Characterization of Bacillus pacificus G124 and Its Promoting Role in Plant Growth and Drought Tolerance
Abstract
1. Introduction
2. Results
2.1. Morphological Observation of the Strain G124
2.2. Molecular Identification of the Strain G124
2.3. Potential Host Growth-Promoting Properties of the Strain G124
2.4. B. pacificus G124 Improves Growth and Physiological Parameters of Arabidopsis Thaliana and Medicago Sativa Plants under Drought
2.5. B. pacificus G124 Improves Biochemical Characteristics of M. sativa Plants under Drought
3. Discussion
4. Materials and Methods
4.1. Strain G124 and Plant Materials
4.2. Morphological and Molecular Identification of G124 Strain
4.3. Determination of Growth-Promoting Ability of G124 Strain
4.3.1. Siderophore Production
4.3.2. Phosphorus-Solubilizing Capacity
4.3.3. IAA Secretion Capacity
4.3.4. EPS Production Capacity
4.3.5. ACC Deaminase Activity
4.4. Preparation and Inoculation of G124 Suspension
4.5. Determination of Physiological and Biochemical Indices of Seedling Growth
4.6. Data Processing
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Tian, T.; Wang, S.; Yang, S.; Yang, Z.; Liu, S.; Wang, Y.; Gao, H.; Zhang, S.; Yang, X.; Jiang, C.; et al. Genome assembly and genetic dissection of a prominent drought-resistant maize germplasm. Nat. Genet. 2023, 55, 496–506. [Google Scholar] [CrossRef] [PubMed]
- Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269. [Google Scholar] [CrossRef] [PubMed]
- Cheng, Y.T.; Zhang, L.; He, S.Y. Plant-Microbe Interactions Facing Environmental Challenge. Cell Host Microbe 2019, 26, 183–192. [Google Scholar] [CrossRef] [PubMed]
- Gao, C.; Xu, L.; Montoya, L.; Madera, M.; Hollingsworth, J.; Chen, L.; Purdom, E.; Singan, V.; Vogel, J.; Hutmacher, R.B.; et al. Co-occurrence networks reveal more complexity than community composition in resistance and resilience of microbial communities. Nat. Commun. 2022, 13, 3867. [Google Scholar] [CrossRef] [PubMed]
- Gholizadeh, S.; Nemati, I.; Vestergård, M.; Barnes, C.J.; Kudjordjie, E.N.; Nicolaisen, M. Harnessing root-soil-microbiota interactions for drought-resilient cereals. Microbiol. Res. 2024, 283, 127698. [Google Scholar] [CrossRef]
- Jansson, J.K.; Hofmockel, K.S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 2020, 18, 35–46. [Google Scholar] [CrossRef]
- Naylor, D.; Coleman-Derr, D. Drought Stress and Root-Associated Bacterial Communities. Front. Plant Sci. 2018, 8, 2223. [Google Scholar] [CrossRef]
- Naylor, D.; DeGraaf, S.; Purdom, E.; Coleman-Derr, D. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 2017, 11, 2691–2704. [Google Scholar] [CrossRef]
- de Vries, F.T.; Griffiths, R.I.; Knight, C.G.; Nicolitch, O.; Williams, A. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 2020, 368, 270–274. [Google Scholar] [CrossRef]
- Niu, X.G.; Song, L.C.; Xiao, Y.N.; Ge, W.D. Drought-Tolerant Plant Growth-Promoting Rhizobacteria Associated with Foxtail Millet in a Semi-arid Agroecosystem and Their Potential in Alleviating Drought Stress. Front. Microbiol. 2018, 8, 2580. [Google Scholar] [CrossRef]
- Xu, L.; Naylor, D.; Dong, Z.B.; Simmons, T.; Pierroz, G.; Hixson, K.K.; Kim, Y.M.; Zink, E.M.; Engbrecht, K.M.; Wang, Y.; et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc. Natl. Acad. Sci. USA 2018, 115, E4284–E4293. [Google Scholar] [CrossRef] [PubMed]
- Bogati, K.; Walczak, M. The Impact of Drought Stress on Soil Microbial Community, Enzyme Activities and Plants. Agronomy 2022, 12, 189. [Google Scholar] [CrossRef]
- Ahmad, H.M.; Fiaz, S.; Hafeez, S.; Zahra, S.; Shah, A.N.; Gul, B.; Aziz, O.; Mahmood Ur, R.; Fakhar, A.; Rafique, M.; et al. Plant Growth-Promoting Rhizobacteria Eliminate the Effect of Drought Stress in Plants: A Review. Front. Plant Sci. 2022, 13, 875774. [Google Scholar] [CrossRef] [PubMed]
- Chieb, M.; Gachomo, E.W. The role of plant growth promoting rhizobacteria in plant drought stress responses. BMC Plant Biol. 2023, 23, 407. [Google Scholar] [CrossRef] [PubMed]
- Kisvarga, S.; Hamar-Farkas, D.; Ördögh, M.; Horotán, K.; Neményi, A.; Kovács, D.; Orlóci, L. The Role of the Plant-Soil Relationship in Agricultural Production-With Particular Regard to PGPB Application and Phytoremediation. Microorganisms 2023, 11, 1616. [Google Scholar] [CrossRef]
- Niu, S.Q.; Gao, Y.; Zi, H.X.; Liu, Y.; Liu, X.M.; Xiong, X.Q.; Yao, Q.Q.; Qin, Z.W.; Chen, N.; Guo, L.; et al. The osmolyte-producing endophyte Streptomyces albidoflavus OsiLf-2 induces drought and salt tolerance in rice via a multi-level mechanism. Crop J. 2022, 10, 375–386. [Google Scholar] [CrossRef]
- Huang, X.F.; Zhou, D.M.; Lapsansky, E.R.; Reardon, K.F.; Guo, J.H.; Andales, M.J.; Vivanco, J.M.; Manter, D.K. Mitsuaria sp. and Burkholderia sp. from Arabidopsis rhizosphere enhance drought tolerance in Arabidopsis thaliana and maize (Zea mays L.). Plant Soil 2017, 419, 523–539. [Google Scholar] [CrossRef]
- Rashid, U.; Yasmin, H.; Hassan, M.N.; Naz, R.; Nosheen, A.; Sajjad, M.; Ilyas, N.; Keyani, R.; Jabeen, Z.; Mumtaz, S.; et al. Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep. 2022, 41, 549–569. [Google Scholar] [CrossRef]
- Slimani, A.; Raklami, A.; Oufdou, K.; Meddich, A.J.G.P. Isolation and Characterization of PGPR and Their Potenzial for Drought Alleviation in Barley Plants. Gesunde Pflanz. 2022, 75, 377–391. [Google Scholar] [CrossRef]
- Hyder, S.; Rizvi, Z.F.; de los Santos-Villalobos, S.; Santoyo, G.; Gondal, A.; Khalid, N.; Fatima, S.N.; Nadeem, M.; Rafique, K.; Rani, A. Applications of plant growth-promoting rhizobacteria for increasing crop production and resilience. J. Plant Nutr. 2023, 46, 2551–2580. [Google Scholar] [CrossRef]
- Selim, S.; Hassan, Y.M.; Saleh, A.M.; Habeeb, T.H.; AbdElgawad, H. Actinobacterium isolated from a semi-arid environment improves the drought tolerance in maize (Zea mays L.). Plant Physiol. Biochem. 2019, 142, 15–21. [Google Scholar] [CrossRef] [PubMed]
- Trivedi, P.; Leach, J.E.; Tringe, S.G.; Sa, T.; Singh, B.K. Plant-microbiome interactions: From community assembly to plant health. Nat. Rev. Microbiol. 2020, 18, 607–621. [Google Scholar] [CrossRef] [PubMed]
- Banerjee, S.; van der Heijden, M.G.A. Soil microbiomes and one health. Nat. Rev. Microbiol. 2023, 21, 6–20. [Google Scholar] [CrossRef] [PubMed]
- de Andrade, L.A.; Santos, C.H.B.; Frezarin, E.T.; Sales, L.R.; Rigobelo, E.C. Plant Growth-Promoting Rhizobacteria for Sustainable Agricultural Production. Microorganisms 2023, 11, 1088. [Google Scholar] [CrossRef] [PubMed]
- Timmusk, S.; Behers, L.; Muthoni, J.; Muraya, A.; Aronsson, A.C. Perspectives and Challenges of Microbial Application for Crop Improvement. Front. Plant Sci. 2017, 8, 49. [Google Scholar] [CrossRef]
- Al-Turki, A.; Murali, M.; Omar, A.F.; Rehan, M.; Sayyed, R.Z. Recent advances in PGPR-mediated resilience toward interactive effects of drought and salt stress in plants. Front. Microbiol. 2023, 14, 1214845. [Google Scholar] [CrossRef]
- Etesami, H.; Glick, B.R. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience. Microbiol. Res. 2024, 281, 127602. [Google Scholar] [CrossRef]
- Li, H.P.; Han, Q.Q.; Liu, Q.M.; Gan, Y.N.; Rensing, C.; Rivera, W.L.; Zhao, Q.; Zhang, J.L. Roles of phosphate-solubilizing bacteria in mediating soil legacy phosphorus availability. Microbiol. Res. 2023, 272, 127375. [Google Scholar] [CrossRef]
- Rawat, P.; Das, S.; Shankhdhar, D.; Shankhdhar, S.C. Phosphate-Solubilizing Microorganisms: Mechanism and Their Role in Phosphate Solubilization and Uptake. J. Soil Sci. Plant Nutr. 2021, 21, 49–68. [Google Scholar] [CrossRef]
- Benbrik, B.; Elabed, A.; Iraqui, M.; El Ghachtouli, N.; Douira, A.; Amir, S.; Filali-Maltouf, A.; El Abed, S.; El Modafar, C.; Ibnsouda-Koraichi, S. A phosphocompost amendment enriched with PGPR consortium enhancing plants growth in deficient soil. Commun. Soil Sci. Plant Anal. 2021, 52, 1236–1247. [Google Scholar] [CrossRef]
- Kour, D.; Rana, K.L.; Sheikh, I.; Kumar, V.; Yadav, A.N.; Dhaliwal, H.S.; Saxena, A.K. Alleviation of Drought Stress and Plant Growth Promotion by Pseudomonas libanensis EU-LWNA-33, a Drought-Adaptive Phosphorus-Solubilizing Bacterium. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2020, 90, 785–795. [Google Scholar] [CrossRef]
- Saha, I.; Datta, S.; Biswas, D. Exploring the Role of Bacterial Extracellular Polymeric Substances for Sustainable Development in Agriculture. Curr. Microbiol. 2020, 77, 3224–3239. [Google Scholar] [CrossRef] [PubMed]
- Khan, N.; Bano, A. Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 2019, 14, e0222302. [Google Scholar] [CrossRef] [PubMed]
- Naseem, H.; Bano, A.J.J.o.P.I. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J. Plant Interact. 2014, 9, 689–701. [Google Scholar] [CrossRef]
- Sarwar, S.; Khaliq, A.; Yousra, M.; Sultan, T.; Ahmad, N.; Khan, M. Screening of Siderophore-Producing PGPRs Isolated from Groundnut (Arachis hypogaea L.) Rhizosphere and Their Influence on Iron Release in Soil. Commun. Soil Sci. Plant Anal. 2020, 51, 1680–1692. [Google Scholar] [CrossRef]
- Shahid, M.; Singh, U.B.; Khan, M.S.; Singh, P.; Kumar, R.; Singh, R.N.; Kumar, A.; Singh, H.V. Bacterial ACC deaminase: Insights into enzymology, biochemistry, genetics, and potential role in amelioration of environmental stress in crop plants. Front. Microbiol. 2023, 14, 1132770. [Google Scholar] [CrossRef]
- Murali, M.; Singh, S.B.; Gowtham, H.G.; Shilpa, N.; Prasad, M.; Aiyaz, M.; Amruthesh, K.N. Induction of drought tolerance in Pennisetum glaucum by ACC deaminase producing PGPR- Bacillus amyloliquefaciens through Antioxidant defense system. Microbiol. Res. 2021, 253, 126891. [Google Scholar] [CrossRef]
- Jasim, B.; Geethu, P.R.; Mathew, J.; Radhakrishnan, E.K. Effect of endophytic Bacillus sp. from selected medicinal plants on growth promotion and diosgenin production in Trigonella foenum-graecum. Plant Cell Tissue Organ Cult. PCTOC 2015, 122, 565–572. [Google Scholar] [CrossRef]
- Liu, C.G.; Wang, Y.J.; Pan, K.W.; Zhu, T.T.; Li, W.; Zhang, L. Carbon and Nitrogen Metabolism in Leaves and Roots of Dwarf Bamboo (Fargesia denudata Yi) Subjected to Drought for Two Consecutive Years During Sprouting Period. J. Plant Growth Regul. 2014, 33, 243–255. [Google Scholar] [CrossRef]
- He, A.L.; Niu, S.Q.; Yang, D.; Ren, W.; Zhao, L.Y.; Sun, Y.Y.; Meng, L.S.; Zhao, Q.; Paré, P.W.; Zhang, J.L. Two PGPR strains from the rhizosphere of Haloxylon ammodendron promoted growth and enhanced drought tolerance of ryegrass. Plant Physiol. Biochem. 2021, 161, 74–85. [Google Scholar] [CrossRef]
- Danish, S.; Zafar-Ul-Hye, M. Co-application of ACC-deaminase producing PGPR and timber-waste biochar improves pigments formation, growth and yield of wheat under drought stress. Sci. Rep. 2019, 9, 5999. [Google Scholar] [CrossRef] [PubMed]
- Arndt, S.K.; Clifford, S.C.; Wanek, W.; Jones, H.G.; Popp, M.J.T.P. Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought stress. Tree Physiol. 2001, 21, 705. [Google Scholar] [CrossRef] [PubMed]
- Razi, K.; Muneer, S. Drought stress-induced physiological mechanisms, signaling pathways and molecular response of chloroplasts in common vegetable crops. Crit. Rev. Biotechnol. 2021, 41, 669–691. [Google Scholar] [CrossRef] [PubMed]
- Xia, Q.; He, B.; Liu, Y.; Xu, J.J.A.E.S. Effects of high temperature stress on the morphological and physiological characteristics in Scaevola albida cutting seedlings. Acta Ecol. Sin. 2010, 30, 5217–5224. [Google Scholar]
- Fahad, S.; Bajwa, A.A.; Nazir, U.; Anjum, S.A.; Farooq, A.; Zohaib, A.; Sadia, S.; Nasim, W.; Adkins, S.; Saud, S.; et al. Crop Production under Drought and Heat Stress: Plant Responses and Management Options. Front. Plant Sci. 2017, 8, 1147. [Google Scholar] [CrossRef]
- Islam, M.Z.; Park, B.J.; Jeong, S.Y.; Kang, S.W.; Shin, B.K.; Lee, Y.T. Assessment of biochemical compounds and antioxidant enzyme activity in barley and wheatgrass under water-deficit condition. J. Sci. Food Agric. 2022, 102, 1995–2002. [Google Scholar] [CrossRef]
- Khan, R.; Ma, X.; Zhang, J.; Wu, X.; Iqbal, A.; Wu, Y.; Zhou, L.; Wang, S. Circular drought-hardening confers drought tolerance via modulation of the antioxidant defense system, osmoregulation, and gene expression in tobacco. Physiol. Plant. 2021, 172, 1073–1088. [Google Scholar] [CrossRef]
- Shehata, S.A.; Omar, H.S.; Elfaidy, A.G.S.; El-Sayed, S.S.F.; Abuarab, M.E.; Abdeldaym, E.A. Grafting enhances drought tolerance by regulating stress-responsive gene expression and antioxidant enzyme activities in cucumbers. BMC Plant Biol. 2022, 22, 408. [Google Scholar] [CrossRef]
- Vurukonda, S.; Vardharajula, S.; Shrivastava, M.; SkZ, A. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 2016, 184, 13–24. [Google Scholar] [CrossRef]
- Zhang, M.; Yang, L.; Hao, R.; Bai, X.; Wang, Y.; Yu, X. Drought-tolerant plant growth-promoting rhizobacteria isolated from jujube (Ziziphus jujuba) and their potential to enhance drought tolerance. Plant Soil 2020, 452, 423–440. [Google Scholar] [CrossRef]
- Ozturk, M.; Turkyilmaz Unal, B.; García-Caparrós, P.; Khursheed, A.; Gul, A.; Hasanuzzaman, M. Osmoregulation and its actions during the drought stress in plants. Physiol. Plant. 2021, 172, 1321–1335. [Google Scholar] [CrossRef] [PubMed]
- Amna; Xia, Y.; Farooq, M.A.; Javed, M.T.; Kamran, M.A.; Mukhtar, T.; Ali, J.; Tabassum, T.; Rehman, S.U.; Munis, M.F.H.; et al. Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol. Biochem. 2020, 151, 640–649. [Google Scholar] [CrossRef] [PubMed]
- Ba, H.; Jiang, H.; Shen, P.; Cao, Y.; Li, L.J.I.C.S.E.; Science, E. Screening of Phosphate-Resolving Bacteria in Rhizosphere of Cold Sunflower and Physiological and Biochemical Study. IOP Conf. Ser. Earth Environ. Sci. 2020, 526, 012038. [Google Scholar] [CrossRef]
- Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F.J.C. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1965, 28, 350–356. [Google Scholar] [CrossRef]
- Bradford, M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Penrose, D.M.; Glick, B.R.J.P.P. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant. 2010, 118, 10–15. [Google Scholar] [CrossRef]
- Gao, H.J.; Lü, X.P.; Ren, W.; Sun, Y.Y.; Zhao, Q.; Wang, G.P.; Wang, R.J.; Wang, Y.P.; Zhang, H.; Wang, S.M.; et al. HaASR1 gene cloned from a desert shrub, Haloxylon ammodendron, confers drought tolerance in transgenic Arabidopsis thaliana. Environ. Exp. Bot. 2020, 180, 104251. [Google Scholar] [CrossRef]
Strains | Phosphorus Solubilizing | Siderophore Production | IAA Content (ΜG·mg−1) | EPS Content (Mg·mg−1) | ACC Activity (U·mg−1) |
---|---|---|---|---|---|
Control | — | — | — | — | — |
G124 | + | ++ | 0.319 | 1.238 | 0.054 |
Group | A. thaliana/M. sativa |
---|---|
CK | Normal watering |
DR | Injected with 1 mL/2 mL of distilled water |
G124 | Inoculated with 1 mL/2 mL of G124 strain suspension |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ma, X.; Zhang, B.; Xiang, X.; Li, W.; Li, J.; Li, Y.; Tran, L.-S.P.; Yin, H. Characterization of Bacillus pacificus G124 and Its Promoting Role in Plant Growth and Drought Tolerance. Plants 2024, 13, 2864. https://doi.org/10.3390/plants13202864
Ma X, Zhang B, Xiang X, Li W, Li J, Li Y, Tran L-SP, Yin H. Characterization of Bacillus pacificus G124 and Its Promoting Role in Plant Growth and Drought Tolerance. Plants. 2024; 13(20):2864. https://doi.org/10.3390/plants13202864
Chicago/Turabian StyleMa, Xiaolan, Benyin Zhang, Xin Xiang, Wenjing Li, Jiao Li, Yang Li, Lam-Son Phan Tran, and Hengxia Yin. 2024. "Characterization of Bacillus pacificus G124 and Its Promoting Role in Plant Growth and Drought Tolerance" Plants 13, no. 20: 2864. https://doi.org/10.3390/plants13202864
APA StyleMa, X., Zhang, B., Xiang, X., Li, W., Li, J., Li, Y., Tran, L.-S. P., & Yin, H. (2024). Characterization of Bacillus pacificus G124 and Its Promoting Role in Plant Growth and Drought Tolerance. Plants, 13(20), 2864. https://doi.org/10.3390/plants13202864