Abstract
The plant growth promoting rhizobacterium (PGPR) strain Bacillus amyloliquefaciens GB03, an important soil-borne bacterium, was shown to promote growth and abiotic stress tolerance in Arabidopsis thaliana as well as in some crop plants. This study aimed to evaluate the effects of GB03 on salt tolerance in Codonopsis pilosula, a traditional Chinese medicinal herb that is sensitive to salinity. Twenty-day-old seedlings of C. pilosula were either inoculated with GB03 or without it (as a control). At the same time, plants were treated with NaCl (0, 50, 100, or 150 mM) for 40 days. Growth parameters, photosynthetic indexes, malondialdehyde concentration, and leaf osmotic potential were measured after treatments. The result indicated that GB03 improved plant biomass of C. pilosula under salt conditions and improved the photosynthetic capacity by increasing net photosynthetic rate and stomatal conductance and decreasing intercellular CO2 concentration under both 0 and 50 mM NaCl. The bacterium strain also decreased leaf osmotic potential and peroxidation of membrane lipids that could help the plant adapt to saline environments. This study provides insights into the application of selected bacteria in the culture of important Chinese herbal plants under mild salinity.
Similar content being viewed by others
Abbreviations
- TBA:
-
Thiobarbituric acid
- MDA:
-
Malondialdehyde
- LB:
-
Luria broth
- PGPR:
-
Plant growth promoting rhizobacteria
- VOC:
-
Volatile organic compounds
- Ψs :
-
Osmotic potential
References
Aziz M, Nadipalli RK, Xitao X, Sun Y, Suowiec K, Zhang JL, Paré PW (2016) Augmenting sulfur metabolism and herbivore defense in Arabidopsis by bacterial volatile signaling. Front Plant Sci 7:458. doi:10.3389/fpls.2016.00458
Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced the salt and drought tolerance in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240. doi:10.1016/j.plantsci.2008.10.009
Choi SK, Jeong H, Kloepper JW., Ryu CM (2014) Genome sequence of Bacillus amyloliquefaciens GB03, an active ingredient of the first commercial biological control product. Genome Announc 2(5). doi:10.1128/genomeA.01092-14
Dardanelli MS, de Cordoba FJF, Espuny MR, Carvajal MAR, Díaz MES, Serrano AMG, Megías M (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721. doi:10.1016/j.soilbio.2008.06.016
Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plants Sci 19:371–379. doi:10.1016/j.tplants.2014.02.001
Freitas MA, Medeiros FH, Carvalho SP, Guilherme LR, Teixeira WD, Zhang H, Paré PW (2015) Augmenting iron accumulation in Cassava by the beneficial soil bacterium Bacillus subtilis (GBO3). Front Plant Sci. doi:10.3389/fpls.2015.00596
Han QQ, Lü XP, Bai JP, Qiao Y, Paré PW, Wang SM, Zhang JL, Wu YN, Pang XP, Xu WB, Wang ZL (2014) Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover. Front Plant Sci 5:1–74. doi:10.3389/fpls.2014.00525
Janz D, Polle A (2012) Harnessing salt for woody biomass production. Tree Physiol 32:1–3. doi:10.1093/treephys/tpr127
Kim EY, Kim JA, Jeon HJ, Kim S, Kim YH, Kim HY, Whang WK (2014) Chemical fingerprinting of Codonopsis pilosula and simultaneous analysis of its major components by HPLC-UV. Arch Pharm Res 37:1148–1158. doi:10.1007/s12272-014-0335-3
Lugtenberg B, Kamilova F (2013) Plant growth promoting rhizobacteria. Ann Rev Microbiol 86:541–556. doi:10.1146/annurev.micro.62.081307.162918
Luna C, Seffino LG, Arias C, Taleisnik E (2000) Oxidative stress indicators as selection tools for salt tolerance in Chloris gayana. Plant Breed 119:341–345. doi:10.1046/j.1439-0523.2000.00504.x
Ma Q, Yue LJ, Zhang JL, Wu G, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13. doi:10.1093/treephys/tpr098
Miao BH, Han XG, Zhang WH (2010) The ameliorative effects of silicon on soybean seedling grown in potassium-deficient medium. Ann Bot 105:967–973. doi:10.1093/aob/mcq063
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911
Niu SQ, Li HR, Paré PW, Aziz M, Wang SM, Shi HZ, Li J, Han QQ, Guo SQ, Li J, Guo Q, Ma Q, Zhang JL (2016) Induced growth promotion and higher salt tolerance in the halophyte grass Puccinellia tenuiflora by beneficial rhizobacteria. Plant Soil. doi:10.1007/s11104-015-2767-z
Paré PW, Farag MA, Krishnamachari V, Zhang H, Ryu CM, Kloepper JW (2005) Elicitors and priming agents initiate plant defense responses. Photosynth Res 85(2):149–159. doi:10.1007/s11120-005-1001-x
Paré PW, Zhang HM, Aziz M, Xie XT, Kim MS, Shen X, Zhang JL (2011) Beneficial 276 rhizobacteria induce plant growth: mapping signaling networks in Arabidopsis. Soil Biol 23:403–412. doi:10.1007/978-3-642-14512-4_15
Rahnama A, James RA, Poustini K, Munns R (2010) Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct Plant Biol 37:255–263. doi:10.1071/FP09148
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100(8):4927–4932. doi:10.1073/pnas.0730845100
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi:10.1104/pp.103.026583
Wang SC, Liang D, Li C, Hao YL, Ma FW, Shu HR (2012) Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. Plant Physiol Biochem 51:81–89. doi:10.1016/j.plaphy.2011.10.014
Wang YL, Zhao YY, Zuo YQ, Chang LP (2013) Characteristics and kinetics analysis of Codonopsis pilosula pyrolysis. J Therm Anal Calorim 111:1939–1945. doi:10.1007/s10973-011-2090-8
Xin T, Zhang FB, Jiang QY, Chen CH, Huang DY, Li YJ, Shen WX, Jin YH, Sui GJ (2012) The inhibitory effect of a polysaccharide from Codonopsis pilosula on tumor growth and metastasis in vitro. Int J Biol Macromol 51:788–793. doi:10.1016/j.ijbiomac.2012.07.019
Yazici I, Türkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57. doi:10.1016/j.envexpbot.2007.02.010
Zhang JL, Shi HZ (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22. doi:10.1071/CP13456
Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851. doi:10.1007/s00425-007-0530-2
Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Microbe In 21:737–744. doi:10.1094/MPMI-21-6-0737
Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273. doi:10.1111/j.1365-313X.2008.03593.x
Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. doi:10.1111/j.1365-313X.2009.03803.x
Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM (2010a) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe Int 23:1097–1104. doi:10.1094/MPMI-23-8-1097
Zhang JL, Flowers TJ, Wang SM (2010b) Mechanisms of sodium uptake by roots of higher plant. Plant Soil 326:45–60. doi:10.1007/s11104-009-0076-0
Zhang JL, Aziz M, Qiao Y, Han QQ, Li J, Wang YQ, Shen X, Wang SM, Paré PW (2014) Soil microbe Bacillus subtilis (GB03) induces biomass accumulation and salt tolerance with lower sodium accumulation in wheat. Crop Pasture Sci 65:423–427. doi:10.1071/CP13456
Zhu JK (2001) Plant salt tolerance. Trends Plants Sci 6:66–71. doi:10.1016/S1360-1385(00)01838-0
Acknowledgements
We thank Prof. Timothy J. Flowers from the University of Sussex, United Kingdom, for his critically reviewing this manuscript for the use of English. This work was financially supported by the National Basic Research Program of China (973 Program, Grant No. 2014CB138701), the National Natural Science Foundation of China (Grant No. 31222053 and 81260616), and the Fundamental Research Funds for the Central Universities (Grant No. lzujbky-2016-183 and lzujbky-2015-194).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Zwiazek.
Q.-Q. Han and Y.-N. Wu contributed equally to this work.
Rights and permissions
About this article
Cite this article
Han, QQ., Wu, YN., Gao, HJ. et al. Improved salt tolerance of medicinal plant Codonopsis pilosula by Bacillus amyloliquefaciens GB03. Acta Physiol Plant 39, 35 (2017). https://doi.org/10.1007/s11738-016-2325-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2325-1