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http://dx.doi.org/10.4014/jmb.2105.05012

Isolation and Characterization of Cold-Adapted PGPB and Their Effect on Plant Growth Promotion  

Li, Mingyuan (College of Grassland Science, Gansu Agricultural University)
Wang, Jilian (College of Biologic and Geographic Sciences, Kashi University)
Yao, Tuo (College of Grassland Science, Gansu Agricultural University)
Wang, Zhenlong (College of Grassland Science, Gansu Agricultural University)
Zhang, Huirong (College of Grassland Science, Gansu Agricultural University)
Li, Changning (College of Grassland Science, Gansu Agricultural University)
Publication Information
Journal of Microbiology and Biotechnology / v.31, no.9, 2021 , pp. 1218-1230 More about this Journal
Abstract
Cold-adapted plant growth-promoting bacteria (PGPB) with multiple functions are an important resource for microbial fertilizers with low-temperature application. In this study, culturable cold-adapted PGPB strains with nitrogen fixation and phosphorus solubilization abilities were isolated. They were screened from root and rhizosphere of four dominant grass species in nondegraded alpine grasslands of the Qilian Mountains, China. Their other growth-promoting characteristics, including secretion of indole-3-acetic acid (IAA), production of siderophores and ACC deaminase, and antifungal activity, were further studied by qualitative and quantitative methods. In addition, whether the PGPB strains could still exert plant growth-promoting activity at 4℃ was verified. The results showed that 67 isolates could maintain one or more growth-promoting traits at 4℃, and these isolates were defined as cold-adapted PGPB. They were divided into 8 genera by 16S rRNA gene sequencing and phylogenetic analysis, of which Pseudomonas (64.2%) and Serratia (13.4%) were the common dominant genera, and a few specific genera varied among the plant species. A test-tube culture showed that inoculation of Elymus nutans seedlings with cold-adapted PGPB possessing different functional characteristics had a significant growth-promoting effect under controlled low-temperature conditions, including the development of the roots and aboveground parts. Pearson correlation analysis revealed that different growth-promoting characteristics made different contributions to the development of the roots and aboveground parts. These cold-adapted PGPB can be used as excellent strain resources suitable for the near-natural restoration of degraded alpine grasslands or agriculture stock production in cold areas.
Keywords
Plant growth-promoting bacteria (PGPB); screen; cold-adapted; the Qilian Mountains; alpine grasslands;
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1 Doebereiner J. 1994. Isolation and identification of aerobic nitrogen fixing bacteria, pp134-141. In Alef K (ed.), Methods in applied soil microbiology and biochemistry, Ed. Academic (eds.), Cambridge, UK.
2 Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7: 248-254.   DOI
3 Murphy J, Riley JP. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27: 31-36.   DOI
4 Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K, Nakai K, et al. 2012. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun. 3: 1926.
5 Wang M, Tachibana S, Murai Y, Li L, Lau SYL, Cao M, et al. 2016. Indole-3-acetic acid produced by Burkholderia heleia acts as a phenylacetic acid antagonist to disrupt tropolone biosynthesis in Burkholderia plantarii. Sci. Rep. 6: 22596.   DOI
6 Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56.   DOI
7 Vassilev N, Eichler-Lobermann B, Vassileva M. 2012. Stress-tolerant P-solubilizing microorganisms. Appl. Microbiol. Biotechnol. 95: 851-859.   DOI
8 Zhang W, Xue X, Peng F, You Q, Hao A. 2019. Meta-analysis of the effects of grassland degradation on plant and soil properties in the alpine meadows of the Qinghai-Tibetan Plateau. Glob. Ecol. Conserv. 20: e00774.   DOI
9 Gao QZ, Wan YF, Xu HM, Li Y, Jiangcun WZ, Borjigidai A. 2010. Alpine grassland degradation index and its response to recent climate variability in Northern Tibet, China. Quatern Int. 226: 143-150.   DOI
10 Liu J, Tang L, Gao H, Zhang M, Guo C. 2019. Enhancement of alfalfa yield and quality by plant growth-promoting rhizobacteria under saline-alkali conditions. J. Sci. Food Agr. 99: 281-289.   DOI
11 Onofre-Lemus J, Hernandez-Lucas I, Girard L, Caballero-Mellado J. 2009. ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in burkholderia species, and its growth-promoting effect on tomato plants. Appl. Environ. Microbiol. 75: 6581-6590.   DOI
12 Jin M, Zhao Q, Zhou Z, Zhu L, Zhang Z, Jiang L. 2020. Draft genome sequence of a potential organic phosphorus-degrading bacterium Brevibacterium frigoritolerans GD44, isolated from radioactive soil in Xinjiang, China. Curr. Microbiol. 77: 2896-2903.   DOI
13 Hussein KA, Joo JH. 2017. Stimulation, purification, and chemical characterization of siderophores produced by the rhizospheric bacterial strain Pseudomonas putida. Rhizosphere 4: 16-21.   DOI
14 Mishra J, Arora NK. 2018. Secondary metabolites of fluorescent pseudomonads in biocontrol of phytopathogens for sustainable agriculture. Appl. Soil Ecol. 125: 35-45.   DOI
15 Trivedi P, Sa T. 2008. Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production, and plant growth at lower temperatures. Curr. Microbiol. 56: 140-144.   DOI
16 Galkiewicz JP, Kellogg CA. 2008. Cross-kingdom amplification using bacteria-specific primers: complications for studies of coral microbial ecology. Appl. Environ. Microbiol. 74: 7828-7831.   DOI
17 Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N. 2015. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Front. Microbiol. 6: 00198.
18 Zhu Z, Zhang H, Leng J, Niu H, Chen X, Liu D, et al. 2020. Isolation and characterization of plant growth-promoting rhizobacteria and their effects on the growth of Medicago sativa L. under salinity conditions. Antonie Van Leeuwenhoek 113: 1263-1278.   DOI
19 Zhang C, Liu G, Song Z, Wang J, Guo L. 2018. Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands. Soil Biol. Biochem. 124: 47-58.   DOI
20 Wagg C, Schlaeppi K, Banerjee S, Kuramae E,van der Heijden MGA. 2019. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat. Commun. 10: 4841.   DOI
21 Wang Z, Tan W, Yang D, Zhang K, Zhao L, Xie Z, et al. 2021. Mitigation of soil salinization and alkalization by bacterium-induced inhibition of evaporation and salt crystallization. Sci. Total Environ. 755: 142511.   DOI
22 Mal B, Mahapatra P, Mohanty S. 2014. Effect of diazotrophs and chemical fertilizers on production and economics of okra (Abelmoschus esculentus, L.) cultivars. Am. J. Plant Sci. 5: 168-174.   DOI
23 Zhou DM, Huang XF, Chaparro JM, Badri DV, Manter DK, Vivanco JM, et al. 2016. Root and bacterial secretions regulate the interaction between plants and PGPR leading to distinct plant growth promotion effects. Plant Soil 401: 259-272.   DOI
24 Li H, Qiu Y, Yao T, Ma Y, Zhang H, Yang X. 2020. Effects of PGPR microbial inoculants on the growth and soil properties of Avena sativa , Medicago sativa , and Cucumis sativus seedlings. Soil Till Res. 199: 104577.   DOI
25 Gupta A, Gopal M, Thomas GV, Manikandan V, Gajewski J, Thomas G, et al. 2014. Whole genome sequencing and analysis of plant growth promoting bacteria isolated from the rhizosphere of plantation crops coconut, cocoa and arecanut. PLoS One 9: e104259.   DOI
26 Tiepo AN, Hertel MF, Rocha SS, Calzavara AK, Oliveira ALMD, Pimenta JA, et al. 2018. Enhanced drought tolerance in seedlings of Neotropical tree species inoculated with plant growth-promoting bacteria. Plant Physiol. Biochem. 130: 277-288.   DOI
27 Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, et al. 2018. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: A review. Microbiol. Res. 209: 21-32.   DOI
28 Hardy R, Holsten R, Jackson E, Burns R. 1968. The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol. 43: 1185-1207.   DOI
29 Wu H, Gu Q, Xie Y, Lou Z, Xue P, Fang L, et al. 2019. Cold-adapted Bacilli isolated from the Qinghai-Tibetan Plateau are able to promote plant growth in extreme environments. Environ. Microbiol. 21: 3505-3526.   DOI
30 Nautiyal CS. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170: 265-270.   DOI
31 Khan MS, Gao J, Zhang M, Chen X, Moe TS, Du Y, et al. 2020. Isolation and characterization of plant growth-promoting endophytic bacteria Bacillus stratosphericus LW-03 from Lilium wardii. 3 Biotech. 10: 305.
32 Etesami H, Beattie GA. 2018. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 9: 00148.   DOI
33 Chen Y, Xu T, Veresoglou SD, Hu H, Hao Z, Hu Y, et al. 2017. Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol. Biochem. 110: 12-21.   DOI
34 Turan M, Gulluce M, Sahin F. 2012. Effects of plant growth-promoting rhizobacteria on yield, growth, and some physiological characteristics of wheat and barley plants. Commun. Soil Sci. Plan. 43: 1658-1673.   DOI
35 Navarro-Noya YE, Hernandez-Mendoza E, Morales-Jimenez J, Jan-Roblero J, Martinez-Romero E, Hernandez-Rodriguez C. 2012. Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Appl. Soil Ecol. 62: 52-60.   DOI
36 Qin Y, Druzhinina IS, Pan X, Yuan Z. 2016. Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol. Adv. 34: 1245-1259.   DOI
37 Gao J, Luo Y, Wei Y, Huang Y, Zhang H, He W, et al. 2019. Screening of plant growth promoting bacteria (PGPB) from rhizosphere and bulk soil of Caragana microphylla in different habitats and their effects on the growth of Arabidopsis seedlings. Biotechnol. Biotechnol. Equip. 33: 921-930.   DOI
38 Berg M, Koskella B. 2018. Nutrient-and dose-dependent microbiome-mediated protection against a plant pathogen. Curr. Biol. 28: 2487-2492.   DOI
39 Sarkar J, Chakraborty B, Chakraborty U. 2018. Plant growth promoting rhizobacteria protect wheat plants against temperature stress through antioxidant signalling and reducing chloroplast and membrane injury. J. Plant Growth Regul. 37: 1396-1412.   DOI
40 Vries FTd, Griffiths RI, Knight CG, Nicolitch O, Williams A. 2020. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368: 270-274.   DOI
41 Fierer N. 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15: 579-590.   DOI
42 Yadav AN, Sachan SG, Verma P, Saxena AK. 2016. Bioprospecting of plant growth promoting psychrotrophic Bacilli from the cold desert of north western Indian Himalayas. Indian J. Exp. Biol. 54: 142-150.
43 Pandey A, Yarzabal LA. 2019. Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl. Microbiol. Biotechnol. 103: 643-657.   DOI
44 Gomez-Godinez LJ, Fernandez-Valverde SL, Romero JCM, Martinez-Romero E. 2019. Metatranscriptomics and nitrogen fixation from the rhizoplane of maize plantlets inoculated with a group of PGPRs. Syst. Appl. Microbiol. 42: 517-525.   DOI
45 Molina-Romero D, Baez A, Quintero-Hernandez V, Castaneda M, Fuentes-Ramirez LE, Bustillos MdR, et al. 2017. Compatible bacterial mixture, tolerant to desiccation, improves maize plant growth. PLos One 12: e0187913.   DOI
46 Chrastil J. 1976. Colorimetric estimation of indole-3-acetic acid. Anal. Biochem. 72: 134-138.   DOI
47 Penrose DM, Glick BR. 2003. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plantarum. 118: 10-15.   DOI
48 Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874.   DOI
49 Chauhan A, Guleria S, Balgir PP, Walia A, Mahajan R, Mehta P, et al. 2017. Tricalcium phosphate solubilization and nitrogen fixation by newly isolated Aneurinibacillus aneurinilyticus CKMV1 from rhizosphere of Valeriana jatamansi and its growth promotional effect. Braz. J. Microbiol. 48: 294-304.   DOI
50 Agarwal P, Singh PC, Chaudhry V, Shirke PA, Chakrabarty D, Farooqui A, et al. 2019. PGPR-induced OsASR6 improves plant growth and yield by altering root auxin sensitivity and the xylem structure in transgenic Arabidopsis thaliana. J. Plant Physiol. 240: 153010.   DOI
51 Defez R, Andreozzi A, Romano S, Pocsfalvi G, Fiume I, Esposito R, et al. 2019. Bacterial IAA-delivery into medicago root nodules triggers a balanced stimulation of C and N metabolism leading to a biomass increase. Microorganisms 7: 403.   DOI
52 Shahid M, Hameed S, Zafar M, Tahir M, Ijaz M, Tariq M, et al. 2019. Enterobacter sp. strain Fs-11 adapted to diverse ecological conditions and promoted sunflower achene yield, nutrient uptake, and oil contents. Braz. J. Microbiol. 50: 459-469.   DOI
53 Li H, Singh RK, Singh P, Song Q, Xing Y, Yang L, et al. 2017. Genetic diversity of nitrogen-fixing and plant growth promoting Pseudomonas species isolated from sugarcane rhizosphere. Front. Microbiol. 8: 01268.   DOI
54 Zaheer A, Malik A, Sher A, Qaisrani MM, Mehmood A, Khan SU, et al. 2019. Isolation, characterization, and effect of phosphate-zinc-solubilizing bacterial strains on chickpea (Cicer arietinum L.) growth. Saudi J. Biol. Sci. 26: 1061-1067.   DOI
55 Etesami H, Maheshwari DK. 2018. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 156: 225-246.   DOI
56 Marilyn ST, Felipe RP, Jonathan ML, Gutierrez AY, Christian V, Edwin CR, et al. 2021. Genomic and phenotypic analysis of rock phosphate-solubilizing rhizobacteria. Rhizosphere 17: 100290.   DOI