ALLEVIATORY ACTIVITIES IN MYCORRHIZAL TOBACCO PLANTS SUBJECTED TO INCREASING CHLORIDE IN IRRIGATION WATER

Document Type : Research Paper

Author

Abstract

Background and objectives: Excessive quantities of chloride in the cured leaf reduce the rate of burn and cause certain adverse effects such as increased hygroscopicity, dinginess, uneven colors and undesirable odors in cured tobacco leaves. Arbuscular mycorrhizal fungi (AMF) are associated with the roots of over 80% terrestrial plant species including halophytes, hydrophytes and xerophytes. AMF have been shown to promote plant growth and salinity tolerance; they promote salinity tolerance by employing various mechanisms. To date, no information is available about the interaction between of AM fungi and high chloride concentration in irrigation water on the agronomical and physiological responses of tobacco.
Material and Methos: Field experiments were conducted in the field research of Payame Noor University, Gorgan, Golestan province, Iran during two years (2012-2013). A factorial randomized block design with four replications on agronomic and chemical properties of Virginia tobacco (cv. K-326, included two mycorrhizal (Rhizophagus irregularis) levels (with AM, AM+ or without AM, AM-) and four chloride levels in irrigation water (C1-C4); Chloride was added to the water as CaCl2. The fact that the10 mg Cl L-1 concentration in water is considered very low and without adverse effects on tobacco, leads us to the decision to take this chloride concentration as control.
Results: Mycorrhizal plants had significantly higher uptake of nutrients in shoots and number of leaves regardless of intensities of chloride stress. The cured leaves yield of AM+ plants under C2-C4 chloride stressed conditions was higher than AM- plants. Leaf chloride content increased in linearly with the increase of chloride level while AMF colonized plants maintained low Cl content. AM+ plants produced tobacco leaves that contain significantly higher quantities of nicotine than AM- plants. AM inoculation ameliorated the chloride stress to some extent. Antioxidant enzymes like superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR) as well as non-enzymatic antioxidants (ascorbic acid and glutathione) also exhibited decrease with chloride treatment. Chloride stress caused great alterations in the endogenous levels of growth hormones with abscisic acid showing increment. AMF inoculated plants maintained higher levels of growth hormones and also allayed the negative impact of chloride.
Conclusion: Based on the previuos results it is preferable to use irrigation water with chloride concentration below 25 mg L-1 since at this level the chloride concentration in the leaves remained around 1%. On the other hand, the chloride level of 40 mg L-1 in irrigation water in combination with AMF can be considered as the threshold upper limit. In such high concentrations the use of AMF are recommended, because keep the leaf chloride concentrations around the acceptable level.

Keywords

Main Subjects


1. Abdel Latef, A.A.H., and Chaoxing, H. 2011. Arbuscular mycorrhizal influence on growth,
photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected
to low temperature stress. Acta Physiol. Plant. 33: 1217–1225.
2. Abd_Allah, E.F., Hashem, A., Alqarawi, A.A., Bahkali, A.H., and Alwhibi, M.S. 2015.
Enhancing growth performance and systemic acquired resistance of medicinal plant
Sesbania sesban (L.) Merr using arbuscular mycorrhizal fungi under salt stress. Saudi J.
Biological Sci., 22: 274–283.
3. Abeer, H., Abd_Allah, E.F., Alqarawi, A.A., and Egamberdieva, D. 2015. Induction of salt
stress tolerance in cowpea [Vigna unguiculata (L.) Walp.] by arbuscular mycorrhizal fungi.
Legume Res. 38: 5, 579- 588.
4. AOAC. 1997. Official methods of analysis of the Association of Official Analytical
Chemists, 14th ed. Arlington, VA: AOAC.
5. Anderson, M.E. 1985. Determination of glutathione and glutathione disulfide in biological
samples. Methods Enzymol. 113: 548–555.
6. Aroca, R., Ruiz-Lozano, J.M., Zamarre˜no, A.M., Paza, J.A., Garcia-Mina, J.M., Pozoa,
M.J., and Lopez-Raez, J.A. 2013. Arbuscular mycorrhizal symbiosis influences strigolactone
production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170: 47–
55.
7. Asrar, A., and Elhindi, K.M. 2011. Alleviation of drought stress of marigold (Tagetes ereca)
plants by using arbuscular mycorrhizal fungi. Saudi J. Biol. Sci. 18: 93-98.
8. Bates, L.S., Waldren, R.P., and Teare, L.D. 1973. Rapid determination of free proline for
water-stress studies. Plant Soil. 39: 205-207.
9. Bilgili, U., Çarpici, E.B., Asik, B.B., and Çelik, N. 2011. Root and shoot response of
common vetch (Vicia sativa L.), forage pea (Pisum sativum L.) and canola (Brassica napus
L.) to salt stress during early seedling growth stages. Turkish J. Field Crops. 16: 1, 33-38.
10. Boyer, J.S. 1995. Why measure water status? In: Measuring the Water Status of Plants and
Soils, Academic Press, London, Pp: 1–12.
11. Bremmer, J.M., and Mulvaney, C.S. 1982. Nitrogen-total. In Methods of soil analysis. Part
2. Chemical and microbiological properties, 2nd ed., eds. A.L. Page, R.H. Miller, and D.R.
Keeney, 595–624. Madison, WI: American Society of Agronomy.
12. Cantrell IC and Linderman R.G., 2001. Preinoculation of lettuce and onion with VA
mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil. 233: 269–281.
13. Carlberg, I., and Mannervik, B. 1985. Glutathione reductase. Methods Enzymol. 113: 484–
490.
14. Colella, T., Candido, V., Campanelli, G., Camele, I., and Battaglia, D. 2014. Effect of
irrigation regimes and artificial mycorrhization on insect pest infestations and yield in
tomato crop. Phytoparasitica. 42: 235–246.
15. Collins, W.K., and Hawks Jr, S.N. 1993. Principles of flue-cured tobacco production.
Raleigh, NC: North Carolina State University.
16. CORESTA, 1994a. CORESTA recommended method No 35. Determination of total alkaloids
(as nicotine) in tobacco by continuous flow analysis. http://www.coresta.org/Recommended
Methods/CRM 35.pdf.
17. CORESTA, 1994b. CORESTA recommended method No 38. Determination of reducing
carbohydrates in tobacco by continuous flow analysis.
http://www.coresta.org/Recommended Methods/CRM 38.pdf.
18. Cosme, M., and Wurst, S. 2013. Interactions between arbuscular mycorrhizal fungi,
rhizobacteria, soil phosphorus and plant cytokinin deficiency change the root morphology,
yield and quality of tobacco. Soil Biol. Biochem. 57: 436-443.
19. Daei, G., Ardekani, M., Rejali, F., Teimuri, S., and Miransari, M. 2009. Alleviation of
salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular
mycorrhizal fungi under field conditions. J. Plant Physiol. 166: 217–225.
20. Datta, P., and Kulkarni, M. 2014. Arbuscular mycorrhizal colonization improves growth and
biochemical profile in Acacia arabica under salt stress. J. BioSci. Biotech. 3: 235-245.
21. Dionisio-Sese, M.L., and Tobita, S. 1998. Antioxidant responses of rice seedlings to salinity
stress. Plant Sci. 135: 1-9.
22. Enteshari, S.H., and Hajbagheri, S. 2011. Effect of mycorrhizal fungi on photosynthetic
pigments, root colonization and morphological characteristic of salt stressed Ocimum
basilicum L. Iran. J. Plant Physiol. 1(4): 215-222.
23. Fritz, C., Palacios-Rojas, N., Feil, R., and Stitt, M. 2006. Regulation of secondary
metabolism by the carbonenitrogen status in tobacco: nitrate inhibits large sectors of
phenylpropanoid metabolism. Plant J. 46: 533-548.
24. Gerdemann, J.W. 1975. Vesicular arbuscular mycorrhizal. In: Torrey DG, Clarkson DTC,
editors. The Development and Function of Roots. London: Academic Press. Pp: 575–591.
25. Giovannetti, M., and Mosse, B. 1980. Estimating the percentage of root length colonized
(Gridline-Intersect Method). New Phytol. 84: 489–500.
26. Giri, B., and Mukerji, K.G. 2004. Mycorrhizal inoculant alleviates salt stress in Sesbania
aegyptiaca and Sesbania grandiflora under field condition: evidence for reduced sodium and
improved magnesium uptake. Mycorrhiza. 14: 307-312.
27. Hedari Sharif Abadi, H. 2001. Plant aridy and drought. Research Institute of Forests and
Rangelands, Pp: 1-199.
28. Heikham, E., Kapoor, R., and Giri, B. 2009. Arbuscular mycorrhizal fungi in alleviation of
salt stress: a review. Ann. Bot-London. 104: 1263–1280.
29. Karaivazoglou, N.A., Papakosta, D.K., and Divanidis, S. 2006. Effect of Chloride in
Irrigation Water on Oriental (Sun-Cured) Tobacco. J. Plant Nut. 29: 1413–1431.
30. Karaivazoglou, N.A., Papakosta, D.K., and Divanidis, S. 2005. Effect of chloride in
irrigation water and form of nitrogen fertilizer on Virginia (flue-cured) tobacco. Field Crops
Res. 92: 61–74.
31. Kumar, A., Sharma, S., Mishra, S., and Dames, J.F. 2015. Arbuscular mycorrhizal
inoculation improves growth and antioxidative response of Jatropha curcas (L.) under
Na2SO4 salt stress. Plant Biosyst. 149: 2, 260–269.
32. Kumar, A., Sharma, S., and Mishra, S. 2010. Influence of arbuscular mycorrhizal (AM)
fungi and salinity on seedling growth, solute accumulation and mycorrhizal dependency of
Jatropha curcas L. J. Plant Growth Regul. 29: 297–306.
33. Latef, A.A.H.A., and Chaoxing, H. 2011. Effect of arbuscular mycorrhizal fungi on growth,
mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity
stress. Sci. Hort. 127: 228–233.
34. Law, M.Y., Charles, S.A., and Halliwell, B. 1983. Glutathione and ascorbic acid in spinach
(Spinacia oleracea) chloroplasts: the effect of hydrogen peroxide and of Paraquat. Biochem.
J. 210: 899–903.
35. Luck, H. 1974. Catalases. In: Bregmeyer, H.U. (Ed.), Methods of Enzymatic Analysis.
Academic Press, New York, USA.
36. Martinez-Ballesta, M.C., Martinez, V., and Carvajal, M. 2004. Osmotic adjustment, water
relations and gas exchange in pepper plants grown under NaCl or KCl. Environ. Exp. Bot.
52: 161–174.
37. Miransari, M. 2010. Contribution of arbuscular mycorrhizal symbiosis to plant growth under
different types of soil stress. Plant Biol. 12: 563–569.
38. Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:
405–410.
39. Moran, R. 1982. Formula for determination of chlorophyllous pigments extracted with N.N.
dimethylformamide. Plant Physiol. 69: 1371-1381.
40. Nakano, Y., and Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific
peroxidase in spinach chloroplast. Plant Cell Physiol. 22: 867–880.
41. Netondo, G.F., Onyango, J.C., and Beck, E. 2004. Crop physiology and metabolism.
Sorghum and salinity: I. Response of growth, water relation and ion accumulation to NaCl
salinity. Crop Soc. Am. 44: 797-805.
42. Olsen, S.R., and Sommers, L.E. 1982. Phosphorus. In Methods of soil analysis. Part 2.
Chemical and microbiological properties, 2nd ed., eds. A.L. Page, R.H. Miller, and D.R.
Keeney, 403–430. Madison, WI: American Society of Agronomy.
43. Philips, J., and Hayman, D.S. 1970. Improved procedure for cleaning roots andstaining
parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans
Br MycolSoc. 55: 158–161.
44. Porcel, R., Barea, J.M., and Ruiz-Lozano, J.M. 2004. Arbuscular mycorrhizal influence on
leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to
drought stress. J. Exp. Bot. 55: 1743-1750.
45. Selvakumar, G., Kim, K., Hu, S., and Sa, T. 2014. Effect of Salinity on Plants and the Role
of Arbuscular Mycorrhizal Fungi and Plant Growth-Promoting Rhizobacteria in Alleviation
of Salt Stress. In: Ahmad P, Wani M.R, (eds). Physiological Mechanisms and Adaptation
Strategies in Plants Under Changing Environment, vol. 1. Springer New York Heidelberg
Dordrecht London. Pp: 116-137.
46. Schu¨ßler, A., and Walker, C., 2010. The Glomeromycota: a species list with new families
and genera. Edinburgh and Kew, UK: The Royal Botanic Garden; Munich, Germany:
Botanische Staatssammlung Munich; Oregon, USA: Oregon State University. URL:
http://www.amf-phylogeny.com. ISBN-13: 978- 1466388048; ISBN-10: 1466388048.
47. Sifola, M.I., and Postiglione, L. 2002. The effect of increasing NaCl in irrigation water on
growth, gas exchange and yield of tobacco Burley type. Field Crops Res. 74: 81–91.
48. Smith, S.E., and Read, D.J. 1997. Mycorrhizal symbiose Second edition. Academic Press,
London, U.K.
49. Turner, N.C. 1981. Techniques and experimental approaches for the measurement of plant
water status. Plant Soil. 58: 339–366.
50. Van Rossum, M.W.P.C., Alberda, M., and van der Plas, L.H.W. 1997. Role of oxidative
damage in tulip bulb scale micropropagation. Plant Sci. 130: 207–216.
51. Wu, Q.S., Zou, Y.N., and Abd_Allah, E.F. 2014. Mycorrhizal Association and ROS in
Plants. In: P. Ahmad (Ed): Oxidative Damage to Plants. DOI:
http://dx.doi.org/10.1016/B978-0-12-799963-0.00015-0©2014 Elsevier Inc. All rights
reserved. Pp: 453- 475.
52. Zhu, X.C., Song, F.B., Liu, S.Q., and Liu, T.D. 2011. Effects of arbuscular mycorrhizal
fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil.
346: 189–199.