Growth promotion of raspberry and strawberry plants by bacterial inoculants
Paweł Trzciński
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0003-4568-6504
Mateusz Frąc
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-9220-4227
Anna Lisek
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0002-3421-8759
Michał Przybył
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0001-7018-2207
Magdalena Frąc
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin Polandhttps://orcid.org/0000-0001-9437-3139
Lidia Sas-Paszt
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Polandhttps://orcid.org/0000-0003-4076-4032
Abstrakt
Study on potential mechanisms influencing the growth of raspberry and strawberry plants showed that the most active was Bacillus sp. strain AF75BC producing IAA and siderophores, and having the ability to release phosphorus. The latter feature was also present in the strains Sp115AD (B. subtilis) and SP116AC (Paenibacillus polymyxa). Two of the tested strains: SP116AC and JaFGU (Lysobacter sp.) showed the ability to fix atmospheric nitrogen, while the AF75AB2 (Bacillus sp.) produced siderophores and IAA. All strains showed an antagonism toward the most important pathogens of strawberry and raspberry, i.e. Verticillium dahliae, Botrytis cinerea, Phytophthora cactorum and Colletotrichum acutatum, limiting their growth to a different extent on the PDA medium. Inoculation of raspberry roots with the tested bacteria resulted in an increase of some growth parameters of their above-ground part in cv. Poemat. In the case of cv. Polana, a significant increase was found only in the chlorophyll content in the leaves. All the inoculants caused an increase in dry mass of roots in cv. Polana, and in cv. Poemat similar effect was observed after applying Inoculants 1 and 3. The treatments of strawberry roots with any of the inoculants resulted in a significant increase in the total leaf surface area in cv. Rumba, but they had no effect on the chlorophyll content in the leaves of either cultivar. All the inoculants significantly increased the total length of roots and their total surface area in cv. Rumba. This parameter also increased in cv. Elsanta, and the number of root tips also significantly increased in this cultivar. Our study showed that the tested inocula is a promising alternative as a bio-fertilizer for small fruit production in sustainable and organic agricultural systems.
Słowa kluczowe:
growth mechanisms, antagonism, pathogens, growth parameters, microbial inoculantsBibliografia
Adesemoye, A.O., Kloepper, J.W. (2009). Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl. Microbiol. Biotechnol., 85, 1–12. https://doi.org/10.1007/s00253-009-2196-0
Ahmed, E., Holmstrom, S.J. (2014). Siderophores in environmental research: roles and applications. Microb. Biotechnol., 7, 196–208. https://doi.org/10.1111/1751-7915.12117
Alexander, D.B., Zuberer, D.A. (1991). Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fert. Soils, 12, 39–45.
Altaf, M.A., Shahid, R., Qadir, A., Naz, S., Ren, M.X., Ejaz, S., Altaf, M.M., Shakoor, A. (2019). Potential role of Plant Growth Promoting Rhizobacteria (PGPR) to reduce chemical fertilizer in horticultural crops. Int. J. Res. Agric. For., 6, 21–30.
Backer, R., Rokem, J.S., Ilangumaran, G., John Lamont, J., Praslickova, D., Ricci, E., Subramanian, S., Smith, D.L. (2018). Plant Growth-Promoting Rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci., 9, 1473. https://doi.org/10.3389/fpls.2018.01473
Bashan, Y. (1998). Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol. Adv., 16, 729–770. https://doi.org/10.1016/S0734-9750(98)0 0003-2
Bent, E., Tuzun, S., Chanway, C.P., Enebak, S. (2001). Alterations in plant growth and in root hormone levels of lodgepole pines inoculated with rhizobacteria. Can. J. Microbiol., 47(9), 793–800.
Bhattacharyya, P.N., Jha, D.K. (2012). Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol., 28, 1327–1350.
Bottini, R., Cassán, F., Piccoli, P. (2004). Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol., 65, 497–503.
Grand View Research (2018). Biostimulants Market Size Worth $4.14 Billion By 2025|CAGR: 10.2%. Available online: https://www.grandviewresearch.com/press-release/global-biostimulants-market [access 8 March 2019].
Calvo, P., Nelson, L. Kloepper, J. (2014). Agricultural uses of plant biostimulants. Plant Soil., 383(1), 3–41.
Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard C., Mahillon, J. (2019). Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group.
Front. Microbiol., 10, 302. tttps://doi.org/10.3389/fmicb.2019.00302
Cheng, F., Li, G., Peng, Y., Wang, A., Zhu, J. (2020). Mixed bacterial fermentation can control the growth and development of Verticillium dahliae. Biotechnol. Biotechnol. Equip., 34(1), 58–69. https://doi.org/10.1080/13102818.2020.1713023
de Silva, A., Patterson, K., Rothrock, C., Moore, J. (2000). Growth promotion of highbush blueberry by fungal and bacterial inoculants. HortScience, 35(7), 1228–1230.
du Jardin, P. (2015). Plant biostimulants: definition, concept, main categories and regulation. Sci. Hortic., 196, 3–14. https://doi.org/10.1016/j.scienta.2015.09.021
Erturk, Y., Ercisli, S., Cakmakci, R. (2012). Yield and growth response of strawberry to plant growth-promoting rhizobacteria inoculation. J. Plant Nutr., 35, 817–826.
Esitken, A., Karlidag, H., Ercisli, S., Turan, M., Sahin, F. (2003). The effect of spraying a growth promoting bacterium on the yield, growth and nutrient element composition of leaves of apricot (Prunus armeniaca L. cv. Hacihaliloglu). Aust. J. Agric. Res., 54, 377–380.
Esitken, A., Pirlak, L., Turan, M., Sahin, F. (2006). Effects of floral and foliar application of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrition of sweet cherry. Sci. Hortic., 110, 324–327.
Esitken, A., Yildiza, H.E., Ercisli, S., Donmez, M.F., Turan, M., Gunes, A. (2010). Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci. Hortic., 124, 62–66.
Exposito, R.G., Postma, J., Raaijmakers, J.M., De Bruijn, I. (2015). Diversity and activity of Lysobacter species from disease suppressive soils. Front. Microbiol., 6, 1243. https://doi.org/10.3389/fmicb.2015.01243
Falardeau, J., Wise, C., Novitsky, L. Avis, T.J. (2013). Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J. Chem. Ecol., 39, 869–878.
Gouda, S., Kerry, R.G., Das, G., Paramithiotis, S., Shin, H.-S., Patra, J.K. (2018). Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol. Res., 206, 131–140. https://doi.org/10.1016/j.micres.2017.08.016
Govindasamy, V., Senthilkumar, M., Magheshwaran, V., Kumar, U., Bose, P., Sharma, V., Annapurna, K. (2010). Bacillus and Paenibacillus spp.: potential PGPR for sustainable agriculture. In: Plant growth and health promoting bacteria, D.K. Maheshwari (eds.), Springer-Verlag, Berlin–Heidelberg, 333–364. https://doi.org/10.1007/978-3-642-13612-2_15
Gutiérrez‐Mañero, F.J., Ramos‐Solano, B., Probanza, A.N., Mehouachi, J.,R. Tadeo, F., Talon, M. (2001). The plant‐growth‐promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant., 111(2), 206–211.
Hinarejos, E., Castellano, M., Rodrigo, I., Belles, J.M., Conejero, V., Lopez-Gresa, M.P., Lisón, P. (2016). Bacillus subtilis IAB/BS03 as a potential biological controlagent. Eur. J. Plant Pathol., 146, 597–608. https://doi.org/10.1007/s10658-016-0945-3
Iwata, K., Azlan, A., Yamakawa, H., Omori, T. (2010). Ammonia accumulation in culture broth by the novel nitrogen-fixing bacterium, Lysobacter sp. E4. J. Biosci. Bioeng., 110(4), 415–418.
Karlidag, H., Yildirim, E., Turan, M., Donmez, M.P.F. (2013). Plant growth-promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria × ananassa). HortScience, 48(5), 563–567.
Karlidag, H., Yildirim, E., Turan, M., Donmez, F. (2011). Effect of plant growth promoting bacteria on mineral organic fertilizer use efficiency, plant growth and mineral contents of strawberry (Faragria × ananassa L. Duch). Ind. J. Biotechnol., 9, 289–297.
Kurokura, T., Hiraide, S., Shimamura, Y., Yamane, K. (2017). PGPR improves yield of strawberry species under less-fertilized conditions. Environ. Control Biol., 55(3), 121–128. https://doi.org/10.2525/ecb.54.121
Lane, D.J. (1991). 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematics, Stackebrandt, E., Goodfellow, M., (eds.). John Wiley and Sons, New York, 115–175.
Le Mire, G., Nguyen, M.L., Fassotte, B., du Jardin, P., Verheggen, F., Delaplace, P., Jijakli, M.H. (2016). Implementing plant biostimulants and biocontrol strategies in the agroecological management of cultivated ecosystems. A review. Biotechnol. Agron. Soc. Environ., 20(S1), 299–313.
Liu, D., Yang, Q., Ge, K., Hu, X., Qi, G., Du, B., Liu, K., Ding, Y. (2017). Promotion of iron nutrition and growth on peanut by Paenibacillus illinoisensis and Bacillus sp. strains in calcareous soil. Braz. J. Microbiol., 48, 656–670.
Loper, J.E., Henkels, M.D. (1997). Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl. Environ. Microbiol., 63, 99–105.
Mikiciński, A., Puławska, J., Molzhigitova, A., Sobiczewski, P. (2020). Bacterial species recognized for the first time for its biocontrol activity against fire blight (Erwinia amylovora). Eur. J. Plant Pathol., 156, 257–272.
Nautiyal, C.S. (1999). An effcient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett., 170, 265–270.
Neufeld, H., Chappelka, A., Somers, G., Burkey, K., Davison, A., Finkelstein, P. (2006). Visible foliar injury caused by ozone alters the relationship between SPAD meter readings and chlorophyll concentrations in cutleaf coneflower. Photosynth. Res., 87, 281–286. https://doi.org/10.1007/s11120-005-9008-x
Orhan, E., Esitken, A., Ercisli, S., Turan, M., Sahin, F. (2006). Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci. Hortic-Amsterdam, 111, 38–43.
Pii, Y., Mimmo, T., Tomasi, N., Terzano, R., Cesco, S., Crecchio, C. (2015). Microbial interactions in the rhizosphere: beneficial influences of plant growth promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils 51, 403–415. https://doi.org/10.1007/s00374-015-0996-1
Pylak, M., Oszust, K., Frąc, M. (2019). Review report on the role of bioproducts, biopreparations, biostimulants and microbial inoculants in organic production of fruit. Rev. Environ. Sci. Biotechnol., 18, 597–616. https://doi.org/10.1007/s11157-019-09500-5
Ricci, M., Tilbury, L., Daridon, B., Sukalac, K. (2019). General principles to justify plant biostimulant claims. Front. Plant Sci., 10, 494. https://doi.org/10.3389/fpls.2019.00494
Ribeiro, C.M., Cardoso, E.J.B.N. (2012). Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil pine (Araucaria angustifolia). Microbiol. Res., 167, 69–78.
Richardson, A.E., Hadobas, P.A., Hayes, J.E., O’Hara, C.P., Simpson R.J. (2001). Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil micro-organisms. Plant Soil, 229, 47–56.
Robledo-Buriticá J., Aristizábal-Loaiza, J.C., Ceballos-Aguirre, N., Cabra Cendales, T. (2018). Influence of plant growth-promoting rhizobacteria (PGPR) on blackberry (Rubus glaucus Benth. cv. thornless) growth under semi-cover and field conditions. Acta Agron., 67(2), 258–263.
Rouphael, Y., Colla, G. (2020). Biostimulants in agriculture. Front. Plant Sci., 11. https://doi.org/10.3389/fpls.2020.00040article 40
Sabir, A. (2013). Improvement of grafting efficiency in hard grafting grape Berlandieri hybrid rootstocks by plant growth-promoting rhizobacteria (PGPR). Sci. Hortic., 164, 24–29.
Santos, M.S., Nogueira, M.A., Hungria, M. (2019). Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of benefcial bacteria in agriculture. AMB Express, 9(1), 205.
Sas-Paszt, L., Sumorok, B., Derkowska, E., Trzciński, P., Lisek, A., Grzyb, S. Z., Sitarek, M., Przybył, M., Frąc, M. (2019a). Effect of microbiologically enriched fertilizers on the vegetative growth of strawberry plants in container-based cultivation at different levels of irrigation. J. Res. Appl. Agric. Engineer., 64(2), 38–46.
Sas-Paszt, L., Sumorok, B., Derkowska, E., Trzciński, P., Lisek, A., Grzyb, Z.S., Sitarek, M., Przybył, M., Frąc, M. (2019b). Effect of microbiologically enriched fertilizers on the vegetative growth of strawberry plants under field conditions in the first year of plantation. J. Res. Appl. Agric. Engineer., 64(2), 29–37.
Sas-Paszt, L., Sumorok, B., Grzyb. Z.S., Głuszek, S., Sitarek, M., Lisek, A., Derkowska, E., Trzciński, P., Przybył, M., Frąc, M., Górnik, K. (2020a). Effect of microbiologically enriched fertilizers on the yielding of strawberry plants under field conditions in the second year of plantation. J. Res. Appl. Agric. Engineer., 65(1), 31–38.
Sas-Paszt, L., Sumorok, B., Grzyb, Z.S., Głuszek, S., Sitarek, M., Lisek, A., Derkowska, E., Trzciński, P., Stępień, W., Przybył, M., Frąc, M., Górnik, K. (2020b). Effect of microbiologically enriched fertilizers on the yielding of strawberry plants in container-based cultivation at diffrent levels of irrigation. J. Res. Appl. Agric. Engineer., 65(1), 21–29.
Satapute, P.P., Olekar, H.S., Shetti, A.A., Kulkarni, A.G., Hiremath, G.B., Patagundi B.I., Shivsharan, C.T., Kaliwal B.B. (2012). Isolation and characterization of nitrogen fixing Bacillus subtilis strain As-4 from agricultural soil. Int. J. Rec. Sci. Res., 9, 762 –765.
Seema, K., Mehta, K., Singh, N. (2018). Studies on the effect of plant growth promoting rhizobacteria (PGPR) on growth, physiological parameters, yield and fruit quality of strawberry cv. Chandler. J. Pharmacogn. Phytochem., 7(2), 383–387.
Singh, R.K., Singh, P., Li, H.-B., Song, Q.-Q., Guo, D.-J., Solanki, M.K., Verma, K.K., Malviya, M.K., Song, X.-P., Lakshmanan, P., Yang, L.T., Li, Y.-R. (2020). Diversity of nitrogen-fixing rhizobacteria associated with sugarcane: a comprehensive study of plant-microbe interactions for growth enhancement in Saccharum spp. BMC Plant Biol., 20, 220. https://doi.org/10.1186/s12870-020-02400-9
Spaepen, S., Dobbelaere, S., Croonenborghs, A., Vanderleyden, J. (2008). Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil, 312, 15–23.
Swain, M.R., Naskar, S.K., Ray, R.C. (2007). Indole-3-acetic acid production and effect on sprouting of Yam (Dioscorea rotundata L.) minisetts by Bacillus subtilis isolated from culturable cowdung microflora. Pol. J. Microbiol., 56, 103–110.
Timmusk, S., Nicander, B., Granhall, U., Tillberg, E. (1999). Cytokinin production by Paenibacillus polymyxa. Soil Biol. Biochem., 31, 1847–1852.
Toral, L., Rodriguez, M., Béjar, V., Sampedro, I. (2018). Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Front. Microbiol., 9, 1315. https://doi.org/10.3389/fmicb.2018.01315.
Traon, D., Amat, L., Zotz, F., du Jardin, P. (2014). A legal framework for plant biostimulants and agronomic fertiliser additives in the EU. Report to the European Commission, Enterprise & Industry Directorate – General. Brussels, Arcadia International. Available: http://ec.europa.eu/DocsRoom/documents/5403/attachments/1/translations/en/renditions/native
Vessey, J.K. (2003). Plant growth promoting rhizobacteria as biofertilizer. Plant Soil 255(2), 571–586. https://doi.org/10.1023/A:1026037216893
Whipps, J.M. (2001). Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot., 52, 487–511.
Yu, X., Ai, C., Xin, L., Zhou, G. (2011). The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur. J. Soil Biol., 47(2), 138–145. https://doi.org/10.1016/j.ejsobi.2010.11.001
Zhang, F., Li, X.-L., Zhu, S.-J., Ojaghian, M.R., Zhang J.-Ze. (2018). Biocontrol potential of Paenibacillus polymyxa against Verticillium dahliae infecting cotton plants. Biol. Control, 127, 70–77.
Zhang, L.-N., Wang, D.-C., Hu, Q., Dai, X-Q., Xie, Y.-S., Li, Q., Liu, H.-M., Guo, J.-H. (2019). Consortium of plant growth-promoting rhizobacteria strains suppresses sweet pepper disease by altering the rhizosphere microbiota. Front. Microbiol., https://doi.org/10.3389/fmicb.2019.01668
Zhang, Y., Ren, J., Wang, W., Chen, B., Li, E., Chen, S. (2020). Siderophore and indolic acid production by Paenibacillus triticisoli BJ-18 and their plant growth-promoting and antimicrobe abilities. Peer J., 8, e9403. http://doi.org/10.7717/peerj.9403
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Poland https://orcid.org/0000-0003-4568-6504
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-9220-4227
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Poland https://orcid.org/0000-0002-3421-8759
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Poland https://orcid.org/0000-0001-7018-2207
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin Poland https://orcid.org/0000-0001-9437-3139
The National Institute of Horticultural Research, Department of Microbiology and Rhizosphere, Pomologiczna 18, 96-100 Skierniewice, Poland https://orcid.org/0000-0003-4076-4032
Licencja
Artykuły są udostępniane na zasadach CC BY 4.0 (do 2021 r. na zasadach CC BY-NC-ND 4.0 międzynarodowe).
Przysłanie artykułu do redakcji oznacza, że nie był on opublikowany wcześniej i nie jest rozpatrywany do publikacji gdzie indziej.
Autor podpisuje oświadczenie o oryginalności dzieła, wkładzie poszczególnych osób i źródle finansowania.
