Document Type : Research Paper


1 Genetics and Agricultural Biotechnology Institute of Tabarestan, Sari Agricultural Sciences and Natural Resources University

2 Genetics and Agricultural biotechnology Institute of Tabarestan (GABIT), Sari Agricultural Sciences and Natural Resources University (SANRU), Sari, Iran

3 Department of Soil Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

4 Department of plant protection, Sari University of agricultural sciences and natural resources, Sari, Iran


Arbuscular mycorrhizal fungi (AMF) symbiosis could mitigate the adverse effects of abiotic stresses in various plants. The aim of this study was to investigate the effect of AMF-inoculation on expression of several stress-responsive genes in two rice cultivars under different water conditions. The seedlings of Tarom-Hashemi and Nemat rice cultivars were transplanted in soil with or without G. mosseae spores. At the tilling stage, the AMF-inoculated (+AMF) and AMF-uninoculated (−AMF) plants were subjected to flooded and water deficit conditions (70% field capacity (FC) and 50%FC). The genes expression was evaluated by qRT-PCR and reported relative to control (flooded, -AMF) plants. The results showed lower expression of osDREB2A in +AMF plants in comparison with –AMF plants under water deficient conditions. The expression of OsPIP1;2 was significantly increased in roots of +AMF to –AMF plants. But, the expression of this gene was decreased in shoots of +AMF and –AMF plants in comparison with control plants. The stress-responsive gene transcripts, OsPIP2;3, OsGH3-8, OsLTP, OsAOS2 and OsADC1 in +AMF rice cultivars was higher than -AMF plants at both water deficit conditions. Expression of OsP5CS in +AMF and –AMF plants was increased in comparison with control plants, though, their differences was not significant. In 70%FC, OsEXP15 gene expression of +AMF and –AMF root plants was increased in comparison with control plants. However, under 50%FC the gene expression was decreased and not changed in -AMF and +AMF plants, respectively. It seems AMF induced changes in rice genes expression may enhance tolerance to water deficit conditions.


Main Subjects

  • Alca ́zar R, C.J., Patron M, Altabella T, Tiburcio AF Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 2006. 128: p. 448-455.
  • Aroca, R., et al., Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Annals of Botany, 2006. 98(6): p. 1301-1310.
  • Aroca, R., Porcel, R., and Ruiz-lozano, J. M., How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? . New Phytol, 2006. 173: p. 808-816.
  • Asch F, D.M., Sow A, Audebert A Drought-induced changes in rooting patterns and assimilate partitioning between root and shoot in upland rice. Field Crop Res, 2005. 93: p. 223-236.
  • Augé, R.M., Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 2001. 11(1): p. 3-42.
  • Azhiri-Sigari, T.A., Yamauchi, A., Kamoshita, A., Wade, L. J., Genotypic variation in response of rainfed lowland rice to drought would help to elucidate how rooting depth and deep root and rewatering II. Root growth. Plant Prod Sci, 2000. 3: p. 180-188.
  • Bárzana, G., Aroca, R., Bienert, G. P., Chaumont, F., and Ruiz-Lozano, J. M., New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maiz. . Plant Microbe Interact, 2014. 27: p. 349-363.
  • Bárzana, G., Aroca, R., Paz, J. A., Chaumont, F., Martinez-Ballesta, M. C., and M. Carvajal, et al., Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann. Bot. 109, 1009-1017. doi: 10.1093/aob/mcs007.
  • Bernier J, A.G., Serraj R, Kumar A, Spaner D., Breeding upland rice for drought resistance. JSciFoodAgric, 2008. 88: p. 927-39.
  • Capell, T., Escobar, C., Liu, H., Burtin, D., Lepri, O., and Christou, P. , Over-expression of the oat arginine decarboxylase cDNA in transgenic rice(Oryza sativaL.) affects normal development patternsin vitroand results inputrescine accumulation in transgenic plants. Appl. Genet., 1998. 97: p. 246-254.
  • Chang, Y.-A., et al., Regulation of rice sucrose transporter 4 gene expression in response to insect herbivore chewing. Journal of Plant Interactions, 2019. 14(1): p. 525-532.
  • Choudhary, N., R. Sairam, and A. Tyagi, Expression of Δ¹-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.).
  • Cuevas, J.C., et al., Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant physiology, 2008. 148(2): p. 1094-1105.
  • Cui, K., et al., Mapping QTLs for seedling characteristics under different water supply conditions in rice (Oryza sativa). Physiologia Plantarum, 2008. 132(1): p. 53-68.
  • Dhakarey, R., P. Kodackattumannil Peethambaran, and M. Riemann, Functional analysis of jasmonates in rice through mutant approaches. Plants, 2016. 5(1): p. 15.
  • Ding X, C.Y., Huang L, Zhao J, Xu C, Li X, Wang S. , Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. T. he Plant Cell, 2008. 20: p. 228-240.
  • Domingo C, A.F., Tharreau D, Iglesias DJ, Talón M., Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant Microbe Interact., 2009. 22(2): p. 201-210.
  • Domingo C, A.F., Tharreau D, Iglesias DJ, Talon M. , Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Molecular Plant-Microbe Interactions 2009. 22: p. 201-210.
  • FAO, in FAOSTAT database, F.a.A. Organization, Editor. 2013: Rome: Food and Agricultral Organization.
  • Guo, L.Y., H.; Zhang, X.; Yang, S., Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. Exp. Bot, 2013. 64: p. 1755-1767.
  • Hadiarto, T. and L.-S.P. Tran, Progress studies of drought-responsive genes in rice. Plant cell reports, 2011. 30(3): p. 297-310.
  • Hause B, M.W., Miersch O, Kramell R, Strack D () Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiology, 2002. 130: p. 1213-1220.
  • Igarashi, Y., et al., Characterization of the gene for Δ 1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant molecular biology, 1997. 33(5): p. 857-865.
  • , R.-L., Arbuscular mycorhhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza, 2003. 13:309-317.
  • , R.-L., Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. . Mycorrhiza 2003. 13: p. 309-317.
  • Johanson, I., Karlsson, M., Shukla, V.K., Chrispeels, M.J., Larsson, C. and Kjellbom, P., Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. . Plant Cell . 1998. 10: p. 451-459.
  • Jovanovic, Z., et al., The expression of drought responsive element binding protein ('DREB2A') related gene from pea ('Pisum sativum'L.) as affected by water stress. Australian Journal of Crop Science, 2013. 7(10): p. 1590-1596.
  • Kant, P., et al., Functionalgenomicsbased identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant, Cell & Environment, 2008. 31(6): p. 697-714.
  • Kavi Kishor, P., et al., Overexpression of delta 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant physiology (Lancaster, Pa.)(USA), 1995.
  • Khattab, H., et al., Effect of selenium and silicon on transcription factors NAC5 and DREB2A involved in drought-responsive gene expression in rice. Biologia plantarum, 2014. 58(2): p. 265-273.
  • Kruse, E., Uehlein, N., Kaldenhoff, R., The aquaporins. Genome Biology 2006. 7: p. 206.
  • Lemoine, R., et al., Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in plant science, 2013. 4: p. 272.
  • Lian, H.L., Yu, X., Ye Q, Ding X, Kitagawa, Y., Kwak, S. S., Su, W. A.,Tang,  C., The role of aquaporin RWC3 in drought avoidance in rice. . Plant Cell Physiol 2004. 45: p. 481-489.
  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K.,, Two transcription factors, DREB1 and DREB2,with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression respectively,in Arabidopsis. . PlantCell, 1998. 10: p. 1391-1406.
  • Ma Y, S.V., Merewitz EB Transcriptome analysis of creeping bentgrass exposed to drought stress and polyamine treatment. PLoSONE 2017. 12(4): p. e0175848.
  • Mahdieh, M., et al., Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant and Cell Physiology, 2008. 49(5): p. 801-813.
  • Marjanović, Ž., Uehlein, N., Kaldenhoff, R., Zwiazek, J. J., Weiß, M., Hampp, R., & Nehls, U. (). . Aquaporins in poplar: what a difference a symbiont makes! Planta, 2005. 222 (2): p. 258-268.
  • Mei, C., et al., Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Molecular Plant-Microbe Interactions, 2006. 19(10): p. 1127-1137.
  • Morillon, R. and M.J. Chrispeels, The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proceedings of the National Academy of Sciences, 2001. 98(24): p. 14138-14143.
  • Parniske, M., Arbuscular mycorrhiza: the mother of plant root endosymbioses. Rev. Microbiol, 2008. 6,: p. 763-775.
  • Pawłowicz, I., et al., Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. Journal of applied genetics, 2017. 58(4): p. 421-435.
  • Porcel, R., et al., PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant molecular biology, 2006. 60(3): p. 389-404.
  • Porcel, R., Aroca, R., and Ruiz-Lozano, J. M., Salinity stress alleviation using arbuscular mycorrhizal fungi. . A review. Agron. Sustain. Dev., 2012. 32: p. 181-200.
  • Porcel, R. and J.M. Ruiz-Lozano, Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of experimental botany, 2004. 55(403): p. 1743-1750.
  • Postaire, O., et al., A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant physiology, 2010. 152(3): p. 1418-1430.
  • Qin, F., et al., Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal, 2007. 50(1): p. 54-69.
  • Rapparini, F. and J. Peñuelas, Mycorrhizal fungi to alleviate drought stress on plant growth, in Use of Microbes for the Alleviation of Soil Stresses, Volume 1. 2014, Springer. p. 21-42.
  • Recchia, G.H., et al., Arbuscular mycorrhizal symbiosis leads to differential regulation of drought-responsive genes in tissue-specific root cells of common bean. Frontiers in microbiology, 2018. 9: p. 1339.
  • Ruiz-Sa´nchez M, A.R., Mun˜oz Y, Polo´n R, Ruiz-Lozano JM and (rbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862-869. 2010) A.
  • Sakurai, J., et al., Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant and Cell Physiology, 2005. 46(9): p. 1568-1577.
  • Secchi, F., C. Lovisolo, and A. Schubert, Expression of OePIP2. 1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Annals of Applied Biology, 2007. 150(2): p. 163-167.
  • Singh, A.P., et al., OsJAZ9 overexpression improves potassium deficiency tolerance in rice by modulating jasmonic acid levels and signaling. bioRxiv, 2018: p. 440024.
  • Smith SE, R.D., Mycorrhizal symbiosis, 3rd edn. Academic Press, Elsevier, London. 2008
  • Sugaya, S., et al. Expression analysis of genes encoding aquaporins during the development of peach fruit. in XXVI International Horticultural Congress: Environmental Stress and Horticulture Crops 618. 2002.
  • Surma, M. and P. Krajewski, Methodology of system approach to study drought tolerance in barley. Dissertations and Monographs, IPG PAS, 2014.
  • Tapia, G., et al., Study of nsLTPs in Lotus japonicus genome reveal a specific epidermal cell member (LjLTP10) regulated by drought stress in aerial organs with a putative role in cutin formation. Plant molecular biology, 2013. 82(4-5): p. 485-501.
  • Tsuchihira, A., et al., Effect of overexpression of radish plasma membrane aquaporins on water-use efficiency, photosynthesis and growth of Eucalyptus trees. Tree physiology, 2010. 30(3): p. 417-430.
  • Tyerman, S., et al., Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. Journal of Experimental Botany, 1999: p. 1055-1071.
  • Vallino, M., Greppi, D., Novero, M., Bonfante, P., ,Lupotto, E., Rice root colonisation by mycorrhizal and endophytic fungi in aerobic  Ann Appl Biol, 2009. 154: p. 195-204.
  • Vinod, M., et al., Candidate genes for drought tolerance and improved productivity in rice (Oryza sativa L.). Journal of biosciences, 2006. 31(1): p. 69-74.
  • Wen, N., Z. Chu, and S. Wang, Three types of defense-responsive genes are involved in resistance to bacterial blight and fungal blast diseases in rice. Molecular Genetics and Genomics, 2003. 269(3): p. 331-339.
  • Yamada, S., Katsuhara, M., Kelly, W.B., Michalowski, C.B. and Bonhert, H.J. , A family of transcripts encoding water channel proteins: tissue-specific expression in common ice plant. . Plant Cell, 1995. 7: p. 1129-1142.
  • Yang  J, Z.J., Liu  K,  Wang  Z,  Liu  L,  et  al, Involvement  of polyamines in the drought resistance of rice. J Exp Bot 2007. 58: p. 1545-1555.
  • Yooyongwech, S., S. Cha-um, and K. Supaibulwatana, Water relation and aquaporin genes (PIP1; 2 and PIP2; 1) expression at the reproductive stage of rice (Oryza sativa L. spp. indica) mutant subjected to water deficit stress. Plant Omics, 2013. 6(1): p. 79.
  • Zenoni, S., Fasoli, M., Tornielli, G. B., Dal Santo, S., Sanson, A., de Groot, P., Sordo, S., Citterio, S., Monti, F. and  Pezzotti., Overexpression of PhEXPA1 increases cell size, modifies cell wall polymer composition and affects the timing of axillary meristem development in Petunia hybrida. New Phytologist, 2011. 191(3): p. 662-677.
  • Zhang, S.-W., et al., Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3. 13 activation. Plant physiology, 2009. 151(4): p. 1889-1901.
  • Zhao, J., L.C. Davis, and R. Verpoorte, Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology advances, 2005. 23(4): p. 283-333.
  • Zhou, B., et al., The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Molecular plant-microbe interactions, 2006. 19(11): p. 1216-1228.
  • Zhou, S., et al., The involvement of expansins in response to water stress during leaf development in wheat. Journal of plant physiology, 2015. 183: p. 64-74.
  • Zimmermann, H.M., et al., Chemical composition of apoplastic transport barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.). Planta, 2000. 210(2): p. 302-311.