ Stress Crop Sci 2009; 2(1): 87-91.

52. Pill WG, Frett JJ, Morneau DC. Germination and seedling emergence of primed tomato and asparagus seeds under adverse conditions. Hort Sci 1991; 26(9): 1160-1162.

53. Miceli A, Moncada A, D’Anna F. Effect of water salinity on seeds germination of Ocimum basilicum L., Eruca sativa L. and Petroselinum hortense Hoffm. Acta Hort 2003; 609: 365-370.

54. Zapryanova N, Atanassova B. Effects of salt stress on growth and flowering of ornamental annual species. Biotechnol Biotechnol Equip 2009; 23(sup1): 177-179.

55. Cicevan R, Al Hassan M, Sestras AF, Prohens J, Vicente O, Sestras RE, Boscaiu M. Screening for drought tolerance in cultivars of the ornamental genus Tagetes (Asteraceae). Peer J 2016; 4: e2133.

56. Jaleel PM, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Vam RP. Drought stress in plants: a review on morphological characteristics and pigments composition Int J Agric Biol 2009; 11: 100-105.

57. Kaya MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı Ö. Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur J Agron 2006; 24(4): 291-295.

58. Giménez Luque E, Delgado Fernández IC, Gómez Mercado F. Effect of salinity and temperature on seed germination in Limonium cossonianum. Botany 2012; 91(1): 12-16.

59. Al Hassan M, Estrelles E, Soriano P, López-Gresa MP, Bellés JM, Boscaiu M, Vicente O. Unraveling salt tolerance mechanisms in halophytes: a comparative study on four Mediterranean Limonium species with different geographic distribution patterns. Front Plant Sci 2017; 8:1438. doi: 10.3389/fpls.2017.01438

60. Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012. doi: 10.1155/2012/217037

61. Serrano R, Mulet JM, Rios G, Marquez JA, Larrinoa IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft M, Ros R, Montesinos C. A glimpse of the mechanisms of ion homeostasis during salt stress. J Exper Bot 1999; 50: 1023-1036.

62. Yan K, Shao H, Shao C, Chen P, Zhao S, Brestic M, Chen X. Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 2013; 35(10): 2867-2878.

63. Nakabayashi R, Mori T, Saito K. Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal Behav 2014; pii: e29518.

64. Alam MA, Juraimi, AS, Rafii MY, Hamid AA, Aslani F, Hakim MA. Salinity induced changes in the morphology and major mineral nutrient composition of purslane (Portulaca oleracea L.) accessions. Biol Res 2016; 49: 24. doi: 10.1186/s40659-016-0084-5

65. van Zandt PA, Mopper S. Delayed and carry over effects of salinity on flowering in Iris hexagona (Iridaceae). Am J Bot 2002; 89(11): 1847-1851.

66. Boyd RS, Barbour MG. Relative salt tolerance of Cakile edentula (Brassicaceae) from lacustrine and marine beaches. Am J Bot 1986; 73(2): 236-241.

67. Blits KC, Gallagher JL. Morphological and physiological responses to increased salinity in marsh and dune ecotypes of Sporobolus virginicus (L.). Kunth Oecologia 1991; 87(3): 330-335.

68. Ludlow MM, Ng TT. Water stress suspends leaf ageing. Plant Sci Lett 1974; 3: 235-240.

69. Amirul Alam M, Shukor A, Rafii JMY, Hamid AA, Uddin MK, Alam MZ, Latif MA. Genetic improvement of purslane (Portulaca oleracea L.) and its future prospects Mol Biol Rep 2014; 41: 7395-7411. doi 10.1007/s11033-014-3628-1

70. Schulze ED. Whole-plant responses to drought. Aust J Plant Physiol 1986; 13: 127-141.

71. Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 2009; 103(4): 551-560.

72. Qados AMA. Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). Journal of the Saudi Society of Agricultural Sciences 2011; 10(1): 7-15.

73. Misra AN, Latowski D and Strzalka K. The xanthophyll cycle activity in kidney bean and cabbage leaves under salinity stress. Russ J Plant Physiol 2006; 53(1): 102-109.

74. Murillo-Amador B, Yamada S, Yamaguchi T, Rueda-Puente E, Ávila-Serrano N, García-Hernández JL, Nieto-Garibay A. Influence of calcium silicate on growth, physiological parameters and mineral nutrition in two legume species under salt stress. J Agron Crop Sci 2007; 193(6): 413-421.

75. Gummuluru S, Jana S, Hobbs S. Genotypic variability in physiological characters and its relationship to drought tolerance in durum wheat. Can. J. Plant Sci 1989; 69(3): 703-711.

76. Ayala-Astorga GI, Alcaraz-Meléndez L. Salinity effects on protein content, lipid peroxidation, pigments, and proline in Paulownia imperialis (Siebold & Zuccarini) and Paulownia fortunei (Seemann & Hemsley) grown in vitro. Electron J Biotechnol 2010; 13(5): 13-14.

77. Beinsan C, Camen D, Sumalan R, Babau M. Study concerning salt stress effect on leaf area dynamics and chlorophyll content in four bean local landraces from Banat area. Fac Hortic 2003; 119: 416-419.

78. Siddiqi EH, Ashraf M, Hussain M, Jamil A. Assessment of intercultivar variation for salt tolerance in safflower (Carthamus tinctorius L.) using gas exchange characteristics as selection criteria. Pak J Bot 2009; 41(5): 2251-2259.

79. Kafi M, Rahimi Z. Effect of salinity and silicon on root characteristics, growth, water status, proline content and ion accumulation of purslane (Portulaca oleracea L.). J Soil Sci Plant Nutr 2011; 57(2): 341-347.

80. Rodriguez P, Dell’Amico J, Morales D, Blanco MS, Alarcón JJ. Effects of salinity on growth, shoot water relations and root hydraulic conductivity in tomato plants. J Agric Sci 1997; 128(4): 439-444.

81. Gama PBS, Inanaga S, Tanaka K, Nakazawa R. Physiological response of common bean (Phaseolus vulgaris L.) seedlings to salinity stress. Afr J Biotechnol 2007; 6(2): 79-88.

82. Gama PBS, Tanaka K, Eneji AE, Eltayeb AE, Siddig KE. Salt-induced stress effects on biomass, photosynthetic rate, and reactive oxygen species-scavenging enzyme accumulation in common bean. J Plant Nut 2009; 32(5): 837-854.

83. Munns R. Physiological processes limiting plant growth in saline salt: some dogmas and hypotheses. Plant Cell Environ 1993; 16: 15-24.

84. Li Z, Wakao S, Fischer BB, Niyogi KK. Sensing and responding to excess light. Annu Rev Plant Biol 2009; 60: 239-260. doi: 10.1016/j.cub.2005.06.041.

85. Greenway H, Munns R. Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 1980; 31(1): 149-190.

86. Collander R. Selective absorption of cations by higher plants. Plant Physiol 1941; 16(4): 691-720.

87. Karakaş S, Cullu MA, Dikilitaş M. Comparison of two halophyte species (Salsola soda and Portulaca oleracea) for salt removal potential under different soil salinity conditions. Turk J Agric For, 2017; 41(3): 183-190.

88. Niu X, Bressan RA, Hasegawa PM, Pardo JM. Ion homeostasis in NaCl stress environments. Plant Physiol 1995; 109: 735-742.

89. Maathuis FJM, Amtmann A. K+ nutrition and Na+ toxicity: The basis of cellular K+/Na+ ratios. Ann Bot. 1999; 84: 123-133.

90. Gorham J, Hughes LL, Wyn Jones RG. Low-molecular-weight carbohydrates in some salt-stressed plants. Physiol Plant 1981; 53(1): 27-33.

91. Abel GH, MacKenzie AJ. Salt tolerance of soybean varieties (Glycine max L. Merrill) during germination and later growth. Crop Sci 1964; 4(2): 157-161.

92. Rains DW. Plant tissue and protoplast culture: applications to stress physiology and biochemistry. In: Jones HG, Flowers TJ, Jones MB, eds. Plants Under Stress: Biochemistry, Physiology and Ecology and Their Application to Plant Improvement 1989; Seminar Series 39: 181-196.

93. Ali G, Srivastava PS, Iqbal M. Proline accumulation, protein pattern and photosynthesis in regenerants grown under NaCl stress. Biol Plant 1999; 42: 89-95.

94. Rhodes D, Verslues PE, Sharp RE. Role of amino acids in abiotic stress resistance. In: Singh BK, ed., Plant Amino Acids: Biochemistry and Biotechnology. Marcel Dekker, NY 1999; 319-356.

95. Ozturk L, Demir Y. In vivo and in vitro protective role of proline. Plant Growth Regul 2002; 38: 259-264.

96. Hsu SY, Hsu YT, Kao CH. The effect of polyethylene glycol on proline accumulation in rice leaves. Biol Plant 2003; 46: 73-78.

97. Kavi Kishore PB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 2005; 88: 424-438.

98. Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS. Over-expression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 1995; 108: 1387-1394.

99. Satoh R, Nakashima K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2002. ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis. Plant Physiol 2002; 130: 709-719.

100. Oono Y, Ooura C, Rahman A, Aspuria ET, Hayashi K, Tanaka A, Uchimiya H. P-clorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiol 2003; 133: 1135-1147.

101. Chinnusamy V, Jagendorf A, Zhu JK. Understanding and improving salt tolerance in plants. Crop Sci 2005; 45: 437-448.

102. Yazici I, Türkan I, Sekmen AH, Demiral T. Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 2007; 61(1): 49-57.

103. Lutts S, Majerus V, Kinet JM. NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 1999; 105: 450-458.

104. Lacerda CFD, Cambraia J, Oliva MA, Ruiz HA. Osmotic adjustment in roots and leaves of two sorghum genotypes under NaCl stress. Braz J Plant Physiol 2003; 15(2): 113-118.

105. Al Hassan M, Morosan M, López-Gresa MP, Prohens J, Vicente O, Boscaiu M. Salinity-induced variation in biochemical markers provides insight into the mechanisms of salt tolerance in common (Phaseolus vulgaris) and runner (P. coccineus) beans. Int J Mol Sci 2016; 17: 1582. doi:10.3390/ijms17091582

106. Venkatesan A, Chellappan KP. Accumulation of proline and glycine betaine in Ipomoea pes-caprae induced by NaCl. Biol Plant 1998; 41: 271-276. doi:10.1023/A:1001839302627

107. Mansour MMF. Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 2000; 43: 491-500. doi: 10.1023/A:1002873531707

108. Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK. Transgenics of an elite indica rice variety pusa basmati 1 harbouring the coda gene are highly tolerant to salt stress. Theor Appl Genet 2002; 106: 51-57. doi:10.1007/s00122-002-1063-5

109. Rhodes D, Hanson AD. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 1993; 44: 357-384.

110. Papageorgiou GC, Murata N. The unusually strong stabilizing effects of glycinebetaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 1995; 44: 243-252.

111. Shaw B, Thomas TH, Cooke DT. Responses of sugar beet (Beta vulgaris L.) to drought and nutrient deficiency stress. Plant Growth Reg 2002; 37(1): 77-83.

112. Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A. Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 2003; 158(3): 455-463.

113. Ishitani M, Nakamura T, Han SY, Takabe T. Expression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Mol Biol 1995; 27: 307-315.

114. Weimberg R, Lerner HR, Poljakoffmayber A. Changes in growth and water soluble solute concentrations in Sorghum bicolor stressed with sodium and potassium salts. Physiol Plant 1984; 62: 472-480. doi:10.1111/j.1399-3054.1984.tb04605.x

115. Nishimura N, Zhang J, Abo M, Okubo A, Yamazaki S. Application of capillary electrophoresis to the simultaneous determination of betaines in plants. Anal Sci 2001; 17(1): 103-106.

116. Gil R, Boscaiu M, Lull C, Bautista I, Lidón A, Vicente O. Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct. Plant Biol 2013; 40: 805-818.

117. Cram WJ. Negative feedback regulation of transport in cells. The maintenance of turgor, volume and nutrient supply. In: Luttge U, Pitman MG, eds. Encyclopaedia of Plant Physiology, New Series, Springer-Verlag, Berlin 1976; 2: 284-316.

118. Popp N, Smirnoff N. Polyol accumulation and metabolism during water deficit. In: Smirnoff N, ed., Environment and Plant Metabolism: Flexibility and Acclimation, Bios Scientific, Oxford 1995; 199-215.

119. Murakeozy EP, Nagy Z, Duhaze C, Bouchereau A, Tuba Z. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol 2003; 160: 395-401.

120. Ashraf M, Tufail M. Variation in salinity tolerance in sunflower (Helianthus annuus L.), J Agron Soil Sci 1995; 174: 351-362.

121. Ashraf M, Fatima H. Responses of some salt tolerant and salt sensitive lines of safflower (Carthamus tinctorius L.). Acta Physiol Plant 1995; 17: 61-71.

122. Alscher, RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 2002; 53(372): 1331-1341.

123. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci 2006; 11: 15-19.

124. Xu S, Li J, Zhang X, Wei H, Cui L. Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 2006; 56: 274-285.

125. Koca M, Bor M, Ozdemir F, Turkan I. The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 2007; 60: 344-351.

126. Agarwal S, Shaheen R. Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Braz J Plant Physiol 2007; 19(2): 149-161.

127. Al Hassan M, Chaura J, Donat-Torres MP, Boscaiu M, Vicente O. Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima. AoB Plants 2017; 9(2). doi:10.1093/aobpla/plx009.

128. Gould KS, Lister C. Flavonoid function in plants. In: Andersen ØM, Marham KR, eds. Flavonoids, Chemistry, Biochemistry and Application, CRC Press, Boca Raton, FL, 2006; 397-442.

129. Akula R, Ravishankar GA. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 2011; 6(11): 1720-1731.

130. Waśkiewicz A, Muzolf-Panek M, Goliński P. Phenolic content changes in plants under salt stress. In: Ahmad P, Azooz MM, Prasad MNV, eds. Ecophysiology and responses of plants under salt stress. Springer 2013.

131. Harborne JB, Williams CA. Advances in flavonoid research since 1992. Phytochemistry 2000; 55(6): 481-504.

132. Winkel-Shirley B. Biosynthesis of flavonoids and effect of stress. Curr Opin Plant Biol 2002; 5: 218-223. doi: 10.1016/S1369-5266(02)00256-X

133. Agati G, Tattini M. Multiple functional roles of flavonoids in photoprotecion. New Phytol 2010; 186: 786-793.

134. Rausher MD. The evolution of flavonoids and their genes. In: The science of flavonoids. Springer New York 2006; 175-211.

135. Swain T, The evolution of flavonoids. In: Plant Flavonoids in Biology and Medicine, Buffalo, New York (USA) 1986.

136. Stafford HA. Flavonoid evolution: an enzymic approach. Plant Physiol 1991; 96(3): 680-685.

137. Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G. Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol 2004; 163: 547-561.

138. Lillo C, Lea US, Ruoff P. Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 2008; 31: 587-601.

139. Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M. The biosynthesis of flavonoids is enhanced by UV radiation and root zone salinity in L vulgare leaves, J Plant Physiol 2011; 168: 204-212

140. Rivero RM, Ruiz JM, Garcia PC, Lopez-Lefebre LR, Sánchez E, Romero L. Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 2001; 160(2): 315-321.

141. Larkindale J, Huang B. Thermo-tolerance and antioxidant systems in Agrostis stoloifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 2004; 161: 405-413.

142. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002; 7: 405-410.

143. Naya L, Ladrera R, Ramos J, Gonzalez EM, Arrese-Igor C, Minchin FR, Becana M. The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 2017; 144: 1104–1114. doi 10.1104/pp.107.099648

144. Jin R, Wang Y, Liu R, Gou J, Chan Z. Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front Plant Sci 2015; 6: 1123. doi: 10.3389/fpls.2015.01123

145. Bologa M, Jităreanu CD, Slabu C, Marta AE. Salinity Stress Effects on the Growing Rates of Tomato (Lycopersicon esculentum Mill.). Bulletin USAMV series Agriculture 2015; 72(1): 277-278.

146. Gharsallah C, Fakhfakh H, Grubb D, Gorsane F. Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants. 2016; 8. doi: 10.1093/aobpla/plw055.

147. Amini F, Ehsanpour AA. Soluble proteins, proline, carbohydrates and Na+/K+ changes in two tomato (Lycopersicon esculentum Mill.) cultivars under in vitro salt stress. Am J Biochem Biotechnol 2005; 1(4): 204-208.

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