Journal of Microbiology and Biotechnology

  • 제21권9호
  • /
  • Pages.893-902
  • /
  • 2011
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Salinity Stress Resistance Offered by Endophytic Fungal Interaction Between Penicillium minioluteum LHL09 and Glycine max. L

  • Khan, Abdul Latif (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Hamayun, Muhammad (Department of Botany, Abdul Wali Khan University) ;
  • Ahmad, Nadeem (Department of Botany, Islamia College University) ;
  • Hussain, Javid (Kohat University of Science and Technology) ;
  • Kang, Sang-Mo (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Kim, Yoon-Ha (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Adnan, Muhammad (Kohat University of Science and Technology) ;
  • Tang, Dong-Sheng (Key Laboratory of Agri-biodiversity and Pest Management, Yunnan Agricultural University) ;
  • Waqas, Muhammad (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Radhakrishnan, Ramalingam (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Hwang, Young-Hyun (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Lee, In-Jung (School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University)
  • 투고 : 2011.03.07
  • 심사 : 2011.06.02
  • 발행 : 2011.09.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Endophytic fungi are little known for their role in gibberellins (GAs) synthesis and abiotic stress resistance in crop plants. We isolated 10 endophytes from the roots of field-grown soybean and screened their culture filtrates (CF) on the GAs biosynthesis mutant rice line - Waito-C. CF bioassay showed that endophyte GMH-1B significantly promoted the growth of Waito-C compared with controls. GMH-1B was identified as Penicillium minioluteum LHL09 on the basis of ITS regions rDNA sequence homology and phylogenetic analyses. GC/MS-SIM analysis of CF of P. minioluteum revealed the presence of bioactive $GA_4$ and $GA_7$. In endophyte-soybean plant interaction, P. minioluteum association significantly promoted growth characteristics (shoot length, shoot fresh and dry biomasses, chlorophyll content, and leaf area) and nitrogen assimilation, with and without sodium chloride (NaCl)-induced salinity (70 and 140 mM) stress, as compared with control. Field-emission scanning electron microcopy showed active colonization of endophyte with host plants before and after stress treatments. In response to salinity stress, low endogenous abscisic acid and high salicylic acid accumulation in endophyte-associated plants elucidated the stress mitigation by P. minioluteum. The endophytic fungal symbiosis of P. minioluteum also increased the daidzein and genistein contents in the soybean as compared with control plants, under salt stress. Thus, P. minioluteum ameliorated the adverse effects of abiotic salinity stress and rescued soybean plant growth by influencing biosynthesis of the plant's hormones and flavonoids.

키워드

참고문헌

  1. Ahmad, N., M. Hamayun, S. A. Khan, A. L. Khan, I. J. Lee, and D. H. Shin. 2010. Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J. Microbiol. Biotechnol. 20: 1744-1749.
  2. Alonso-Ramirez, A., D. Rodriguez, D. Reyes, J. A. Jimenez, G. Nicolas, M. Lopez-Climent, et al. 2009. Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol. 150: 1335-1344. https://doi.org/10.1104/pp.109.139352
  3. Aoki, T., T. Akasaki, and S. Ayabe. 2000. Flavonoids of leguminous plants: Structure, biological activity and biosynthesis. J. Plant Res. 113: 475-488. https://doi.org/10.1007/PL00013958
  4. Arnold, A. E., D. A. Henk, R. L. Eells, F. Lutzoni, and R. Vilgalys. 2007. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99: 185-206. https://doi.org/10.3852/mycologia.99.2.185
  5. Arnold, A. E. 2008. Endophytic fungi: hidden components of tropical community ecology, pp. 254-271. In W. F. Carson and S. A. Schnitzer (eds.). Tropical Forest Community Ecology. John Wiley & Sons, Oxford, UK.
  6. Bacon, C. W. 1993. Abiotic stress tolerances (moisture, nutrients) and photo-synthesis in endophyte-infected tall fescue. Agri. Ecosyst. Environ. 44: 123-141. https://doi.org/10.1016/0167-8809(93)90042-N
  7. Bomke, C. and B. Tudzynski. 2009. Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70: 1876-1893. https://doi.org/10.1016/j.phytochem.2009.05.020
  8. Catford, J. G., C. Staehelin, G. Larose, Y. Piche, and H. Vierheilig. 2006. Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285: 257-266. https://doi.org/10.1007/s11104-006-9012-8
  9. Cheplick, C. P. 2004. Recovery from drought stress in Lolium perenne (Poaceae): Are fungal endophytes detrimental? Am. J. Bot. 91: 1960-1968. https://doi.org/10.3732/ajb.91.12.1960
  10. Choi, W. Y., S. O. Rim, J. H. Lee, J. M. Lee, I. J. Lee, K. J. Cho, et al. 2005. Isolation of gibberellins-producing fungi from the root of several Sesamum indicum plants. J. Microbiol. Biotechnol. 15: 22-28.
  11. Dakora, F. D. and D. A. Phillips. 1996. Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Mol. Plant Physiol. 49: 1-20. https://doi.org/10.1006/pmpp.1996.0035
  12. Fateh, S. H. and W. F. Fagan. 2002. Fungal endophytes: Common host plant symbionts but uncommon mutualists. Integ. Comp. Biol. 42: 360-368. https://doi.org/10.1093/icb/42.2.360
  13. Franck, C., J. Lammertyn, and B. Nicolai. 2005. Metabolic profiling using GC-MS to study biochemical changes during long-term storage of pears. Proceedings of 5th International Postharvest Symposium, Mencarelli F, Tonutti P (eds.). Acta Hort. 682: 1991-1998.
  14. Grant, M. R. and J. D. G. Jones. 2009. Hormone (dis)harmony moulds plant health and disease. Science 324: 750. https://doi.org/10.1126/science.1173771
  15. Gamalero, E., G. Berta, and B. R. Glick. 2009. The use of microorganisms to facilitate the growth of plants in saline soils, pp. 1-22. In M. S. Khan, A. Zaidi, and J. Mussarat, (eds.). Microbial Strategies for Crop Improvement. Springer-Verlag, Berlin, Heidelberg.
  16. Ganley, R. J., S. J. Brunsfeld, and G. Newcombe. 2004. A community of unknown, endophytic fungi in western white pine. Proc. Nat. Acad. Sci. USA 101: 10107-10112. https://doi.org/10.1073/pnas.0401513101
  17. Gough, C., C. Galera, J. Vasse, G. Webster, E. C. Cocking, and J. Denarie. 1997. Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571 10. Mol. Plant Microb Interact. 5: 560-570.
  18. Hamayun, M., S. A. Khan, I. Iqbal, B. Ahmad, and I. J. Lee. 2010. Isolation of a gibberellin-producing fungus (Penicillium sp. MH7) and growth promotion of crown daisy (Chrysanthemum coronarium). J. Microbiol. Biotechnol. 20: 202-207.
  19. Hamayun, M., S. A. Khan, A. L. Khan, J. H. Shin, and I. J. Lee. 2010. Exogenous gibberellic acid reprograms soybean to higher growth, and salt stress tolerance. J. Agric. Food Chem. 58: 7226-7232. https://doi.org/10.1021/jf101221t
  20. Herrera-Medina, M. J., S. Steinkellner, H. Vierheilig, J. A. O. Bote, and J. M. G. Garrido. 2007. Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol. 175: 554-564. https://doi.org/10.1111/j.1469-8137.2007.02107.x
  21. Hoffmann-Benning, S. and H. Kende. 1992. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol. 99: 1156-1161. https://doi.org/10.1104/pp.99.3.1156
  22. Hussain, T. M., T. Chandrasekhar, M. Hazara, Z. Sultan, B. K. Saleh, and G. R. Gopal. 2008. Recent advances in salt stress biology - a review. Biotech. Mol. Biol. Rev. 3: 8-13.
  23. Hyde, K. D. and K. Soytong. 2008. The fungal endophyte dilemma. Fungal Div. 33: 163-173.
  24. Iqbal, M. and M. Ashraf. 2010. Gibberellic acid mediated induction of salt tolerance in wheat plants: Growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Env. Exp. Bot. DOI:10.1016/j.envexpbot.2010.06.002
  25. Kirakosyan, A., P. B. Kaufman, S. C. Chang, S. Warber, S. Bolling, and H. Vardapetyan. 2006. Regulation of isoavone production in hydroponically grown Pueraria montana (kudzu) by cork pieces, XAD-4, and methyl jasmonate. Plant Cell Rep. 25: 1387-1391. https://doi.org/10.1007/s00299-006-0198-2
  26. Khan, A. L., M. Hamayun, Y. H. Kim, S. M. Kang, and I. J. Lee. 2011. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol. Biochem. 49: 852-861. https://doi.org/10.1016/j.plaphy.2011.03.005
  27. Khan, A. L., M. Hamayun, Y. H. Kim, S. M. Kang, J. H. Lee, and I. J. Lee. 2011. Gibberellins-producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, plant growth and isoflavone biosynthesis in soybean under salt stress. Process Biochem. 46: 440-447. https://doi.org/10.1016/j.procbio.2010.09.013
  28. Khan, S. A., M. Hamayun, H. J. Yoon, H. Y. Kim, S. J. Suh, S. K. Hwang, et al. 2008. Plant growth promotion and Penicillium citrinum. BMC Microbiol. 8: 231-237. https://doi.org/10.1186/1471-2180-8-231
  29. Lee, I. J., K. Foster, and P. W. Morgan. 1998. Photoperiod control of gibberellin levels and flowering in sorghum. Plant Physiol. 116: 1003-1011. https://doi.org/10.1104/pp.116.3.1003
  30. Mauch-Mani, B. and F. Mauch. 2005. The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 8: 409-414. https://doi.org/10.1016/j.pbi.2005.05.015
  31. Munns, R. and M. Tester. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
  32. Murakami-Mizukami, Y., Y. Yamamoto, and S. Yamaki. 1991. Analyses of indole acetic acid and abscisic acid contents in nodules of soybean plants bearing VA mycorrhizas. Soil Sci. Plant Nutr. 37: 291-298. https://doi.org/10.1080/00380768.1991.10415039
  33. Oses, R., S. Valenzuela, J. Freer, E. Sanfuentes, and J. Rodriguez. 2008. Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Div. 33: 77-86.
  34. Phommalth, S., Y. Jeong, Y. Kim, K. H. Dhakal, and Y. Hwang. 2008. Effects of light treatment on isoflavone content of germinated soybean seeds. J. Agric. Food Chem. 56: 10123-10128. https://doi.org/10.1021/jf802118g
  35. Pozo, M. J. and C. Azcon-Aguilar. 2007. Unraveling mycorrhizainduced resistance. Curr. Opin. Plant Biol. 10: 393-398. https://doi.org/10.1016/j.pbi.2007.05.004
  36. Qi, Q. G., P. A. Rose, G. D. Abrams, D. C. Taylor, S. R. Abrams, and A. J. Cutler. 1998. Abscisic acid metabolism, 3-ketoacyl-coenzyme A synthase gene expression and very-long-chain monounsaturated fatty acid biosynthesis in Brassica napus embryos. Plant Physiol. 117: 979-987. https://doi.org/10.1104/pp.117.3.979
  37. Rajjou, L., M. Belghazi, R. Huguet, C. Robin, A. Moreau, C. Job, and D. Job. 2006. Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141: 910-923. https://doi.org/10.1104/pp.106.082057
  38. Richardson, A. E., J. Barea, A. M. Mcneill, and C. Prigent-Combaret. 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321: 305-339. https://doi.org/10.1007/s11104-009-9895-2
  39. Rijke, E. D., L. Aardenburg, J. V. Dijk, F. Ariese, W. H. O. Ernst, C. Gooijer, and U. A. Brinkman. 2005. Changed isoflavone levels in red clover (Trifolium pratense L.) leaves with disturbed root nodulation in response to waterlogging. J. Chem. Ecol. 31: 1285-1298. https://doi.org/10.1007/s10886-005-5286-1
  40. Ryals, J. A., U. H. Neuenschwander, M. G. Willits, A. Molina, H. Y. Steiner, and M. D. Hunt. 1996. Systemic acquired resistance. Plant Cell 8: 809-1819.
  41. Sawada, Y., M. Aoki, K. Nakaminami, W. Mitsuhashi, K. Tatematsu, T. S. Kushiro, et al. 2008. Phytochrome- and gibberellin-mediated regulation of abscisic acid metabolism during germination of photoblastic lettuce seeds. Plant Physiol. 146: 1386-1396. https://doi.org/10.1104/pp.107.115162
  42. Schulz, B. and C. Boyle. 2005. The endophytic continuum. Mycol. Res. 109: 661-686. https://doi.org/10.1017/S095375620500273X
  43. Seskar, M., V. Shulaev, and I. Raskin. 1998. Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol. 116: 387-392. https://doi.org/10.1104/pp.116.1.387
  44. Shaw, L. J., P. Morris, and J. E. Hooker. 2006. Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ. Microbiol. 8: 1867-1880. https://doi.org/10.1111/j.1462-2920.2006.01141.x
  45. Sharifi, M., M. Ghorbanli, and H. Ebrahimzadeh. 2007. Improved growth of salinity-stressed soybean after inoculation with pretreated mycorrhizal fungi. J. Plant Physiol. 164: 1144-1151. https://doi.org/10.1016/j.jplph.2006.06.016
  46. Subramanian, S., G. Stacey, and O. Yu. 2006. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J. 48: 261-273. https://doi.org/10.1111/j.1365-313X.2006.02874.x
  47. Taylor, D. L. and T. D. Bruns. 1999. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: Minimal overlap between the mature forest and resistant propagule communities. Microbial Ecol. 8: 1837-1850.
  48. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
  49. Volpin, H., D. A. Phillips, Y. Okon, and Y. A. Kapulnik. 1995. Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol. 108: 1449-1454. https://doi.org/10.1104/pp.108.4.1449
  50. Yu, O. and B. McGonigle. 2005. Metabolic engineering of isoavone biosynthesis. Adv. Agron. 86: 147-190.
  51. Wang, Y., S. Mopper, and K. H. Hasenstein. 2001. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. J. Chem. Ecol. 27: 327-342. https://doi.org/10.1023/A:1005632506230
  52. Waller, F., B. Achatz, H. Baltruschat, J. Fodor, K. Becker, M. Fischer, et al. 2005. The endophytic fungus Piriformis indica reprograms barley to salt-stress tolerance, disease resistance and higher yield. Proc. Natl. Acad. Sci. USA 102: 13386-13391. https://doi.org/10.1073/pnas.0504423102

피인용 문헌

  1. Fungal Diversity and Plant Growth Promotion of Endophytic Fungi from Six Halophytes in Suncheon Bay vol.22, pp.11, 2011, https://doi.org/10.4014/jmb.1205.05010
  2. 부안갯벌 생태계 복원을 위한 칠면초와 해홍나물의 내생진균류에 대한 유전학적 다양성 분석 vol.40, pp.4, 2012, https://doi.org/10.4014/kjmb.1207.07025
  3. 고창갯벌의 염생식물 뿌리로부터 분리된 내생진균의 다양성 vol.40, pp.2, 2011, https://doi.org/10.4489/kjm.2012.40.2.86
  4. 무안 염습지에 자생하는 염생식물(halophyte)의 뿌리로부터 분리된 내생진균(endophytic fungi)의 유전학적 다양성 vol.22, pp.7, 2012, https://doi.org/10.5352/jls.2012.22.7.970
  5. 칠면초의 뿌리로부터 분리된 Fusarium solani에 의해 생산된 지베렐린 A4 vol.22, pp.12, 2011, https://doi.org/10.5352/jls.2012.22.12.1718
  6. Cadophora malorum Cs‐8‐1 as a new fungal strain producing gibberellins isolated from Calystegia soldanella vol.53, pp.7, 2011, https://doi.org/10.1002/jobm.201200002
  7. IAA-Producing Penicillium sp. NICS01 Triggers Plant Growth and Suppresses Fusarium sp.-Induced Oxidative Stress in Sesame (Sesamum indicum L.) vol.23, pp.6, 2011, https://doi.org/10.4014/jmb.1209.09045
  8. Spermine Promotes Acclimation to Osmotic Stress by Modifying Antioxidant, Abscisic Acid, and Jasmonic Acid Signals in Soybean vol.32, pp.1, 2011, https://doi.org/10.1007/s00344-012-9274-8
  9. Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity vol.29, pp.11, 2011, https://doi.org/10.1007/s11274-013-1378-1
  10. Endophytes Aspergillus caespitosus LK12 and Phoma sp. LK13 of Moringa peregrina produce gibberellins and improve rice plant growth vol.9, pp.1, 2011, https://doi.org/10.1080/17429145.2014.917384
  11. Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease vol.9, pp.1, 2011, https://doi.org/10.1080/17429145.2014.930524
  12. 태안반도에 자생하는 해안식물 뿌리에서 분리한 내생진균의 다양성 분석 vol.42, pp.1, 2014, https://doi.org/10.4489/kjm.2014.42.1.79
  13. 태안반도에 자생하는 염생식물의 뿌리로부터 분리한 내생 진균의 다양성 vol.42, pp.4, 2011, https://doi.org/10.4489/kjm.2014.42.4.269
  14. A comparative study of phosphate solubilization and the host plant growth promotion ability of Fusarium verticillioides RK01 and Humicola sp. KNU01 under salt stress vol.65, pp.1, 2011, https://doi.org/10.1007/s13213-014-0894-z
  15. Endophytic fungi from the genus Colletotrichum are abundant in the Phaseolus vulgaris and have high genetic diversity vol.118, pp.2, 2011, https://doi.org/10.1111/jam.12696
  16. Endophytic fungi: resource for gibberellins and crop abiotic stress resistance vol.35, pp.1, 2011, https://doi.org/10.3109/07388551.2013.800018
  17. 동해안 자생식물로부터 분리된 내생균류의 식물생장촉진활성 및 동정 vol.51, pp.1, 2011, https://doi.org/10.7845/kjm.2015.5005
  18. Impact of a natural soil salinity gradient on fungal endophytes in wild barley (Hordeum maritimum With.) vol.32, pp.11, 2011, https://doi.org/10.1007/s11274-016-2142-0
  19. Fungal root endophytes of Quercus robur subjected to flooding vol.46, pp.1, 2011, https://doi.org/10.1111/efp.12212
  20. 독도 번행초에서 분리된 내생균류의 배양적 특성과 Aspergillus tubingensis YH103의 gibberellin A7의 생산 vol.52, pp.1, 2016, https://doi.org/10.7845/kjm.2016.5071
  21. Molecular characterization of endophytic fungi associated with the roots of Chenopodium quinoa inhabiting the Atacama Desert, Chile vol.11, pp.None, 2011, https://doi.org/10.1016/j.gdata.2016.12.015
  22. Molecular characterization of endophytic fungi associated with the roots of Chenopodium quinoa inhabiting the Atacama Desert, Chile vol.11, pp.None, 2011, https://doi.org/10.1016/j.gdata.2016.12.015
  23. Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress vol.219, pp.3, 2018, https://doi.org/10.1007/s11258-017-0791-1
  24. Fungal Diversity and Community Composition of Culturable Fungi in Stanhopea trigrina Cast Gibberellin Producers vol.9, pp.None, 2018, https://doi.org/10.3389/fmicb.2018.00612
  25. A Survey of Culturable Fungal Endophytes From Festuca rubra subsp. pruinosa , a Grass From Marine Cliffs, Reveals a Core Microbiome vol.9, pp.None, 2011, https://doi.org/10.3389/fmicb.2018.03321
  26. Endophytes from the crop wild relative Hordeum secalinum L. improve agronomic traits in unstressed and salt-stressed barley vol.4, pp.1, 2011, https://doi.org/10.1080/23311932.2018.1549195
  27. Paddy Chlorophyll Concentrations in Drought Stress Condition and Endophytic Fungi Application vol.156, pp.None, 2011, https://doi.org/10.1088/1755-1315/156/1/012040
  28. Integrated phytohormone production by the plant growth-promoting rhizobacterium Bacillus tequilensis SSB07 induced thermotolerance in soybean vol.14, pp.1, 2011, https://doi.org/10.1080/17429145.2019.1640294
  29. Synthesis of Biologically Active Gibberellins GA4 and GA7 by Microorganisms vol.81, pp.2, 2019, https://doi.org/10.15407/microbiolj81.02.090
  30. Benefits of a root fungal endophyte on physiological processes and growth of the vulnerable legume tree Prosopis chilensis (Fabaceae) vol.12, pp.2, 2019, https://doi.org/10.1093/jpe/rty019
  31. Tackling Salinity in Sustainable Agriculture-What Developing Countries May Learn from Approaches of the Developed World vol.11, pp.17, 2011, https://doi.org/10.3390/su11174558
  32. Agricultural and Other Biotechnological Applications Resulting from Trophic Plant-Endophyte Interactions vol.9, pp.12, 2011, https://doi.org/10.3390/agronomy9120779
  33. Soybean Fungal Endophytes Alternaria and Diaporthe spp. are Differentially Impacted by Fungicide Application vol.104, pp.1, 2020, https://doi.org/10.1094/pdis-05-19-1001-re
  34. Investigation of the mycelial morphology of Monascus and the expression of pigment biosynthetic genes in high-salt-stress fermentation vol.104, pp.6, 2020, https://doi.org/10.1007/s00253-020-10389-2
  35. Endophytic Penicillium species and their agricultural, biotechnological, and pharmaceutical applications vol.10, pp.3, 2011, https://doi.org/10.1007/s13205-020-2081-1
  36. Enhancement of Seawater Stress Tolerance in Barley by the Endophytic Fungus Aspergillus ochraceus vol.11, pp.7, 2011, https://doi.org/10.3390/metabo11070428
  37. Halotolerant-Koccuria rhizophila (14asp)-Induced Amendment of Salt Stress in Pea Plants by Limiting Na+ Uptake and Elevating Production of Antioxidants vol.11, pp.10, 2011, https://doi.org/10.3390/agronomy11101907