PROTEOMIC STUDIES IN THE SYMBIOTIC ASSOCIATIONS BETWEEN ARBUSCULAR MYCORRHIZAL FUNGI Funneliformis mosseae WITH MELON (Cucumis melo L.) UNDER SALT CONDITIONS
Yong-Hong Lin
Department of Plant Industry, National Pingtung University of Science and Technology, Pingtung, TaiwanChung-Li Wang
Department of Plant Industry, National Pingtung University of Science and Technology, Pingtung, TaiwanJuei-Yu Chiu
Department of Environmental Science and Engineering, National Pingtung University of Science and Technology, Pingtung, TaiwanAbstract
Arbuscular mycorrhizal fungi (AMF) that can cause mutualism with higher plants. Some studies showed that the symbiosis of AMF will increase nutrients absorption, the capacity of anti-stress (e.g. drought, salt and disease) by melon (Cucumis melo L.). This study evaluated the roles of proteins on salt-tolerance mechanism after melon was symbiotic with AMF (Funneliformis mosseae). The melons were cultivated in the hydroponic solution containing 0 M, 0.042 M or 0.084 M NaCl for inoculated AMF and non-AMF inoculated seedlings. Root apice of AMF seedling after treating with different NaCl concentrations that were chosen for the estimation of proteins. The results showed that 12 proteins were significantly different after treating with different sodium chlorite (NaCl) concentrations, with proteins that four upregulated and eight downregulated. The tolerance of NaCl stress by root of melon that was inoculated by AMF were attributable to cellular activities involved in carbohydrate metabolism, energy metabolism, production of organic acid, relief of salt injury, which may be critical for promotion of nutrients absorption, anti-stress. This study can offer an important clue to advanced genomic exploration for the inoculation of AMF on different plants.
Keywords:
arbuscular mycorrhizal fungi (AMF), melon, salt-tolerance, proteinReferences
Alqarawi, A.A., Hashem, A., Abd Allah, E.F., Alshahrani, T.S., Huqail, A.A. (2014b). Effect of salinity on moisture content, pigment system, and lipid composition in Ephedra alata Decne. Acta Biol. Hung., 65, 61–71. https://doi.org/10.1556/ABiol.65.2014.1.6
Alqarawi, A.A., Abd Allah, E.F., Hashem, A. (2014a). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J. Plant Interact., 9, 802–810. https://doi.org/10.1080/17429145.2014.949886
Auge, R.M. (2001). Water relations, drought and vesiculararbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3–42. https://doi.org/10.1007/s005720100097
Balliu, A., Sallaku, G., Rewald, B. (2015). AMF inoculation enhances growth and improves the nutrient uptake rates of transplanted, salt-stressed tomato seedlings. Sustainability, 7(12), 15967–15981. https://doi.org/10.3390/su71215799
Bansal, P., Sharma, P., Goyal, V. (2002). Impact of lead and cadmium on enzyme of citric acid cycle in germinating pea seeds. Biol. Plant., 45, 125–127. https://doi.org/10.1023/A:1015173112842
Bray, E.A. (1997). Plant responses to water deficit. Trends Plant Sci., 2, 48–54. https://doi.org/10.1016/S1360-1385(97)82562-9
Bethke, P.C., Jones, R.L. (1998). Gibberellin signaling. Curr. Opin. Plant Biol., 1, 440–446. https://doi.org/10.1016/S1369-5266(98)80270-7
Brumbarova, T., Matros, A., Mock, H.P., Bauer, P. (2008). A proteomic study showing differential regulation of stress, redox regulation and peroxidase proteins by iron supply and the transcription factor FER. Plant J., 54, 321–334. https://doi.org/10.1111/j.1365-313X.2008.03421.x
Ceccarelli, D.F.J., Frappier, L. (2000). Functional analyses of the EBNA1 origin DNA binding protein of Epstein-Barr virus. J. Virol., 74, 4939–4948. https://doi.org/10.1128/.74.11.4939-4948.2000
Chen, J.H., Lin, Y.H. (2010). Sodium chloride causes variation in organic acids and proteins in tomato root. Afr. J. Biotechnol., 9, 8161–8167. https://doi.org/10.5897/AJB09.1994
Cletus, J., Balasubramanian, V., Vashisht, D. (2013). Transgenic expression of plant chitinases to enhance disease resistance. Biotechnol. Lett., 35, 1719–1732. https://doi.org/10.1007/s10529-013-1269-4
Delhaize, E., Ryan, P.R. (1995). Aluminum toxicity and tolerance in plants. Plant Physiol., 107, 315–321. https://doi.org/10.1104/pp.107.2.315
Du, H., Feng, B.R., Yang, S.S., Huang, Y.B., Tang, Y.X. (2012). The R2R3-MYB transcription factor gene family in maize. PloS ONE, 7(6): https://doi.org/10.1371/journal.pone.0037463
Dhingra, H.R., Varghese, T.M. (1985). Effect of growth regulators on the in vitro germination and tube growth of maize (Zea mays L.) pollen from plants raised under sodium chloride salinity. New Physiol., 100, 563–569. https://doi.org/10.1111/j.1469-8137.1985.tb02802.x
Fidelibus, M.W., Martin, C.A., Wright, G.C., Stutz, J.C. (2000). Effect of arbuscular mycorrhizal (AM) fungal communities on growth of ‘Volkamer’ lemon in continually moist or periodically dry soil. Sci. Hortic., 84, 127–140. https://doi.org/10.1016/S0304-4238(99)00112-0
Fidelibus, M.W., Martin, C.A., Stutz, J.C. (2001). Geographic isolates of Glomus increase root growth and whole-plant transpiration of citrus seedlings grown with high phosphorus. Mycorrhiza, 10, 231–236. https://doi.org/10.1007/s005720000084
Gadkar, V., David-Schwartz, R., Kunik, T., Kapulnik, Y. (2001). Arbuscular mycorrhizal fungal colonization. Factors involved in host recognition. Plant Physiol., 127, 1493–1499. https://doi.org/10.1104/pp.010783
Gamalero, E., Berta, G., Massa, N., Glick, B.R., Lingua, G. (2010). Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences for the growth of cucumber under salt-stress conditions. J. Appl. Microbiol., 108, 236–245. https://doi.org/10.1111/j.1365-2672.2009.04414.x
Gao, D., Abernathy, B., Rohksar, D., Schmutz, J., Jackson, S.A. (2014). Annotation and sequence diversity of transposable elements in common bean (Phaseolus vulgaris). Front Plant Sci., 5, 339. https://doi.org/10.3389/fpls.2014.00339
Gharahdaghi, F., Weinberg, C.R., Meagher, D.A., Imai, B.S., Mische, S.M. (1999). Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis, 20, 601–605. https://doi.org/10.1002/(SICI)1522-2683(19990301)20:3<601::AID-ELPS601>3.0.CO;2-6
Gorg, A., Postel, W., Gunther, S. (1998). The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis, 9, 531–546. https://doi.org/10.1002/elps.1150090913
Graham, J.H., Syvertsen, J.P. (1985). Host determinants of mycorrhizal dependency of citrus rootstock seedlings. New Phytol., 101, 667–676. https://doi.org/10.1111/j.1469-8137.1985.tb02872.x
Hashem, A., Abd Allah, E., Alqarawi, A.A., El-Didamony, G., Alwhibi, M.S., Egamberdieva, D., Ahmad, P. (2014). Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak. J. Bot., 46, 2003–2013. https://doi.org/10.1007/BF00041276
Hashem, A., Abd Allah, E.F., Alqarawi, A.A., Aldubise, A., Egamberdieva, D. (2015). Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J. Plant Interact., 10, 230–242. https://doi.org/10.1080/17429145.2015.1052025
Hashem, A., Abd Allah, E.F., Alqarawi, A.A., Al-Huqail, A.A., Wirth, S., Egamberdieva, D. (2016a). The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol., 7, 1089. https://doi.org/10.3389/fmicb.2016.01089
Hashem, A., Alqarawi, A.A., Radhakrishnan, R., Al-Arjani, A.B.F., Aldehaish, H.A., Egamberdieva, D., Abd Allah, E.F. (2018). Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J. Biol. Sci., 25, 1102–1114. https://doi.org/10.1016/j.sjbs.2018.03.009
Hayes, J.D., McLellan, L.I. (1999). Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Rad. Biol. Med. Res., 31, 273–300. https://doi.org/10.1080/10715769900300851
Huang, J.C., Jiang, W.J., Lin, G.C. (2012). Research on application of a growth medium containing mycorrhizal for nursery in melons (Cucumis melo L.) crops. Bull. Tainan District Agric. Res. Ext. Station, 60, 38–47. https://doi.org/10.29558/XLZY.201212.0005 (in Chinese)
Huang, Z., Zou, Z., He, C. et al. (2011). Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil, 339, 391–399. https://doi.org/10.1007/s11104-010-0591-z
Iqbal, N., Umar, S., Khan, N.A. (2015). Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J. Plant Physiol., 178, 84–91. https://doi.org/10.1016/j.jplph.2015.02.006
Kanaoka, M., Urbanb, S., Freemanc, M., Okada, K. (2005). An Arabidopsis Rhomboid homolog is an intramembrane protease in plants. FEBS Letters, 579, 5723–5728. https://doi.org/10.1016/j.febslet.2005.09.049
Kochian, L.V. (1995): Cellular mechanisms of aluminum toxicity and resistance in plants. Plant Mol. Biol., 46, 237–260. https://doi.org/10.1146/annurev.pp.46.060195.001321
Konish, S., Miyamoto, S., Taki, T. (1985). Stimulatory effect of aluminum on tea plants grown under low and high phosphorus supply. Soil Sci. Plant Nutr., 31, 361–368. https://doi.org/10.1080/00380768.1985.10557443
Koonin, E.V., Makarova, K.S., Rogozin, I.B., Davidovic, L., Letellier, M.C., Pellegrini, L. (2003). The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genom Biol., 4, 19. https://doi.org/10.1007/978-1-4020-6311-4_4
Koske, R.E., Gemma, J.N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. Mycol. Res., 92, 486–505. https://doi.org/10.1016/S0953-7562(89)80195-9
Lin, C.Y., Wang, V.C., Shui, H.A., Juang, R.H., Hour, A.L., Chen, P.S., Huang, H.M., Wu, S.Y., Lee, J.C., Tsai, T.Z., Chen, H.M. (2009). A comprehensive evaluation of imidazole-zinc reverse stain for current proteomic researches. Proteomic, 9, 696–709. https://doi.org/10.1002/pmic.200700470
Ling, H. Q., Bauer, P., Bereczky, Z., Keller, B. (2002). The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc. Natl. Acad Sci. USA, 99, 13938–13943. https://doi.org/10.1073/pnas.212448699
Lopez-Millan, A.F., Morales, F., Abadia, A., Abadia, J. (2000). Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiol., 124, 873–884. https://doi.org/10.1104/pp.124.2.873
Mo, Y., Wang, Y., Yang, R., Zheng, J., Liu, C., Li, H., Ma, J., Zhang, Y., Wei, C., Zhang, X. (2016). Regulation of plant prowth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front. Plant Sci., 7, 644. https://doi.org/10.3389/fpls.2016.00644
Pysh, L.D., Wysocka-Diller, J.W., Camilleri, C., Bouchez, D., Benfey, P.N. (1999). The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE gene. Plant J., 18, 111–119. https://doi.org/10.1046/j.1365-313X.1999.00431.x
Rengel, Z. (1996). Uptake of aluminium by plant cells. New Phytol., 134, 389–406. https://doi.org/10.1111/j.1469-8137.1996.tb04356.x
Roldan-Fajardo, B.E. (1994). Effect of indigenous arbuscular mycorrhizal endophytes on the development of six wild plants colonizing a semi-arid area in south-east Spain. New Phytol., 127, 115–121. https://doi.org/10.1111/j.1469-8137.1994.tb04265.x
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
Sánchez-Rodríguez, C. (2012). Chitinase-like1/pom-pom1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell, 24, 589–607. https://doi.org/10.1105/tpc.111.094672
Selig, M., Xavier, K.B., Santos, H., Schönheit, P. (1997). Comparative analysis of Embden-Meyerhof and Entner-Doudoroff glycolytic pathways in hyperthermophilic archaea and the bacterium Thermotoga. Arch. Microbiol., 167, 217–232. https://doi.org/10.1007/BF03356097
Sheehan, D., Meade, G., Foley, V.M., Dowd, C.A. (2001). Structure, function, and evolution of glutathione tranferrases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J., 360, 1–16. https://doi.org/10.1042/0264-6021:3600001
Shekoofeh, E., Sepideh, H., Roya, R. (2012). Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. J. Biotech., 11, 2223–2235. https://doi.org/10.5897/AJB11.1672
Shevchenko, A., Wilm, M., Vorm, O., Mann, M. (1996). Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem., 68, 850–858. https://doi.org/10.1021/ac950914h
Shih, S.C., Huang, H. (1993). Effects of salt content on the germination and seedling growth of muskmelon. Bull. Kaoh. Agric. Ext. Station., 5, 62–70. (In Chinese) https://doi.org/10.19045/bspab.2018.700218
Silverstone, A.L., Ciampaglio, C.N., Sun, T.P. (1998). The Arabidopsis RGA gene encodes a trascriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell., 10, 155–169. https://doi.org/10.2307/3870695
Singh, N.K., Haseguwa, P.M. (1987). Protein associate with adaptation of cultured to tobacco cells to NaCl. Plant Physiol., 7, 126–137, https://doi.org/10.1104/pp.79.1.126
Sun, T.P. (2000). Gibberellin signal transduction. Curr. Opin. Plant Biol., 3, 374–380, https://doi.org/10.1016/S1369-5266(00) 00099-6Tang, M., Chen, H., Huang, J.C., Tian, Z.Q. (2009). AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. Soil Biol. Biochem., 41, 936–940, https://doi.org/10.1016/j.soilbio.2008.11.007
Thimm, O., Essigmann, B., Kloska, S., Altmann, T. (2001). Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol., 127, 1030–1043. https://doi.org/10.1104/pp.010191
Tiffin, L.O. (1966). Iron translocation I. plant culture, exudate sampling, iron-citrate analysis. Plant Physiol., 41, 510–514. https://doi.org/10.1104/pp.41.3.510
Wu, Q.S., Zou, Y.N., Xia, R.X., Wang, M.Y. (2007). Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot. Studies, 48, 147–154. https://doi.org/10.1093/aob/mcm113
Yamaguchi, T. (1983). World vegetables. AVI Press, Westport. https://doi.org/10.1007/978-94-011-7907-2_1
Ye, L., Zhao, X., Bao, E., Cao, K., Zou, Z. (2019). Effects of arbuscular mycorrhizal fungi on watermelon growth, elemental uptake, antioxidant, and photosystem II activities and stress-response gene expressions under salinity-alkalinity stresses. Front Plant Sci., 10, 863. https://doi.org/10.3389/fpls.2019.00863
Zhou, G., Li, H., DeCamp, D., Chen, S., Shu, H., Gong, Y., Flaig, M., Gillespie, J.W., Hu, N., Taylor, P.R., Emmert-Buck, M.R., Liotta, L.A., Petricoin, E.F., Zhao, Y. (2002). 2D differential in-gel electrophoresis for the identification of esophageal scans cell cancer-specific protein markers. Mol. Cell. Proteomics, 1, 117–124. https://doi.org/10.1074/mcp.M100015-MCP200
Department of Plant Industry, National Pingtung University of Science and Technology, Pingtung, Taiwan
Department of Plant Industry, National Pingtung University of Science and Technology, Pingtung, Taiwan
Department of Environmental Science and Engineering, National Pingtung University of Science and Technology, Pingtung, Taiwan
License
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.
