Stimulation of Arabidopsis thaliana Seed Germination at Suboptimal Temperatures through Biopriming with Biofilm-Forming PGPR Pseudomonas putida KT2440
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
LM2023048
Novo Nordisk Foundation and Ministry of Education for Youth and Sports of CR within the CzeCOS program
PubMed
39409551
PubMed Central
PMC11479300
DOI
10.3390/plants13192681
PII: plants13192681
Knihovny.cz E-zdroje
- Klíčová slova
- arabidopsis, beneficial microbe, biofilm, biopriming, biostimulant, ecotypes, germination, rhizobacteria, temperature,
- Publikační typ
- časopisecké články MeSH
This study investigated the germination response to temperature of seeds of nine Arabidopsis thaliana ecotypes. They are characterized by a similar temperature dependency of seed germination, and 10 °C and 29 °C were found to be suboptimal low and high temperatures for all nine ecotypes, even though they originated from regions with diverse climates. We tested the potential of four PGPR strains from the genera Pseudomonas and Bacillus to stimulate seed germination in the two ecotypes under these suboptimal conditions. Biopriming of seeds with only the biofilm-forming strain Pseudomonas putida KT2440 significantly increased the germination of Cape Verde Islands (Cvi-0) seeds at 10 °C. However, biopriming did not significantly improve the germination of seeds of the widely utilized ecotype Columbia 0 (Col-0) at any of the two tested temperatures. To functionally investigate the role of KT2440's biofilm formation in the stimulation of seed germination, we used mutants with compromised biofilm-forming abilities. These bacterial mutants had a reduced ability to stimulate the germination of Cvi-0 seeds compared to wild-type KT2440, highlighting the importance of biofilm formation in promoting germination. These findings highlight the potential of PGPR-based biopriming for enhancing seed germination at low temperatures.
Zobrazit více v PubMed
Zhao S., Garcia D., Zhao Y., Huang D. Hydro-Electro Hybrid Priming Promotes Carrot (Daucus Carota L.) Seed Germination by Activating Lipid Utilization and Respiratory Metabolism. IJMS. 2021;22:11090. doi: 10.3390/ijms222011090. PubMed DOI PMC
Fiodor A., Ajijah N., Dziewit L., Pranaw K. Biopriming of Seed with Plant Growth-Promoting Bacteria for Improved Germination and Seedling Growth. Front. Microbiol. 2023;14:1142966. doi: 10.3389/fmicb.2023.1142966. PubMed DOI PMC
Taylor A.G. Seed Storage, Germination, Quality, and Enhancements. In: Wien H.C., Stutzel H., editors. The Physiology of Vegetable Crops. CABI; Wallingford, UK: 2020. pp. 1–30.
Tamindžić G., Azizbekian S., Miljaković D., Ignjatov M., Nikolić Z., Budakov D., Vasiljević S., Grahovac M. Assessment of Various Nanoprimings for Boosting Pea Germination and Early Growth in Both Optimal and Drought-Stressed Environments. Plants. 2024;13:1547. doi: 10.3390/plants13111547. PubMed DOI PMC
Rajendra Prasad S., Kamble U.R., Sripathy K.V., Udaya Bhaskar K., Singh D.P. Seed Bio-Priming for Biotic and Abiotic Stress Management. In: Singh D.P., Singh H.B., Prabha R., editors. Microbial Inoculants in Sustainable Agricultural Productivity. Springer India; New Delhi, India: 2016. pp. 211–228.
Gupta R., Anand G., Bar M. Developmental Phytohormones: Key Players in Host-Microbe Interactions. J. Plant Growth Regul. 2023;42:7330–7351. doi: 10.1007/s00344-023-11030-y. DOI
Mahmood A., Turgay O.C., Farooq M., Hayat R. Seed Biopriming with Plant Growth Promoting Rhizobacteria: A Review. FEMS Microbiol. Ecol. 2016;92:fiw112. doi: 10.1093/femsec/fiw112. PubMed DOI
Makhaye G., Aremu A.O., Gerrano A.S., Tesfay S., Du Plooy C.P., Amoo S.O. Biopriming with Seaweed Extract and Microbial-Based Commercial Biostimulants Influences Seed Germination of Five Abelmoschus Esculentus Genotypes. Plants. 2021;10:1327. doi: 10.3390/plants10071327. PubMed DOI PMC
Pérez-Jaramillo J.E., Mendes R., Raaijmakers J.M. Impact of Plant Domestication on Rhizosphere Microbiome Assembly and Functions. Plant Mol. Biol. 2016;90:635–644. doi: 10.1007/s11103-015-0337-7. PubMed DOI PMC
Miljaković D., Marinković J., Tamindžić G., Đorđević V., Tintor B., Milošević D., Ignjatov M., Nikolić Z. Bio-Priming of Soybean with Bradyrhizobium Japonicum and Bacillus Megaterium: Strategy to Improve Seed Germination and the Initial Seedling Growth. Plants. 2022;11:1927. doi: 10.3390/plants11151927. PubMed DOI PMC
Van Der Heijden M.G.A., Bardgett R.D., Van Straalen N.M. The Unseen Majority: Soil Microbes as Drivers of Plant Diversity and Productivity in Terrestrial Ecosystems. Ecol. Lett. 2008;11:296–310. doi: 10.1111/j.1461-0248.2007.01139.x. PubMed DOI
Adeleke B.S., Babalola O.O. The Endosphere Microbial Communities, a Great Promise in Agriculture. Int. Microbiol. 2021;24:1–17. doi: 10.1007/s10123-020-00140-2. PubMed DOI
Chen L., Hao Z., Li K., Sha Y., Wang E., Sui X., Mi G., Tian C., Chen W. Effects of Growth-promoting Rhizobacteria on Maize Growth and Rhizosphere Microbial Community under Conservation Tillage in Northeast China. Microb. Biotechnol. 2021;14:535–550. doi: 10.1111/1751-7915.13693. PubMed DOI PMC
Mekureyaw M.F., Pandey C., Hennessy R.C., Nicolaisen M.H., Liu F., Nybroe O., Roitsch T. The Cytokinin-Producing Plant Beneficial Bacterium Pseudomonas Fluorescens G20-18 Primes Tomato (Solanum Lycopersicum) for Enhanced Drought Stress Responses. J. Plant Physiol. 2022;270:153629. doi: 10.1016/j.jplph.2022.153629. PubMed DOI
Bean K.M., Kisiala A.B., Morrison E.N., Emery R.J.N. Trichoderma Synthesizes Cytokinins and Alters Cytokinin Dynamics of Inoculated Arabidopsis Seedlings. J. Plant Growth Regul. 2022;41:2678–2694. doi: 10.1007/s00344-021-10466-4. DOI
Stegelmeier A.A., Rose D.M., Joris B.R., Glick B.R. The Use of PGPB to Promote Plant Hydroponic Growth. Plants. 2022;11:2783. doi: 10.3390/plants11202783. PubMed DOI PMC
Akhtar S.S., Amby D.B., Hegelund J.N., Fimognari L., Großkinsky D.K., Westergaard J.C., Müller R., Moelbak L., Liu F., Roitsch T. Bacillus Licheniformis FMCH001 Increases Water Use Efficiency via Growth Stimulation in Both Normal and Drought Conditions. Front. Plant Sci. 2020;11:297. doi: 10.3389/fpls.2020.00297. PubMed DOI PMC
Mekureyaw M.F., Beierholm A.E., Nybroe O., Roitsch T.G. Inoculation of Tomato (Solanum Lycopersicum) Roots with Growth Promoting Pseudomonas Strains Induces Distinct Local and Systemic Metabolic Biosignatures. Physiol. Mol. Plant Pathol. 2022;117:101757. doi: 10.1016/j.pmpp.2021.101757. DOI
Eichmann R., Richards L., Schäfer P. Hormones as Go-betweens in Plant Microbiome Assembly. Plant J. 2021;105:518–541. doi: 10.1111/tpj.15135. PubMed DOI PMC
Backer R., Rokem J.S., Ilangumaran G., Lamont J., Praslickova D., Ricci E., Subramanian S., Smith D.L. Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture. Front. Plant Sci. 2018;9:1473. doi: 10.3389/fpls.2018.01473. PubMed DOI PMC
Saleemi M., Kiani M.Z., Sultan T., Khalid A., Mahmood S. Integrated Effect of Plant Growth-Promoting Rhizobacteria and Phosphate-Solubilizing Microorganisms on Growth of Wheat (Triticum Aestivum L.) under Rainfed Condition. Agric. Food Secur. 2017;6:46. doi: 10.1186/s40066-017-0123-7. DOI
Mellidou I., Karamanoli K. Unlocking PGPR-Mediated Abiotic Stress Tolerance: What Lies Beneath. Front. Sustain. Food Syst. 2022;6:832896. doi: 10.3389/fsufs.2022.832896. DOI
Ahmad I., Ahmad M., Hussain A., Jamil M. Integrated Use of Phosphate-Solubilizing Bacillus Subtilis Strain IA6 and Zinc-Solubilizing Bacillus Sp. Strain IA16: A Promising Approach for Improving Cotton Growth. Folia Microbiol. 2021;66:115–125. doi: 10.1007/s12223-020-00831-3. PubMed DOI
Tournay R.J., Firrincieli A., Parikh S.S., Sivitilli D.M., Doty S.L. Effect of Arsenic on EPS Synthesis, Biofilm Formation, and Plant Growth-Promoting Abilities of the Endophytes Pseudomonas PD9R and Rahnella Laticis PD12R. Environ. Sci. Technol. 2023;57:8728–8738. doi: 10.1021/acs.est.2c08586. PubMed DOI
Saleem S., Iqbal A., Ahmed F., Ahmad M. Phytobeneficial and Salt Stress Mitigating Efficacy of IAA Producing Salt Tolerant Strains in Gossypium Hirsutum. Saudi J. Biol. Sci. 2021;28:5317–5324. doi: 10.1016/j.sjbs.2021.05.056. PubMed DOI PMC
Nilsson M., Chiang W., Fazli M., Gjermansen M., Givskov M., Tolker-Nielsen T. Influence of Putative Exopolysaccharide Genes on Pseudomonas Putida KT2440 Biofilm Stability. Environ. Microbiol. 2011;13:1357–1369. doi: 10.1111/j.1462-2920.2011.02447.x. PubMed DOI
Neal A., Ton J. Systemic Defense Priming by Pseudomonas Putida KT2440 in Maize Depends on Benzoxazinoid Exudation from the Roots. Plant Signal. Behav. 2013;8:e22655. doi: 10.4161/psb.22655. PubMed DOI PMC
Heredia-Ponce Z., De Vicente A., Cazorla F.M., Gutiérrez-Barranquero J.A. Beyond the Wall: Exopolysaccharides in the Biofilm Lifestyle of Pathogenic and Beneficial Plant-Associated Pseudomonas. Microorganisms. 2021;9:445. doi: 10.3390/microorganisms9020445. PubMed DOI PMC
Lee Y., Seo H., Yeom J., Park W. Molecular Characterization of the Extracellular Matrix in a Pseudomonas Putida dsbA Mutant: Implications for Acidic Stress Defense and Plant Growth Promotion. Res. Microbiol. 2011;162:302–310. doi: 10.1016/j.resmic.2010.11.002. PubMed DOI
Tran H., Ficke A., Asiimwe T., Höfte M., Raaijmakers J.M. Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol. 2007;175:731–742. doi: 10.1111/j.1469-8137.2007.02138.x. PubMed DOI
Glick B.R. Beneficial Plant-Bacterial Interactions. Springer International Publishing; Cham, Switzerland: 2015. Biocontrol of Bacteria and Fungi; pp. 181–230.
Ramasamy K., Joe M.M., Kim K.-Y., Lee S.-M., Shagol C., Rangasamy A., Chung J.-B., Islam M.d.R., Sa T.-M. Synergistic Effects of Arbuscular Mycorrhizal Fungi and Plant Growth Promoting Rhizobacteria for Sustainable Agricultural Production. Korean J. Environ. Agric. 2011;44:637–649. doi: 10.7745/KJSSF.2011.44.4.637. DOI
Kierul K. Ph.D. Dissertation. Humboldt University of Berlin, Faculty of Mathematics and Natural Sciences; Berlin, Germany: 2013. Comprehensive Proteomic Study of Bacillus Amyloliquefaciens Strain FZB42 and Its Response to Plant Root Exudates.
Huang Z., Footitt S., Finch-Savage W.E. The Effect of Temperature on Reproduction in the Summer and Winter Annual Arabidopsis Thaliana Ecotypes Bur and Cvi. Ann. Bot. 2014;113:921–929. doi: 10.1093/aob/mcu014. PubMed DOI PMC
Lasky J.R., Des Marais D.L., McKAY J.K., Richards J.H., Juenger T.E., Keitt T.H. Characterizing Genomic Variation of Arabidopsis Thaliana: The Roles of Geography and Climate. Mol. Ecol. 2012;21:5512–5529. doi: 10.1111/j.1365-294X.2012.05709.x. PubMed DOI
Burghardt L.T., Metcalf C.J.E., Donohue K. A Cline in Seed Dormancy Helps Conserve the Environment Experienced during Reproduction across the Range of Arabidopsis Thaliana. Am. J. Bot. 2016;103:47–59. doi: 10.3732/ajb.1500286. PubMed DOI
Price N., Moyers B.T., Lopez L., Lasky J.R., Monroe J.G., Mullen J.L., Oakley C.G., Lin J., Ågren J., Schrider D.R., et al. Combining Population Genomics and Fitness QTLs to Identify the Genetics of Local Adaptation in Arabidopsis Thaliana. Proc. Natl. Acad. Sci. USA. 2018;115:5028–5033. doi: 10.1073/pnas.1719998115. PubMed DOI PMC
Shelke A., Tapkir P. Formulation of Cost Effective and Locally Available BioFertilizer for Increased Production and Faster Germination. Int. J. Adv. Eng. Manag. 2020;2:25–37.
Kefela T., Gachomo E.W., Kotchoni S.O. Paenibacillus Polymyxa, Bacillus Licheniformis and Bradyrhizobium Japonicum IRAT FA3 Promote Faster Seed Germination Rate, Growth and Disease Resistance under Pathogenic Pressure. J. Plant Biochem. Physiol. 2015;3:10-4172.
Kumawat K.C., Keshani, Nagpal S., Sharma P. Biofertilizers. Elsevier; Amsterdam, The Netherlands: 2021. Present Scenario of Bio-Fertilizer Production and Marketing around the Globe; pp. 389–413.
Houida S., Yakkou L., Kaya L.O., Bilen S., Fadil M., Raouane M., El Harti A., Amghar S. Biopriming of Maize Seeds with Plant Growth-Promoting Bacteria Isolated from the Earthworm Aporrectodea Molleri: Effect on Seed Germination and Seedling Growth. Lett. Appl. Microbiol. 2022;75:61–69. doi: 10.1111/lam.13693. PubMed DOI
Yang N., Nesme J., Røder H.L., Li X., Zuo Z., Petersen M., Burmølle M., Sørensen S.J. Emergent Bacterial Community Properties Induce Enhanced Drought Tolerance in Arabidopsis. Npj Biofilms Microb. 2021;7:82. doi: 10.1038/s41522-021-00253-0. PubMed DOI PMC
Hanifah N.A.S.B., Ghadamgahi F., Ghosh S., Ortiz R., Whisson S.C., Vetukuri R.R., Kalyandurg P.B. Comparative Transcriptome Profiling Provides Insights into the Growth Promotion Activity of Pseudomonas Fluorescens Strain SLU99 in Tomato and Potato Plants. Front. Plant Sci. 2023;14:1141692. doi: 10.3389/fpls.2023.1141692. PubMed DOI PMC
Rostamikia Y., Tabari Kouchaksaraei M., Asgharzadeh A., Rahmani A. The Effect of Plant Growth-Promoting Rhizobacteria on Growth and Physiological Characteristics of Corylus Avellana Seedlings. Ecopersia. 2016;4:1471–1479. doi: 10.18869/modares.ecopersia.4.3.1471. DOI
Zulueta-Rodríguez R., Hernández-Montiel L., Murillo-Amador B., Rueda-Puente E., Capistrán L., Troyo-Diéguez E., Córdoba-Matson M. Effect of Hydropriming and Biopriming on Seed Germination and Growth of Two Mexican Fir Tree Species in Danger of Extinction. Forests. 2015;6:3109–3122. doi: 10.3390/f6093109. DOI
Ajijah N., Fiodor A., Pandey A.K., Rana A., Pranaw K. Plant Growth-Promoting Bacteria (PGPB) with Biofilm-Forming Ability: A Multifaceted Agent for Sustainable Agriculture. Diversity. 2023;15:112. doi: 10.3390/d15010112. DOI
Carezzano M.E., Paletti Rovey M.F., Cappellari L.D.R., Gallarato L.A., Bogino P., Oliva M.D.L.M., Giordano W. Biofilm-Forming Ability of Phytopathogenic Bacteria: A Review of Its Involvement in Plant Stress. Plants. 2023;12:2207. doi: 10.3390/plants12112207. PubMed DOI PMC
Bais H.P., Fall R., Vivanco J.M. Biocontrol of Bacillus Subtilis against Infection of Arabidopsis Roots by Pseudomonas Syringae Is Facilitated by Biofilm Formation and Surfactin Production. Plant Physiol. 2004;134:307–319. doi: 10.1104/pp.103.028712. PubMed DOI PMC
Sandhya V., Sk Z.A., Grover M., Reddy G., Venkateswarlu B. Alleviation of Drought Stress Effects in Sunflower Seedlings by the Exopolysaccharides Producing Pseudomonas Putida Strain GAP-P45. Biol. Fertil. Soils. 2009;46:17–26. doi: 10.1007/s00374-009-0401-z. DOI
Cheng Z., Park E., Glick B.R. 1-Aminocyclopropane-1-Carboxylate Deaminase from Pseudomonas Putida UW4 Facilitates the Growth of Canola in the Presence of Salt. Can. J. Microbiol. 2007;53:912–918. doi: 10.1139/W07-050. PubMed DOI
New Horizons in Plant-Microbe Interactions