Beneficial soil microbe promotes seed germination, plant growth and photosynthesis in herbal crop Codonopsis pilosula
Yong-Na Wu A , Yu-Lan Feng A , Paul W. Paré B , Ying-Long Chen C , Rui Xu D , Shan Wu E , Suo-Min Wang A , Qi Zhao A , Hui-Ru Li A , Yin-Quan Wang D and Jin-Lin Zhang A FA State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou 730000, P. R. China.
B Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, TX 79409-1061, USA.
C Institute of Agriculture, School of Earth and Environment, The University of Western Australia, 35 Stirling Highway Crawley, WA 6009, Australia.
D Departments of Nurse and Chinese Medicine, Gansu University of Traditional Chinese Medicine, Lanzhou, Gansu, 730000, P. R. China.
E Department of Biology, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P. R. China.
F Corresponding author. Email: jlzhang@lzu.edu.cn
Crop and Pasture Science 67(1) 91-98 https://doi.org/10.1071/CP15110
Submitted: 1 April 2015 Accepted: 17 August 2015 Published: 14 January 2016
Abstract
Bacillus subtilis strain GB03 enhances growth and photosynthesis in the model plant Arabidopsis thaliana and several crop plants. In the present study, the effects of seed soaking with GB03 suspension culture and its volatile organic compounds on seed germination of Codonopsis pilosula (Franch.) Nannf. were investigated, and soil-grown C. pilosula seedlings were assayed to measure growth and photosynthetic capacity after soil inoculation with GB03. Both seed soaking with GB03 suspension culture and the presence of volatile organic compounds enhanced seed germination, especially seed germination vigour. GB03 significantly improved shoot and root length, branching, plant biomass (whole plant fresh and dry weight), leaf area and chlorophyll content in C. pilosula seedlings after 20, 40 and 60 days of soil inoculation. GB03 significantly enhanced transpiration rate, stomatal conductance and net photosynthetic rate, but decreased intercellular CO2 concentration. This study provides insight for the application of selected bacteria to improve biomass in Chinese herbal crops.
Additional keywords: Bacillus subtilis, Codonopsis pilosula, growth promotion, photosynthesis, seed germination.
References
Ali B, Sabri AN, Ljung K, Hasnain S (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Letters in Applied Microbiology 48, 542–547.| Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFOhurc%3D&md5=c34c770191ad1c6b7ac663c9137db221CAS | 19220737PubMed |
Baldissera TC, Frak E, Carvalho PC, Louarn G (2013) Plant development controls leaf area expansion in alfalfa plants competing for light. Annals of Botany 113, 145–157.
| Plant development controls leaf area expansion in alfalfa plants competing for light.Crossref | GoogleScholarGoogle Scholar | 24201140PubMed |
Banchio E, Xie X, Zhang H, Paré PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. Journal of Agricultural and Food Chemistry 57, 653–657.
| Soil bacteria elevate essential oil accumulation and emissions in sweet basil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislansQ%3D%3D&md5=cf8f33956a33810b7bcb9d135da9c065CAS | 19128010PubMed |
de Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Molecular Plant 6, 242–245.
| Rhizosphere microbes as essential partners for plant stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWjur8%3D&md5=eca0b20ddfc4cabf7d1295ead190424eCAS | 23475999PubMed |
Earl AM, Losick R, Kolter R (2008) Ecology and genomics of Bacillus subtilis. Trends in Microbiology 16, 269–275.
| Ecology and genomics of Bacillus subtilis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntlSkurc%3D&md5=f0b1777f9d9d2650ae995cb1ee0d3230CAS | 18467096PubMed |
Gao S, Wu H, Wang W, Yang Y, Xie S, Xie Y, Gao X (2013) Efficient colonization and harpins mediated enhancement in growth and biocontrol of wilt disease in tomato by Bacillus subtilis. Letters in Applied Microbiology 57, 526–533.
| Efficient colonization and harpins mediated enhancement in growth and biocontrol of wilt disease in tomato by Bacillus subtilis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsl2htrnO&md5=52644e43645364139393ae7332e1606eCAS | 23937425PubMed |
Gorai M, El Aloui W, Yang X, Neffati M (2014) Toward understanding the ecological role of mucilage in seed germination of a desert shrub Henophyton deserti: interactive effects of temperature, salinity and osmotic stress. Plant and Soil 374, 727–738.
| Toward understanding the ecological role of mucilage in seed germination of a desert shrub Henophyton deserti: interactive effects of temperature, salinity and osmotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeqtbfE&md5=8f0b5235e3ad31aacaee4cf4bcef4733CAS |
Gutiérrez-Boem FH, Thomas GW (2001) Leaf area development in soybean as affected by phosphorus nutrition and water deficit. Journal of Plant Nutrition 24, 1711–1729.
| Leaf area development in soybean as affected by phosphorus nutrition and water deficit.Crossref | GoogleScholarGoogle Scholar |
Han DH, Zheng XF, Wang EJ, Jin L, Zhang Y, Dai L (2013) Effects of different salt-alkaline stress on seed germination and seedling physiological characteristics of Codonopsis pilosula. Journal of Chinese medicinal materials 36, 1039–1043. [in Chinese with English abstract]
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. Frontiers in Plant Science 5, 1–7.
| Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover.Crossref | GoogleScholarGoogle Scholar |
Harvey PR, Warren RA, Wakelin S (2009) Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere. Crop & Pasture Science 60, 144–151.
| Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlyrs7w%3D&md5=64b43844934b2e1f2144bae7a4974a3dCAS |
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. Archives of Pharmacal Research 37, 1148–1158.
| Chemical fingerprinting of Codonopsis pilosula and simultaneous analysis of its major components by HPLC-UV.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2htbk%3D&md5=8ac43fb3bd1853e49dcc33e484e83b3bCAS | 24497036PubMed |
Kloepper JW, Zablotowicz RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In ‘The rhizosphere and plant growth’. (Eds KL Keister, PB Cregan) pp. 315–326. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259–1266.
| Induced systemic resistance and promotion of plant growth by Bacillus spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWlurbL&md5=96f69697288e9f32b4a4ae2d069afa07CAS | 18944464PubMed |
Liu FL, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environmental and Experimental Botany 54, 33–40.
| Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1GmsLw%3D&md5=9b0114f438f67dfed098d96f1a08d0c4CAS |
Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiology 32, 4–13.
| Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVCmt7Y%3D&md5=600d43f138c2c59ade86d4ba0bb111c9CAS | 21979327PubMed |
MacDonald EM, Powell GK, Regier DA, Glass NL, Roberto F, Kosuge T (1986) Secretion of zeatin, ribosylzeatin, and ribosyl-1ʹʹ-methylzeatin by Pseudomonas savastanoi, plasmid-coded cytokinin biosynthesis. Plant Physiology 82, 742–747.
| Secretion of zeatin, ribosylzeatin, and ribosyl-1ʹʹ-methylzeatin by Pseudomonas savastanoi, plasmid-coded cytokinin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXis1Gi&md5=0f43bf4751be75143decb18c517d5a42CAS | 16665104PubMed |
Medeiros FH, Souza RM, Medeiros FC, Zhang H, Wheeler T, Payton P (2011) Transcriptional profiling in cotton associated with Bacillus subtilis (UFLA285) induced biotic-stress tolerance. Plant and Soil 347, 327–337.
| Transcriptional profiling in cotton associated with Bacillus subtilis (UFLA285) induced biotic-stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFyjsbnE&md5=82c05ca1fe7164786bc6e14737257c9fCAS |
Paré PW, Zhang HM, Aziz M, Xie XT, Kim MS, Shen X, Zhang JL (2011) Beneficial rhizobacteria induce plant growth: mapping signaling networks in Arabidopsis. In ‘Biocommunication in soil microorganisms’. Soil Biology Vol. 23. Ch. 15. (Ed. BG Witzany) pp. 403–412. (Springer: Dordrecht, The Netherlands)
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology 134, 1017–1026.
| Bacterial volatiles induce systemic resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1Sjt7w%3D&md5=74e9eaf87f6721ac898ae64518521377CAS | 14976231PubMed |
Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. International Journal of Molecular Sciences 14, 9803–9819.
| Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions.Crossref | GoogleScholarGoogle Scholar | 23698768PubMed |
Song J, Feng G, Tian CY, Zhang FS (2005) Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed germination stage. Annals of Botany 96, 399–405.
| Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed germination stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGltr3J&md5=9f47391c5c2db7c42d8f8711a2fd0d44CAS | 16002418PubMed |
Song J, Fan H, Zhao Y, Jia Y, Du X, Wang B (2008) Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquatic Botany 88, 331–337.
| Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtl2hsr0%3D&md5=f8cc1eaf2177ad4787cfc26426ede3a7CAS |
Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular Microbiology 56, 845–857.
| Bacillus subtilis antibiotics: structures, syntheses and specific functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlyns7Y%3D&md5=645d405c5db2ada7943f54aa25519f85CAS | 15853875PubMed |
Stein T, Borchert S, Conrad B, Feesche J, Hofemeister B, Hofemeister J, Entian KD (2002) Two different lantibiotic like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3. Journal of Bacteriology 184, 1703–1711.
| Two different lantibiotic like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFSht74%3D&md5=9b7610758b22e6364f082dbfc207958eCAS | 11872722PubMed |
Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biology & Biochemistry 31, 1847–1852.
| Cytokinin production by Paenibacillus polymyxa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslGjtLg%3D&md5=d166b13acb74368f866114dc3c83a4f3CAS |
Vicente MJ, Conesa E, Alvarez-Rogel J, Franco JA, Martinez-Sanchez JJ (2007) Effects of various salts on the germination of three perennial salt marsh species. Aquatic Botany 87, 167–170.
| Effects of various salts on the germination of three perennial salt marsh species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntF2rtbo%3D&md5=1da6de7b3ae29627a8aafa6d162dfdbfCAS |
Wang YL, Zhao YY, Zuo YQ, Chang LP (2013) Characteristics and kinetics analysis of Codonopsis pilosula pyrolysis. Journal of Thermal Analysis and Calorimetry 111, 1939–1945.
| Characteristics and kinetics analysis of Codonopsis pilosula pyrolysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivFejt7s%3D&md5=fe9d8c534a639f40250eb21b8cec381aCAS |
Xie X, Zhang H, Paré PW (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signaling & Behavior 4, 948–953.
| Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1ajurw%3D&md5=737bbd7c994675810bd4db9227f6ee86CAS |
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. International Journal of Biological Macromolecules 51, 788–793.
| The inhibitory effect of a polysaccharide from Codonopsis pilosula on tumor growth and metastasis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFClu7zP&md5=d9ba3daaf5b891d19542a9d3a6bfa38fCAS | 22829051PubMed |
Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226, 839–851.
| Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Cnt70%3D&md5=5191f36c5e6e2a07116b574d22ef7013CAS | 17497164PubMed |
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. Molecular Plant–Microbe Interactions 21, 737–744.
| Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1.Crossref | GoogleScholarGoogle Scholar | 18624638PubMed |
Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. The Plant Journal 56, 264–273.
| Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlChu7rI&md5=8b9db8dcd19ecf1df6dbec44e28c118eCAS | 18573192PubMed |
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. The Plant Journal 58, 568–577.
| A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVahur0%3D&md5=1b6c491677ff0350f88277396166e8feCAS | 19154225PubMed |
Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Pare PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Molecular Plant–Microbe Interactions 23, 1097–1104.
| Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFegtbc%3D&md5=ec31817b745af2c1afff48e45bdb1307CAS | 20615119PubMed |
Zhang N, Wu K, He X, Li SQ, Zhang ZH, Shen BH, Yang XM, Zhang RF, Huang QW, Shen QR (2011) A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant and Soil 344, 87–97.
| A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVCjt70%3D&md5=742d42dbdf9a0ca0180dfba611d32e35CAS |
Zhang JL, Aziz M, Qiao Y, Han QQ, Li J, Wang YQ, Shen X, Wang SM, Pare PW (2014) Soil microbe Bacillus subtilis (GB03) induces biomass accumulation and salt tolerance with lower sodium accumulation in wheat. Crop & Pasture Science 65, 423–427.
| Soil microbe Bacillus subtilis (GB03) induces biomass accumulation and salt tolerance with lower sodium accumulation in wheat.Crossref | GoogleScholarGoogle Scholar |