Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum

Mycorrhiza - Tập 23 - Trang 71-86 - 2012
Heikham Evelin1, Bhoopander Giri2, Rupam Kapoor1
1Applied Mycology Laboratory, Department of Botany, University of Delhi, Delhi, India
2Department of Botany, Swami Shraddhanand College, University of Delhi, Delhi, India

Tóm tắt

The study unveils that inoculation with arbuscular mycorrhizal fungus (Glomus intraradices Schenck and Smith) prevents salt-induced ultrastructural alterations in fenugreek (Trigonella foenum-graecum L.) plants. Mycorrhizal (M) and non-mycorrhizal (NM) fenugreek plants were subjected to four levels of NaCl (0, 50, 100, and 200 mM NaCl). Salt-induced ultrastructural changes were captured using a Transmission Electron Microscope. Effects of salt on the ultrastructure of cells include shrinkage of protoplasm, widening apoplastic space between cell wall and cell membrane, disorganization of grana in chloroplast—swelling and reduction in the number of thylakoids, disintegration of chloroplast membrane, accumulation of plastoglobules, dilation of cristae and denser matrix in mitochondria, and aggregation of chromatin in nucleus. However, the extent of salt-induced ultrastructural damage was less in M plants as compared to NM plants. Lower lipid peroxidation and electrolyte leakage in M plants also indicated less membrane damage. This reduction of ultrastructure damage is a demonstration of enhanced tolerance in M plants to salt stress. The AMF-mediated lesser damage may be due to higher osmolyte (glycinebetaine, sugars) and polyamines concentration, and more and bigger plastoglobules (higher α-tocopherol concentration) in M plants as compared to NM plants. While lower Na+ and Cl− ions assures less ionic toxicity, higher osmolytes and tocopherols ensure osmotic adjustment and better capacity to scavenge free radicals generated due to salt stress, respectively.

Tài liệu tham khảo

Al-Garni SMS (2006) Increasing NaCl-salt tolerance of a halophytic plant Phragmites australis by mycorrhizal symbiosis. Am Eurasian J Agric Environ Sci 1:119–126 Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109:1–7 Allen EB, Cunningham GL (1983) Effects of vesicular-arbuscular mycorrhizae on Distichlis spicata under three salinity levels. New Phytol 93:227–236 Andrea B, Tani C (2009) Ultrastructural effects of salinity in Nicotiana bigelovii var. bigelovii callus cells and Allium cepa roots. Caryologia 62:124–133 Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:207–216 Austin JR II, Frost E, Vidi PA, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein sub compartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703 Basu S, Acharya S, Bandara M, Thomas J (2004) Agronomic and genetic approaches for improving seed quality and yield of fenugreek (Trigonella foenum-graecum L.) in western Canada. In: Proceedings of science of changing climates—impact on agriculture, forests and wetlands, 20–23 Jul. 2004. University of Alberta, Edmonton, AB, Canada, pp 38 Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207 Borde M, Dudhane M, Jite P (2011) Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glauca) crop under salinity stress condition. Crop Prot 30:265–271 Brehelin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266 Chattopadhayay MK, Tiwari BS, Chattopadhayay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199 Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20 Ciamporova M, Mistrik I (1993) The ultrastructural response of root cells to stressful conditions. Environ Exp Bot 33:11–26 Cohen AS, Popovic RC, Zalik S (1979) Effects of polyamines on chlorophyll and protein content, photochemical activity and chloroplast ultrastructure of barley leaf discs during senescence. Plant Physiol 64:717–720 Deltour R, Bronchart R (1971) Changements de l’ultrastructure des cellules radiculaires de Zea mays au dfibut de la germination. Planta 97:197–207 Duke AJ (1986) Handbook of legumes of world economic importance. Plemus, New York Elkahoui S, Hernandez AJ, Abdelly C, Ghrir R, Limam FB (2005) Effects of salt on lipid peroxidation and antioxidant enzyme activities of Catharanthus roseus suspension cells. Plant Sci 168:607–613 Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1281 Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217 Feng G, Zhang FS, Xl L, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190 Fidalgo F, Santos A, Santos I, Salema R (2004) Effects of long-term salt stress on antioxidant defence systems, leaf water relations and chloroplast ultrastructure of potato plants. Ann Appl Biol 145:185–192 Flowers TJ, Lauchli A (1983) Sodium versus potassium: substitution and compartmentation. Encycl Plant Physiol 15B:651–681 Galston AW, Kaur Sawhney R (1990) Polyamines in plant physiology. Plant Physiol 94:406–410 Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea). J Agron Crop Sci 195:110–123 Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33 Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500 Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175 Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307 Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45 Gupta SD (2007) Plasma membrane ultrastructure in embryogenic cultures of orchard grass during NaCl stress. Biol Plant 51:759–763 Hamilton EW III, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266–1274 Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553 Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499 Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198 Hecht-Buchholz C, Marschner H (1970) Veranderungen der Feinstrukturen von Zellen der Maiswuzelspitze bei Entzung von Kalium. Z Planzenphysiology 63:416–427 Hernandez JA, Olmos E, Corpas FJ, Sevilla F, del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167 Hoque MA, Okuma E, Banu Mst NA, 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 Huang CX, Van Steveninck RFM (1990) Salinity induced structural changes in meristematic cells of barley roots. New Phytol 115:17–22 Juan M, Rivero RM, Romero L, Ruiz JM (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ Exp Bot 54:193–210 Kapoor R, Giri B, Mukerji KG (2002) Mycorrhization of coriander to enhance the concentration and quality of oil in seeds. J Sci Food Agric 82:1–4 Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138 Kasperbauer MJ, Hamilton JL (1984) Chloroplast structure and starch grain accumulation in leaves that received different red and far-red levels during development. Plant Physiol 74:967–970 Katsuhara M, Kawasaki T (1996) Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol 37:169–173 Kaya C, Ashraf M, Sonmez O, Aydenir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121:1–6 Koyro HN (1997) Ultrastructural and physiological changes in root cells of Sorghum plants (Sorghum bicolor x S. sudanensis cv. Sweet Sioux) induced by NaCl. J Exp Botany 48:693–706 Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500–504 Lopez-Carbonell M, Alegre L, Van Onckelen H (1994) Changes in cell ultrastructure and endogenous abscissic acid and indole-3-acetic acid concentrations in Fatsia japonica leaves under polyethylene glycol-induced water stress. Plant Growth Regul 15:165–174 Makela P, Karkkainen J, Somersalo S (2000) Effect of glycinebetaine on chloroplast ultrastructure, chlorophyll and protein content, and Rubisco activities in tomato grown under drought or salinity. Biol Plant 43:471–475 Manchanda G, Garg N (2011) Alleviation of salt-induced ionic, osmotic and oxidative stresses in Cajanus cajan nodules by AM inoculation. Plant Biosyst 145:88–97 Mansour MMF, Al-Mutawa MM (1999) Stabilization of plasma membrane by polyamines against salt stress. Cytobios 100:7–17 Marcé M, Brown DS, Capell T, Figueras X, Tiburcio AF (1995) Rapid high-performance liquid chromatographic method for the quantification of polyamines as their dansyl derivatives: application to plant and animal tissues. J Chromatogr B 666:329–335 Minocha R, Shortle WC, Long SL, Minocha SC (1994) A rapid and reliable procedure for extraction of cellular polyamines and inorganic ions from plant tissues. J Plant Growth Regul 13:187–193 Miyake H, Mitsuya S, Rahman MDS (2006) Ultrastructural effects of salinity stress in higher plants. In: Rai AK, Takebe T (eds) Abiotic stress tolerance in plants. Springer, The Netherlands, pp 215–226 Murakami S, Packer L (1970) Protonation and chloroplast membrane structure. J Cell Biol 47:332–351 Oksanen E, Riikonen J, Kaakinen S, Holopainen T, Vapaavuori E (2005) Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone. Glob Chang Biol 11:732–748 Paramonova NV, Shevyakova NI, Kuznetsov VV (2004) Ultrastructure of chloroplasts and their storage inclusions in the primary leaves of Mesembryanthemum crystallinum affected by putrescine and NaCl. Russ J Plant Physiol 51:86–96 Pareek A, Singla SL, Grover A (1997) Short-term salinity and high temperature stress associated ultrastructural alterations in young leaf cells of Oryza sativa L. Ann Bot 80:629–639 Peng J, Li Y, Shi P, Chen X, Lin H, Zhao B (2011) The differential behavior of arbuscular mycorrhizal fungi in interaction with Astragalus sinicus L. under salt stress. Mycorrhiza 21:27–33 Petropoulos GA (2002) Fenugreek, The genus Trigonella. Taylor and Francis, London Philips J, Hayman DS (1970) Improved procedure for cleaning roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161 Porcel R, Aroca R, Ruiz-Lozano JM (2011) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev. doi:10.1007/s13593-011-0029-x Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222 Sadasivam S, Manickam A (2008) Biochemical methods, 3rd edn. New Age International Publishers Sannazzaro AI, Echeverria M, Alberto EO, Ruiz OA, Menendez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45:39–46 Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151 Sharma MP, Gour A, Bhatia NP, Adholeya A (1996) Growth responses and dependence of Acacia nilotica var. cupriformis on the indigenous arbuscular mycorrhizal consortium of a marginal wasteland soil. Mycorrhiza 6:169–177 Sheng M, Tang M, Chan H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296 Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430 Taylor AO, Craig AS (1971) Plants under climatic stress: II. Low temperature, high light effects on chloroplast ultrastructure. Plant Physiol 47:719–725 Tiburico AF, Besford RT, Capell T, Borrell A, Testillano PS, Risueno MC (1994) Mechanisms of polyamine action during senesence responses induced by osmotic stress. J Exp Bot 45:1789–1800 Turkmen O, Sensoy S, Demir S, Erdine C (2008) Effects of two different AMF species on growth and nutrient content of pepper seedlings grown under moderate salt stress. Afr J Biotechnol 7:392–396 Utrillas MJ, Alegre L (1997) Impact of water stress on leaf anatomy and ultrastructure in Cynodon dactylon (L.) under natural conditions. Int J Plant Sci 158:313–324 Wang S, Wan C, Wang Y, Chen H, Zhou Z, Fu H, Sosebee RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistance plants of the Alxa Desert, China. J Arid Environ 56:525–539 Werker E, Lerner HR, Weimberg R, Poljakoff-Mayber A (1983) Structural changes occurring in nuclei of barley root cells in response to a combined effect of salinity and ageing. Am J Bot 70:222–225 Yamane K, Rahman MS, Kawasaki M, Taniguchi M, Miyake H (2004) Pretreatment with a low concentration of methyl viologen decreases the effects of salt stress on chloroplast ultrastructure in rice leaves (Oryza sativa L.). Plant Prod Sci 7:435–441 Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788 Zhao FG, Qin P (2004) Protective effect of exogenous polyamines on root tonoplasts function against salt stress in barley seedlings. Plant Growth Regul 42:97–103