<i>Pseudomonas</i> spp. in biological plant protection and growth promotion

Ewelina Nerek; Barbara Sokołowska; Ewelina Nerek; Barbara Sokołowska

doi:10.3934/environsci.2022029

AIMS Environmental Science

2022, Volume 9, Issue 4: 493-504. doi: 10.3934/environsci.2022029

Previous Article Next Article

Review

Pseudomonas spp. in biological plant protection and growth promotion

Ewelina Nerek ^,,
Barbara Sokołowska

Department of Microbiology, Prof. Wacław Dąbrowski Institute of Agricultural and Food Biotechnology-State Research Institute, Warsaw, Poland

Received: 25 April 2022 Revised: 21 June 2022 Accepted: 01 July 2022 Published: 08 August 2022

Nowadays in worldwide agriculture, sustainable strategies are implemented to reduce negative effects on ecosystems created by conventional practice, mainly environmental pollution caused by intensive use of fertilizers and chemical plant protection products. Bacteria from the genus Pseudomonas can be considered biocontrol and plant growth-promoting agents due to their various plant beneficial traits e.g., siderophores production, phytohormones synthesis, antagonism against phytopathogenic fungi. This is a reason for increasing researchers' interest in improving of existing or elaborating new technologies that enable the effective application of these bacteria in agriculture. Pseudomonads are non-sporulating bacteria and it is a major constraint for creating bioformulation for commercial use with a sufficiently high stable number of viable cells during shelf-life. Therefore, scientists are making efforts to improve techniques of bioformulations to enable large-scale production and use of pseudomonads under field conditions. The aim of this review is to describe traits of Pseudomonas spp. which are useful in plant protection and growth-promotion and to highlight examined techniques for preparing bioformulations containing pseudomonads with sufficiently long shelf life.
- Pseudomonas,
- plant growth promotion,
- biocontrol,
- bioformulation
Citation: Ewelina Nerek, Barbara Sokołowska. Pseudomonas spp. in biological plant protection and growth promotion[J]. AIMS Environmental Science, 2022, 9(4): 493-504. doi: 10.3934/environsci.2022029

Related Papers:

Abstract

Nowadays in worldwide agriculture, sustainable strategies are implemented to reduce negative effects on ecosystems created by conventional practice, mainly environmental pollution caused by intensive use of fertilizers and chemical plant protection products. Bacteria from the genus Pseudomonas can be considered biocontrol and plant growth-promoting agents due to their various plant beneficial traits e.g., siderophores production, phytohormones synthesis, antagonism against phytopathogenic fungi. This is a reason for increasing researchers' interest in improving of existing or elaborating new technologies that enable the effective application of these bacteria in agriculture. Pseudomonads are non-sporulating bacteria and it is a major constraint for creating bioformulation for commercial use with a sufficiently high stable number of viable cells during shelf-life. Therefore, scientists are making efforts to improve techniques of bioformulations to enable large-scale production and use of pseudomonads under field conditions. The aim of this review is to describe traits of Pseudomonas spp. which are useful in plant protection and growth-promotion and to highlight examined techniques for preparing bioformulations containing pseudomonads with sufficiently long shelf life.

References

[1]	Warra AA, Prasad MNV (2020) African perspective of chemical usage in agriculture and horticulture-their impact on human health and environment, In: Prasad MNV (Ed.), Agrochemicals detection, treatment and remediation, Kidlington, Oxford: Butterworth Heinemann, 401–436. https://doi.org/10.1016/C2018-0-02947-3
[2]	Mishra J, Arora NK (2016) Bioformulations for plant growth promotion and combating phytopathogens: A sustainable approach, In: Arora N, Mehnaz S, Balestrini R (Eds.), Bioformulations for sustainable agriculture, New Delhi: Springer, 251–267. https://doi.org/10.1007/978-81-322-2779-3_1
[3]	Sanborn M, Kerr KJ, Sanin LH, et al. (2007) Non-cancer health effects of pesticides: Systematic review and implications for family doctors. Can Fam Physician 53: 1712–1720.
[4]	Mahmood I, Imadi SR, Shazadi K, et al. (2016) Effects of pesticides on environment, In: Hakeem K, Akhtar M, Abdullah S (Eds.), Plant, soil and microbes, Cham: Springer, 253–269. https://doi.org/10.1007/978-3-319-27455-3_13
[5]	Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356: 260–264. https://doi.org/10.1126/science.aal2011 doi: 10.1126/science.aal2011
[6]	Akhtar S, Bashir S, Khan S, et al. (2020) Integrated usage of synthetic and bio-fertilizers: An environment friendly approach to improve the productivity of sorghum. Cereal Res Commun 48: 247–253. https://doi.org/10.1007/s42976-020-00029-w doi: 10.1007/s42976-020-00029-w
[7]	O'Brien PA (2017) Biological control of plant diseases. Australas Plant Pathol 46: 293–304. https://doi.org/10.1007/s13313-017-0481-4 doi: 10.1007/s13313-017-0481-4
[8]	Kumar A, Verma H, Singh VK, et al. (2017) Role of Pseudomonas sp. in sustainable agriculture and disease management, In: Meena V, Mishra P, Bisht J, et al. (Eds.), Agriculturally important microbes for sustainable agriculture, Singapore: Springer, 195–216. https://doi.org/10.1007/978-981-10-5343-6_7
[9]	Brenner DJ, Krieg NR, Garrity GM, et al. (2005) Bergey's manual of systematic bacteriology, Volume two: The Proteobacteria, New York: Springer, 322–330.
[10]	Colombo C, Palumbo G, He JZ, et al. (2014) Review on iron availability in soil: Interaction of Fe minerals, plants and microbes. J Soil Sediments 14: 538–548. https://doi.org/10.1007/s11368-013-0814-z doi: 10.1007/s11368-013-0814-z
[11]	Neilands, JB (1993) Siderophores. Arch Biochem Biophys 302: 1–3. https://doi.org/10.1006/abbi.1993.1172 doi: 10.1006/abbi.1993.1172
[12]	Radzki W, Gutierrez Manero FJ, Algar E, et al. (2013) Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Anton van Leeuw 104: 321–330. https://doi.org/10.1007/s10482-013-9954-9 doi: 10.1007/s10482-013-9954-9
[13]	Meziane H, Van der Sluis I, Van Loon LC, et al. (2005) Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol Plant Pathol 6: 177–185. https://doi.org/10.1111/j.1364-3703.2005.00276.x doi: 10.1111/j.1364-3703.2005.00276.x
[14]	Caulier S, Gillis A, Colau G, et al. (2018) Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Front Microbiol 9: 143. https://doi.org/10.3389/fmicb.2018.00143 doi: 10.3389/fmicb.2018.00143
[15]	Cornelis P, Matthijs S (2007) Pseudomonas siderophores and their biological significance, In: Varma A, Chincholkar SB (Eds.), Microbial siderophores. Soil biology, Berlin, Heidelberg: Springer, 193–203. https://doi.org/10.1007/978-3-540-71160-5_9
[16]	Raio A, Puopolo G (2021) Pseudomonas chlororaphis metabolites as biocontrol promoters of plant health and improved crop yield. World J Microbiol Biotechnol 37: 99. https://doi.org/10.1007/s11274-021-03063-w doi: 10.1007/s11274-021-03063-w
[17]	Munmun N, Selin C, Brawerman G, et al. (2017) Hydrogen cyanide, which contributes to Pseudomonas chlororaphis strain PA23 biocontrol, is upregulated in the presence of glycine. Biol Control 108: 47–54. https://doi.org/10.1016/j.biocontrol.2017.02.008 doi: 10.1016/j.biocontrol.2017.02.008
[18]	Biessy A, Novinscak A, St-Onge R, et al. (2021) Inhibition of three potato pathogens by phenazine-producing Pseudomonas spp. is associated with multiple biocontrol-related traits. mSphere 6: e00427-21. https://doi.org/10.1128/mSphere.00427-21
[19]	Zhang QX, Kong XW, Li SY et al. (2020) Antibiotics of Pseudomonas protegens FD6 are essential for biocontrol activity. Australasian Plant Pathol 49: 307–317. https://doi.org/10.1007/s13313-020-00696-7 doi: 10.1007/s13313-020-00696-7
[20]	Wu LQ, Shang HZ, Wang Q, et al. (2016) Isolation and characterization of antagonistic endophytes from Dendrobium candidum Wall ex Lindl., and the biofertilizing potential of a novel Pseudomonas saponiphila strain. Appl Soil Ecol 105: 101–108. https://doi.org/10.1016/j.apsoil.2016.04.008 doi: 10.1016/j.apsoil.2016.04.008
[21]	Nandi M, Selin C, Brawerman G, et al. (2017) Hydrogen cyanide, which contributes to Pseudomonas chlororaphis strain PA23 biocontrol, is upregulated in the presence of glycine. Biol Control 108: 47–54. https://doi.org/10.1016/j.biocontrol.2017.02.008 doi: 10.1016/j.biocontrol.2017.02.008
[22]	Sun JM, Irzykowski W, Jedryczka M, et al. (2005) Analysis of the genetic structure of Sclerotinia sclerotiorum (Lib.) de Bary populations from different regions and host plants by random amplified polymorphic DNA markers. J Integr Plant Biol 47: 385–395. https://doi.org/10.1111/j.1744-7909.2005.00077.x doi: 10.1111/j.1744-7909.2005.00077.x
[23]	Siddiqui IA, Shaukat SS, Sheikh IH, et al. (2006) Role of cyanide production by Pseudomonas fluorescens CHA0 in the suppression of root-knot nematode, Meloidogyne javanica in tomato. World J Microbiol Biotechnol 22: 641–650. https://doi.org/10.1007/s11274-005-9084-2 doi: 10.1007/s11274-005-9084-2
[24]	Wang CW, Wang Y, Wang L, et al. (2021) Biocontrol potential of volatile organic compounds from Pseudomonas chlororaphis ZL3 against postharvest gray mold caused by Botrytis cinerea on chinese cherry. Biol Control 159: 104613. https://doi.org/10.1016/j.biocontrol.2021.104613 doi: 10.1016/j.biocontrol.2021.104613
[25]	Ossowicki A, Jafra S, Garbeva P (2017) The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482. PLoS ONE 12: e0174362. https://doi.org/10.1371/journal.pone.0174362
[26]	Hernández-León R, Rojas-Solís D, Contreras-Pérez M, et al. (2015) Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Control 81: 83–92. https://doi.org/10.1016/j.biocontrol.2014.11.011 doi: 10.1016/j.biocontrol.2014.11.011
[27]	Wang ZR, Zhong T, Chen KW, et al. (2021) Antifungal activity of volatile organic compounds produced by Pseudomonas fluorescens ZX and potential biocontrol of blue mold decay on postharvest citrus. Food Control 120: 107499. https://doi.org/10.1016/j.foodcont.2020.107499 doi: 10.1016/j.foodcont.2020.107499
[28]	Ahmad F, Ahmad I, Khan MS (2008) Screening of free living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163: 173–181. https://doi.org/10.1016/j.micres.2006.04.001 doi: 10.1016/j.micres.2006.04.001
[29]	Liu XX, Jiang XX, He XY, et al. (2019) Phosphate-solubilizing Pseudomonas sp. strain P34-L promotes wheat growth by colonizing the wheat rhizosphere and improving the wheat root system and soil phosphorus nutritional status. J Plant Growth Regul 38: 1314–1324. https://doi.org/10.1007/s00344-019-09935-8 doi: 10.1007/s00344-019-09935-8
[30]	Saha M, Maurya BR, Singh Meena V, et al. (2016) Identification and characterization of potassium solubilizing bacteria (KSB) from Indo-Gangetic Plains of India. Biocatal Agric Biotechnol 7: 202–209. https://doi.org/10.1016/j.bcab.2016.06.007 doi: 10.1016/j.bcab.2016.06.007
[31]	Saravanan VS, Subramoniam SR, Raj SA (2003) Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates. Braz J Microbiol 34: 121–125. https://doi.org/10.1590/S1517-83822004000100020 doi: 10.1590/S1517-83822004000100020
[32]	Iqbal A, Hasnain S (2013) Auxin producing Pseudomonas strains: biological candidates to modulate the growth of Triticum aestivum beneficially. Am J Plant Sci 4: 1693–1700. https://doi.org/10.4236/ajps.2013.49206 doi: 10.4236/ajps.2013.49206
[33]	Kang SM, Radhakrishnan R, Latif Khan A, et al. (2014) Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84: 115–124. https://doi.org/10.1016/j.plaphy.2014.09.001 doi: 10.1016/j.plaphy.2014.09.001
[34]	Grosskinsky DK, Tafner R, Moreno MV, et al. (2016) Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci Rep 6: 23310. https://doi.org/10.1038/srep23310 doi: 10.1038/srep23310
[35]	Nagarajkumar M, Bhaskaran R, Velazhahan R (2004) Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 159: 73–81. https://doi.org/10.1016/j.micres.2004.01.005 doi: 10.1016/j.micres.2004.01.005
[36]	Saravanakumar D, Samiyappan R (2006) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102: 1283–1292. https://doi.org/10.1111/j.1365-2672.2006.03179.x doi: 10.1111/j.1365-2672.2006.03179.x
[37]	Ali SZ, Sandhya V, Venkateswar RL (2014) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann Microbiol 64: 493–502. https://doi.org/10.1007/s13213-013-0680-3 doi: 10.1007/s13213-013-0680-3
[38]	Velazhahan R, Samiyappan R, Vidhyasekaran P (1999) Relationship between antagonistic activities of Pseudomonas fluorescens isolates against Rhizoctonia solani and their production of lytic enzymes. J Plant Dis Prot 106: 244–250.
[39]	Ghadamgahi F, Tarighi S, Taheri P et al. (2022) Plant growth-promoting activity of pseudomonas aeruginosa FG106 and its ability to act as a biocontrol agent against potato, tomato and taro pathogens. Biology 11: 140. https://doi.org/10.3390/biology11010140 doi: 10.3390/biology11010140
[40]	Jain R, Pandey A (2016) A phenazine-1-carboxylic acid producing polyextremophilic Pseudomonas chlororaphis (MCC2693) strain, isolated from mountain ecosystem, possesses biocontrol and plant growth promotion abilities. Microbiol Res 190: 63–71. https://doi.org/10.1016/j.micres.2016.04.017 doi: 10.1016/j.micres.2016.04.017
[41]	Bjelić D, Marinković J, Tintor B et al. (2018) Antifungal and plant growth promoting activities of indigenous rhizobacteria isolated from maize (Zea mays L.) rhizosphere. Commun Soil Sci Plant Anal 49: 88–98. https://doi.org/10.1080/00103624.2017.1421650 doi: 10.1080/00103624.2017.1421650
[42]	Kravchenko LV, Makarova NM, Azarova TS, et al. (2002) Isolation and characterization of plant growth-promoting rhizobacteria with high antiphytopathogenic activity and root-colonizing ability. Microbiology 71: 444–448. https://doi.org/10.1023/A:1019849711782 doi: 10.1023/A:1019849711782
[43]	Siddiqui IA, Haas D, Heeb S (2005) Extracellular protease of Pseudomonas fluorescens CHA0, a biocontrol factor with activity against the root-knot nematode Meloidogyne incognita. Appl Environ Microbiol 71: 5646–5649. https://doi.org/10.1128/AEM.71.9.5646-5649.2005 doi: 10.1128/AEM.71.9.5646-5649.2005
[44]	Novinscak A, Filion M (2020) Long term comparison of talc- and peat-based phytobeneficial Pseudomonas fluorescens and Pseudomonas synxantha bioformulations for promoting plant growth. Front Sustain Food Syst 4: 602911. https://doi.org/10.3389/fsufs.2020.602911 doi: 10.3389/fsufs.2020.602911
[45]	Keswani C, Bisen K, Singh V, et al. (2016) Formulation technology of biocontrol agents: Present status and future prospects, In: Arora NK, Mehnaz S, Balestrini R (Eds.), Bioformulations for sustainable agriculture, New Delhi: Springer, 251–267. https://doi.org/10.1007/978-81-322-2779-3_2
[46]	Bisutti IL, Hirt K, Stephan D (2015) Influence of different growth conditions on the survival and the efficacy of freeze-dried Pseudomonas fluorescens strain Pf153. Biocontrol Sci Technol 25: 1269–1284. https://doi.org/10.1080/09583157.2015.1044498 doi: 10.1080/09583157.2015.1044498
[47]	Mputu Kanyinda JN, Pierart C, Weekers F, et al. (2012) Effects of glycerol on Pseudomonas fluorescens BTP1 freeze-dried. Int J Biotech Biochem 8: 245–258.
[48]	Stephan D, Da Silva AM, Bisutti IL (2016) Optimization of freeze-drying process for the biocontrol agent Pseudomonas spp. and its influence on viability, storability and efficacy. Biol Control 94: 74–81. https://doi.org/10.1016/j.biocontrol.2015.12.004 doi: 10.1016/j.biocontrol.2015.12.004
[49]	Cabrefiga J, Frances J, Montesinos E, et al. (2014) Improvement of a dry formulation of Pseudomonas fluorescens EPS62e for fire blight disease biocontrol by combination of culture osmoadaptation with a freeze-drying lyoprotectant. J Appl Microbiol 117: 1122–1131. https://doi.org/10.1111/jam.12582 doi: 10.1111/jam.12582
[50]	Wu PY, Wang ZP, Zhu QY, et al. (2021) Stress preadaptation and overexpression of rpoS and hfq genes increase stress resistance of Pseudomonas fluorescens ATCC13525. Microbiol Res 250: 126084. https://doi.org/10.1016/j.micres.2021.126804 doi: 10.1016/j.micres.2021.126804
[51]	Bisutti IL, Stephan D (2019) Influence of fermentation temperature and duration on survival and biocontrol efficacy of Pseudomonas fluorescens Pf153 freeze-dried cells. J Appl Microbiol 128: 232–241. https://doi.org/10.1111/jam.14458 doi: 10.1111/jam.14458
[52]	Mputu Kanyinda JN, Pierart C, Weekers, F, et al. (2012) Impact of protective compounds on the viability, physiological state and lipid degradation of freeze-dried Pseudomonas fluorescens BTP1 during storage. Int J Biotech Biochem 8: 17–26.
[53]	Mputu Kanyinda JN, Thonart P (2013) Optimisation of production, freeze-drying and storage of Pseudomonas fluorescens BTP1. Int J Microbiol Res 5: 370–373.
[54]	Palmfeldt J, Radstrom P, Hahn-Hagerdal B (2003) Optimisation of initial cell concentration enhances freeze-drying tolerance of Pseudomonas chlororaphis. Cryobiology 47: 21–29. https://doi.org/10.1016/S0011-2240(03)00065-8 doi: 10.1016/S0011-2240(03)00065-8
[55]	Chavez BE, Ledeboer AM (2007) Drying of probiotics: Optimization of formulation and process to enhance storage survival. Dry Technol 25: 1193–1201. https://doi.org/10.1080/07373930701438576 doi: 10.1080/07373930701438576
[56]	Manikandan R, Saravanakumar D, Rajendran L, et al. (2010) Standardization of liquid formulation of Pseudomonas fluorescens Pf1 for its efficacy against Fusarium wilt of tomato. Biol Control 54: 83–89. https://doi.org/10.1016/j.biocontrol.2010.04.004 doi: 10.1016/j.biocontrol.2010.04.004
[57]	Selvaraj S, Ganeshamoorthi P, Anand T, et al. (2014) Evaluation of liquid formulation of Pseudomonas fluorescens against Fusarium oxysporum f. sp. cubense and Helicotylenchus multicinctus in banana plantation. Biocontrol 59: 345–355. https://doi.org/10.1007/s10526-014-9569-8 doi: 10.1007/s10526-014-9569-8
[58]	Anith KN, Vyshakhi AS, Viswanathan A, et al. (2016) Population dynamics and efficacy of coconut water based liquid formulation of Pseudomonas fluorescens AMB-8. J Trop Agric 54: 184–189.
[59]	Fathi F, Saberi-Riseh R, Khodaygan P (2021) Survivability and controlled release of alginate microencapsulated Pseudomonas fluorescens VUPF506 and their effects on biocontrol of Rhizoctonia solani on potato. Int J Biol Macromol 183: 627–634. https://doi.org/10.1016/j.ijbiomac.2021.04.159 doi: 10.1016/j.ijbiomac.2021.04.159
[60]	Wang XB, Tang DY, Wang W (2021) Characterization of Pseudomonas protegens SN15-2 microcapsule encapsulated with oxidized alginate and starch. Int J Polym Mater Po 70: 684–692. https://doi.org/10.1080/00914037.2020.1760270 doi: 10.1080/00914037.2020.1760270
[61]	Minaxi, Saxeena J (2011) Efficacy of rhizobacterial strains encapsulated in nontoxic biodegradable gel matrices to promote growth and yield of wheat plants. Appl Soil Eco 48: 301–308. https://doi.org/10.1016/j.apsoil.2011.04.007 doi: 10.1016/j.apsoil.2011.04.007
[62]	Saif S, Abid Z, Ashiq MF, et al. (2021) Biofertilizer formulations, In: Inamuddin, Ahmed MI, Boddula R, et al. (Eds.), Biofertilizers: Study and impact, Beverly: Scrievener Publishing, 211–256. https://doi.org/10.1002/9781119724995.ch7
[63]	Correa EB, Sutton JC, Bettiol W (2015) Formulation of Pseudomonas chlororaphis strains for improved shelf life. Biol Control 80: 50–55. https://doi.org/10.1016/j.biocontrol.2014.09.009 doi: 10.1016/j.biocontrol.2014.09.009
[64]	Vidhyasekaran P, Rabindran R, Muthamilan M, et al. (1997) Development of a powder formulation of Pseudomonas fluorescens for control of rice blast. Plant Pathol 46: 291–297. https://doi.org/10.1046/j.1365-3059.1997.d01-27.x doi: 10.1046/j.1365-3059.1997.d01-27.x

Reader Comments

Your name:*

Email:*
© 2022 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)