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http://dx.doi.org/10.1016/j.jgr.2020.01.001

Influence of the plant growth promoting Rhizobium panacihumi on aluminum resistance in Panax ginseng  

Kang, Jong-Pyo (Graduate School of Biotechnology, College of Life Sciences, Kyung Hee University)
Huo, Yue (Department of Oriental Medicinal Biotechnology, Kyung Hee University)
Yang, Dong-Uk (Department of Oriental Medicinal Biotechnology, Kyung Hee University)
Yang, Deok-Chun (Graduate School of Biotechnology, College of Life Sciences, Kyung Hee University)
Publication Information
Journal of Ginseng Research / v.45, no.3, 2021 , pp. 442-449 More about this Journal
Abstract
Background: Panax ginseng is an important crop in Asian countries given its pharmaceutical uses. It is usually harvested after 4-6 years of cultivation. However, various abiotic stresses have led to its quality reduction. One of the stress causes is high content of heavy metal in ginseng cultivation area. Plant growth-promoting rhizobacteria (PGPR) can play a role in healthy growth of plants. It has been considered as a new trend for supporting the growth of many crops in heavy metal occupied areas, such as Aluminum (Al). Methods: In vitro screening of the plant growth promoting activities of five tested strains were detected. Surface-disinfected 2-year-old ginseng seedlings were dipping in Rhizobium panacihumi DCY116T suspensions for 15 min and cultured in pots for investigating Al resistance of P. ginseng. The harvesting was carried out 10 days after Al treatment. We then examined H2O2, proline, total soluble sugar, and total phenolic contents. We also checked the expressions of related genes (PgCAT, PgAPX, and PgP5CS) of reactive oxygen species scavenging response and pyrroline-5-carboxylate synthetase by reverse transcription polymerase chain reaction (RT-PCR) method. Results: Among five tested strains isolated from ginseng-cultivated soil, R. panacihumi DCY116T was chosen as the potential PGPR candidate for further study. Ginseng seedlings treated with R. panacihumi DCY116T produced higher biomass, proline, total phenolic, total soluble sugar contents, and related gene expressions but decreased H2O2 level than nonbacterized Al-stressed seedlings. Conclusion: R. panacihumi DCY116T can be used as potential PGPR and "plant strengthener" for future cultivation of ginseng or other crops/plants that are grown in regions with heavy metal exposure.
Keywords
Aluminum resistance; Aluminum stress; Panax ginseng; Plant growth-promoting rhizobacteria; Rhizobium panacihumi;
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1 Ghnaya AB, Hourmant A, Cerantola S, Kervarec N, Cabon JY, Branchard M, Charles G. Influence of zinc on soluble carbohydrate and free amino acid levels in rapeseed plants regenerated in vitro in the presence of zinc. Plant Cell Tiss Org 2010;102:191-7.   DOI
2 Sukweenadhi J, Kim YJ, Choi ES, Koh SC, Lee SW, Kim YJ, Yang DC. Paenibacillus yonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol Res 2015;172:7-15.   DOI
3 Shokri D, Emtiazi G. Indole-3-acetic acid (IAA) production in symbiotic and non-symbiotic nitrogen-fixing bacteria and its optimization by Taguchi design. Curr Microbiol 2010;61:217-25.   DOI
4 Pikovskaya RI. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 1948;17:362-70.
5 Egler M, Grosse C, Grass G, Nies DH. Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. J Bacteriol 2005;187:2297-307.   DOI
6 Emamverdian A, Ding Y, Mokhberdoran F, Xie Y. Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120.   DOI
7 Kisnieriene V, Lapeikaite I. When chemistry meets biology: the case of aluminium-a review. Chemija 2015;26:148-58.
8 Bojorquez-Quintal E, Escalante-Magana C, Echevarria-Machado I, Martinez-Estevez M. Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci 2017;8:1767.   DOI
9 Dietz KJ, Baier M, Kramer U. Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Heavy metal stress in plants. Springer; 1999. p. 73-97.
10 Zengin FK, Munzuroglu O. Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 2005;47:157-64.
11 de Oliveira DM, de Lima ALA, Diniz NB, Santos C, da Silva SLF, Simoes A. Inoculation of plant-growth-promoting rhizobacteria in Myracrodruon urundeuva Allemao supports in tolerance to drought stress. J Plant Interact 2018;13:91-9.   DOI
12 Yang J, Kloepper JW, Ryu CM. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 2009;14:1-4.   DOI
13 Dimkpa C, Merten D, Svatos A, Buchel G, Kothe E. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 2009;107:1687-96.   DOI
14 Hayat R, Ali S, Amara U, Khalid R, Ahmed I. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 2010;60:579-98.   DOI
15 Schwyn B, Neilands J. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987;160:47-56.   DOI
16 Lane DJ. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Chichester: Wiley; 1991. p. 115-76.
17 Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991;173:697-703.   DOI
18 Glickmann E, Dessaux Y. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 1995;61:793-6.   DOI
19 Gupta K, Chatterjee C, Gupta B. Isolation and characterization of heavy metal tolerant Gram-positive bacteria with bioremedial properties from municipal waste rich soil of Kestopur canal (Kolkata), West Bengal, India. Biologia 2012;67:827-36.   DOI
20 Bashan Y, Holguin G, De-Bashan LE. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can J Microbiol 2004;50:521-77.   DOI
21 Dziewit L, Pyzik A, Szuplewska M, Matlakowska R, Mielnicki S, Wibberg D, Schluter A, Puhler A, Bartosik D. Diversity and role of plasmids in adaptation of bacteria inhabiting the Lubin copper mine in Poland, an environment rich in heavy metals. Front Microbiol 2015;6:152.   DOI
22 Liu J, Wang Q, Sun M, Zhu L, Yang M, Zhao Y. Selection of reference genes for quantitative real-time PCR normalization in Panax ginseng at different stages of growth and in different organs. PLoS One 2014;9:e112177.   DOI
23 Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A. Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 2008;35:412-26.   DOI
24 Irigoyen J, Einerich D, Sanche-Diaz M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 1992;84:55-60.   DOI
25 Mittal S, Meyer JM, Goel R. Isolation and characterization of aluminium and copper Resistant 'P' Solubilizing alkalophilic bacteria. Indian. J Biotechnol 2003;2:583-6.
26 Vardharajula S, Zulfikar-Ali S, Grover M, Reddy G, Bandi V. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 2011;6:1-14.   DOI
27 Kusunoki K, Nakano Y, Tanaka K, Sakata Y, Koyama H, Kobayashi Y. Transcriptomic variation among six Arabidopsis thaliana accessions identified several novel genes controlling aluminium tolerance. Plant Cell Environ 2017;40:249-63.   DOI
28 Alexieva V, Sergiev I, Mapelli S, Karanov E. The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 2001;24:1337-44.   DOI
29 Jin Y, Kim YJ, Jeon JN, Wang C, Min JW, Noh HY, Yang DC. Effect of white, red and black ginseng on physicochemical properties and ginsenosides. Plant Food Hum Nutr 2015;70:141-5.   DOI
30 Daspute AA, Sadhukhan A, Tokizawa M, Kobayashi Y, Panda SK, Koyama H. Transcriptional regulation of aluminum-tolerance genes in higher plants: clarifying the underlying molecular mechanisms. Front Plant Sci 2017;8:1358.   DOI
31 Hu M, Shi Z, Zhang Z, Zhang Y, Li H. Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regul 2012;68:177-88.   DOI
32 Ali A, Alqurainy F. Activities of antioxidants in plants under environmental stress. In: Motohashi N, editor. The lutein-prevention and treatment for diseases. India: Transworld Research Network; 2006. p. 187-256.
33 Hellmann H, Funck D, Rentsch D, Frommer WB. Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 2000;122:357-68.   DOI
34 Sukweenadhi J, Balusamy SR, Kim YJ, Lee CH, Kim YJ, Koh SC, Yang DC. A growth promoting bacteria, Paenibacillus yonginensis DCY84T enhanced salt stress tolerance by activating defense-related systems in Panax ginseng. Front Plant Sci 2018;9:813.   DOI
35 Ezaki B, Suzuki M, Motoda H, Kawamura M, Nakashima S, Matsumoto H. Mechanism of gene expression of Arabidopsis glutathione S-transferase, AtGST1, and AtGST11 in response to aluminum stress. Plant Physiol 2004;134:1672-82.   DOI
36 Wu L, Jin Y, Yin C, Bai L. Co-transformation of Panax major ginsenosides Rb1 and Rg1 to minor ginsenosides C-K and F1 by Cladosporium cladosporioides. J Ind Microbiol Biotechnol 2012;39:521-7.   DOI
37 Chen C, Wanduragala S, Becker DF, Dickman MB. Tomato QM-like protein protects Saccharomyces cerevisiae cells against oxidative stress by regulating intracellular proline levels. Appl Environ Microbiol 2006;72:4001-6.   DOI
38 Keum YS, Park KK, Lee JM, Chun KS, Park JH, Lee SK, Kwon H, Surh YJ. Antioxidant and anti-tumor promoting activities of the methanol extract of heat-processed ginseng. Cancer Lett 2000;150:41-8.   DOI
39 Kim YS, Lee MS, Yeom JH, Song JG, Lee IK, Yeo WH, Yun BS. Screening of antagonistic bacteria for biological control of ginseng root rot. Kor J Mycol 2012;40:44-8.   DOI
40 Farh MEA, Kim YJ, Sukweenadhi J, Singh P, Yang DC. Aluminium resistant, plant growth promoting bacteria induce overexpression of Aluminium stress related genes in Arabidopsis thaliana and increase the ginseng tolerance against Aluminium stress. Microbiol Res 2017;200:45-52.   DOI
41 Kloepper JW. Plant growth-promoting rhizobacteria on radishes. Proc. of the 4th Internet. Proceedings of the 4th International Conference on Plant Pathogenic Bacteria 1978;2:879-82.
42 Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G. Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 2007;76:1145-52.   DOI
43 Ahemad M, Kibret M. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 2014;26:1-20.   DOI
44 Sami F, Yusuf M, Faizan M, Faraz A, Hayat S. Role of sugars under abiotic stress. Plant Physiol Biochem 2016;109:54-61.   DOI
45 Kohler J, Hernandez JA, Caravaca F, Roldan A. Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 2008;35:141-51.   DOI
46 Oaikhena EE, Makaije DB, Denwe SD, Namadi MM, Haroun AA. Bioremediation potentials of heavy metal tolerant bacteria isolated from petroleum refinery effluent. Am J Environ Protect 2016;5:29-34.   DOI
47 Ashraf M, Foolad M. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 2007;59:206-16.   DOI