Engineering the Rhizosphere Microbiome with Plant Growth Promoting Bacteria for Modulation of the Plant Metabolome
Abstract
:1. Introduction
2. Results
2.1. Plant Biochemical Profile—Microcosm Experiments
2.2. Plant Biochemical Profile—Field Experiments
3. Discussion
3.1. Metabolic Shifts and Plant Growth
3.2. Metabolic Shifts and Stress Tolerance
3.3. Biostimulation of Salicornia europaea with PGPB: Implications for Economic Value
4. Materials and Methods
4.1. Reagents
4.2. Plant Inoculation and Growth
4.3. Sample Preparation for Phytochemical Analyses
4.4. Silylation and Gas-Chromatography–Mass-Spectrometry (GC–MS) Analysis
4.5. Extraction and Ultra-High-Performance Liquid-Chromatography–Mass-Spectrometry (UHPLC–MS) Analysis
4.6. Statistical Analyses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Vandenkoornhuyse, P.; Quaiser, A.; Duhamel, M.; Le Van, A.; Dufresne, A. The importance of the microbiome of the plant holobiont. New Phytol. 2015, 206, 1196–1206. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Llorente, I.D.; Pajuelo, E.; Navarro-Torre, S.; Mesa-Marín, J.; Caviedes, M.A. Bacterial Endophytes from Halophytes: How Do They Help Plants to Alleviate Salt Stress? In Saline Soil-Based Agriculture by Halotolerant Microorganisms; Springer: Berlin/Heidelberg, Germany, 2019; pp. 147–160. [Google Scholar] [CrossRef]
- Mesa-Marín, J.; Pérez-Romero, J.A.; Mateos-Naranjo, E.; Bernabeu-Meana, M.; Pajuelo, E.; Rodríguez-Llorente, I.D.; Redondo-Gómez, S. Effect of plant growth-promoting rhizobacteria on salicornia ramosissima seed germination under salinity, CO2 and temperature stress. Agronomy 2019, 9, 655. [Google Scholar] [CrossRef]
- Stanković, M.; Stojanović-Radić, Z.; Jakovljević, D.; Zlatić, N.; Luković, M.; Dajić-Stevanović, Z. Coastal Halophytes: Potent Source of Bioactive Molecules from Saline Environment. Plants 2023, 12, 1857. [Google Scholar] [CrossRef] [PubMed]
- Hameed, A.; Hussain, S.; Rasheed, A.; Ahmed, M.Z.; Abbas, S. Exploring the Potentials of Halophytes in Addressing Climate Change-Related Issues: A Synthesis of Their Biological, Environmental, and Socioeconomic Aspects. World 2024, 5, 36–57. [Google Scholar] [CrossRef]
- Ruiu, L. Plant-Growth-Promoting Bacteria (PGPB) against Insects and Other Agricultural Pests. Agronomy 2020, 10, 861. [Google Scholar] [CrossRef]
- Ali, S.; Charles, T.C.; Glick, B.R. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol. Biochem. 2014, 80, 160–167. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, M.J.; Sierra-Garcia, I.N.; Cremades, J.; António, C.; Rodrigues, A.M.; Pinto, D.C.G.A.; Silva, H.; Cunha, Â. Biostimulation of Salicornia europaea L. crops with plant-growth-promoting bacteria in laboratory and field conditions: Effects on growth and metabolite profile. J. Appl. Microbiol. 2023, 134, lxad036. [Google Scholar] [CrossRef] [PubMed]
- Nephali, L.; Piater, L.A.; Dubery, I.A.; Patterson, V.; Huyser, J.; Burgess, K.; Tugizimana, F. Biostimulants for plant growth and mitigation of abiotic stresses: A metabolomics perspective. Metabolites 2020, 10, 505. [Google Scholar] [CrossRef] [PubMed]
- Díaz Herrera, S.; Grossi, C.; Zawoznik, M.; Groppa, M.D. Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol. Res. 2016, 186–187, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Abdelshafy Mohamad, O.A.; Ma, J.-B.; Liu, Y.-H.; Zhang, D.; Hua, S.; Bhute, S.; Hedlund, B.P.; Li, W.-J.; Li, L. Beneficial Endophytic Bacterial Populations Associated with Medicinal Plant Thymus vulgaris Alleviate Salt Stress and Confer Resistance to Fusarium oxysporum. Front. Plant Sci. 2020, 11, 47. [Google Scholar] [CrossRef] [PubMed]
- Poria, V.; Dębiec-Andrzejewska, K.; Fiodor, A.; Lyzohub, M.; Ajijah, N.; Singh, S.; Pranaw, K. Plant Growth-Promoting Bacteria (PGPB) integrated phytotechnology: A sustainable approach for remediation of marginal lands. Front. Plant Sci. 2022, 13, 999866. [Google Scholar] [CrossRef] [PubMed]
- Mokrani, S.; Nabti, E.; Cruz, C. Recent Trends in Microbial Approaches for Soil Desalination. Appl. Sci. 2022, 12, 3586. [Google Scholar] [CrossRef]
- Alves, N.S.F.; Kaory Inoue, S.G.; Carneiro, A.R.; Albino, U.B.; Setzer, W.N.; Maia, J.G.; Andrade, E.H.; da Silva, J.K.R. Variation in Peperomia pellucida growth and secondary metabolism after rhizobacteria inoculation. PLoS ONE 2022, 17, e0262794. [Google Scholar] [CrossRef]
- Wang, J.; Zhao, H.; Chen, T.; Lin, W.; Lin, S. Effect of Burkholderia ambifaria LK-P4 inoculation on the plant growth characteristics, metabolism, and pharmacological activity of Anoectochilus roxburghii. Front. Plant Sci. 2022, 13, 1043042. [Google Scholar] [CrossRef] [PubMed]
- Mhlongo, M.I.; Piater, L.A.; Steenkamp, P.A.; Labuschagne, N.; Dubery, I.A. Metabolic Profiling of PGPR-Treated Tomato Plants Reveal Priming-Related Adaptations of Secondary Metabolites and Aromatic Amino Acids. Metabolites 2020, 10, 210. [Google Scholar] [CrossRef] [PubMed]
- Mashabela, M.D.; Tugizimana, F.; Steenkamp, P.A.; Piater, L.A.; Dubery, I.A.; Terefe, T.; Mhlongo, M.I. Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust). Front. Plant Sci. 2023, 14, 1103413. [Google Scholar] [CrossRef] [PubMed]
- Alzate Zuluaga, M.Y.; Milani, K.M.L.; Miras-Moreno, M.B.; Lucini, L.; Valentinuzzi, F.; Mimmo, T.; Pii, Y.; Cesco, S.; Rodrigues, E.P.; de Oliveira, A.L.M. The adaptive metabolomic profile and functional activity of tomato rhizosphere are revealed upon PGPB inoculation under saline stress. Environ. Exp. Bot. 2021, 189, 104552. [Google Scholar] [CrossRef]
- Vaishnav, A.; Kumari, S.; Jain, S.; Varma, A.; Tuteja, N.; Choudhary, D.K. PGPR-mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J. Basic Microbiol. 2016, 56, 1274–1288. [Google Scholar] [CrossRef] [PubMed]
- Rahman, M.; Rahman, M.; Sabir, A.A.; Mukta, J.A.; Khan, M.M.A.; Mohi-Ud-Din, M.; Miah, M.G.; Islam, M.T. Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Sci. Rep. 2018, 8, 2504. [Google Scholar] [CrossRef] [PubMed]
- Chamam, A.; Sanguin, H.; Bellvert, F.; Meiffren, G.; Comte, G.; Wisniewski-Dyé, F.; Bertrand, C.; Prigent-Combaret, C. Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemistry 2013, 87, 65–77. [Google Scholar] [CrossRef] [PubMed]
- Pang, Z.; Chen, J.; Wang, T.; Gao, C.; Li, Z.; Guo, L.; Xu, J.; Cheng, Y. Linking Plant Secondary Metabolites and Plant Microbiomes: A Review. Front. Plant Sci. 2021, 12, 621276. [Google Scholar] [CrossRef] [PubMed]
- Santhoshkumar, R.; Akash, P.; Viswam, P.; Soniya, E.V. Imprints of PGPB association on the metabolic dynamism of Piper nigrum. J. Plant Interact. 2022, 17, 967–979. [Google Scholar] [CrossRef]
- Putra, A.M.; Anastasya, N.A.; Rachmawati, S.W.; Yusnawan, E.; Syibli, M.A.; Trianti, I.; Setiawan, A.; Aini, L.Q. Growth performance and metabolic changes in lettuce inoculated with plant growth promoting bacteria in a hydroponic system. Sci. Hortic. 2024, 327, 112868. [Google Scholar] [CrossRef]
- Solomon, W.; Janda, T.; Molnár, Z. Unveiling the significance of rhizosphere: Implications for plant growth, stress response, and sustainable agriculture. Plant Physiol. Biochem. 2024, 206, 108290. [Google Scholar] [CrossRef] [PubMed]
- Abdelaal, K.; Alkahtani, M.; Attia, K.; Hafez, Y.; Király, L.; Künstler, A. The role of plant growth-promoting bacteria in alleviating the adverse effects of drought on plants. Biology 2021, 10, 520. [Google Scholar] [CrossRef] [PubMed]
- Gupta, S.; Schillaci, M.; Roessner, U. Metabolomics as an emerging tool to study plant-microbe interactions. Emerg. Top. Life Sci. 2022, 6, 175–183. [Google Scholar] [CrossRef] [PubMed]
- Jerónimo, D.; Lillebø, A.I.; Cremades, J.; Cartaxana, P.; Calado, R. Recovering wasted nutrients from shrimp farming through the combined culture of polychaetes and halophytes. Sci. Rep. 2021, 11, 6587. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.; Lee, E.Y.; Hillman, P.F.; Ko, J.; Yang, I.; Nam, S.J. Chemical structure and biological activities of secondary metabolites from Salicornia europaea L. Molecules 2021, 26, 2252. [Google Scholar] [CrossRef]
- Hulkko, L.S.S.; Rocha, R.M.; Trentin, R.; Fredsgaard, M.; Chaturvedi, T.; Custódio, L.; Thomsen, M.H. Bioactive Extracts from Salicornia ramosissima J. Woods Biorefinery as a Source of Ingredients for High-Value Industries. Plants 2023, 12, 1251. [Google Scholar] [CrossRef] [PubMed]
- Giordano, R.; Aliotta, G.E.; Johannesen, A.S.; Voetmann-Jensen, D.; Laustsen, F.H.; Andersen, L.A.; Rezai, A.; Fredsgaard, M.; Lo Vecchio, S.; Arendt-Nielsen, L.; et al. Effects of Salicornia-Based Skin Cream Application on Healthy Humans’ Experimental Model of Pain and Itching. Pharmaceuticals 2022, 15, 150. [Google Scholar] [CrossRef] [PubMed]
- Giordano, R.; Saii, Z.; Fredsgaard, M.; Hulkko, L.S.S.; Poulsen, T.B.G.; Thomsen, M.E.; Henneberg, N.; Zucolotto, S.M.; Arendt-Nielsen, L.; Papenbrock, J.; et al. Pharmacological insights into halophyte bioactive extract action on anti-inflammatory, pain relief and antibiotics-type mechanisms. Molecules 2021, 26, 3140. [Google Scholar] [CrossRef]
- Sierra-García, I.N.; Ferreira, M.J.; Torres-Ballesteros, A.; Louvado, A.; Gomes, N.; Cunha, A. Brevibacterium EB3 inoculation enhances rhizobacterial community interactions leading to improved growth of Salicornia europaea. Appl. Soil Ecol. 2024, 196, 105306. [Google Scholar] [CrossRef]
- Balasubramaniam, T.; Shen, G.; Esmaeili, N.; Zhang, H. Plants’ Response Mechanisms to Salinity Stress. Plants 2023, 12, 2253. [Google Scholar] [CrossRef]
- Ferreira, M.J.; Cunha, A.; Figueiredo, S.; Faustino, P.; Patinha, C.; Silva, H.; Sierra-Garcia, I.N. The root microbiome of salicornia ramosissima as a seedbank for plant-growth promoting halotolerant bacteria. Appl. Sci. 2021, 11, 2233. [Google Scholar] [CrossRef]
- Morkunas, I.; Ratajczak, L. The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol. Plant. 2014, 36, 1607–1619. [Google Scholar] [CrossRef]
- Gómez-Ariza, J.; Campo, S.; Rufat, M.; Estopà, M.; Messeguer, J.; San Segundo, B.; Coca, M. Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol. Plant-Microbe Interact. 2007, 20, 832–842. [Google Scholar] [CrossRef]
- Lacrampe, N.; Lopez-Lauri, F.; Lugan, R.; Colombié, S.; Olivares, J.; Nicot, P.C.; Lecompte, F. Regulation of sugar metabolism genes in the nitrogen-dependent susceptibility of tomato stems to Botrytis cinerea. Ann. Bot. 2021, 127, 143–154. [Google Scholar] [CrossRef] [PubMed]
- Stein, O.; Granot, D. An overview of sucrose synthases in plants. Front. Plant Sci. 2019, 10, 95. [Google Scholar] [CrossRef]
- Jeandet, P.; Formela-Luboińska, M.; Labudda, M.; Morkunas, I. The Role of Sugars in Plant Responses to Stress and Their Regulatory Function during Development. Int. J. Mol. Sci. 2022, 23, 5161. [Google Scholar] [CrossRef]
- Ohto, M.A.; Onai, K.; Furukawa, Y.; Aoki, E.; Araki, T.; Nakamura, K. Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol. 2001, 127, 252–261. [Google Scholar] [CrossRef] [PubMed]
- Gouffi, K.; Pica, N.; Pichereau, V.; Blanco, C. Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl. Environ. Microbiol. 1999, 65, 1491–1500. [Google Scholar] [CrossRef] [PubMed]
- O’Hara, L.E.; Paul, M.J.; Wingler, A. How Do Sugars Regulate Plant Growth and Development? New Insight into the Role of Trehalose-6-Phosphate. Mol. Plant 2013, 6, 261–274. [Google Scholar] [CrossRef] [PubMed]
- Zhu, G.-Y.; Geuns, J.M.C.; Dussert, S.; Swennen, R.; Panis, B. Change in sugar, sterol and fatty acid composition in banana meristems caused by sucrose-induced acclimation and its effects on cryopreservation. Physiol. Plant. 2006, 128, 80–94. [Google Scholar] [CrossRef]
- Morkunas, I.; Bednarski, W.; Kozłowska, M. Response of embryo axes of germinating seeds of yellow lupine to Fusarium oxysporum. Plant Physiol. Biochem. 2004, 42, 493–499. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.H.; Yoo, S.D. Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet. 2011, 7, e1001263. [Google Scholar] [CrossRef] [PubMed]
- Siddiqui, H.; Sami, F.; Hayat, S. Glucose: Sweet or bitter effects in plants-a review on current and future perspective. Carbohydr. Res. 2020, 487, 107884. [Google Scholar] [CrossRef] [PubMed]
- Hulkko, L.S.S.; Turcios, A.E.; Kohnen, S.; Chaturvedi, T.; Papenbrock, J.; Thomsen, M.H. Cultivation and characterisation of Salicornia europaea, Tripolium pannonicum and Crithmum maritimum biomass for green biorefinery applications. Sci. Rep. 2022, 12, 20507. [Google Scholar] [CrossRef] [PubMed]
- Walker, V.; Couillerot, O.; von Felten, A.; Bellvert, F.; Jansa, J.; Maurhofer, M.; Bally, R.; Moënne-Loccoz, Y.; Comte, G. Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 2012, 356, 151–163. [Google Scholar] [CrossRef]
- Walker, V.; Bertrand, C.; Bellvert, F.; Moënne-Loccoz, Y.; Bally, R.; Comte, G. Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum. New Phytol. 2011, 189, 494–506. [Google Scholar] [CrossRef] [PubMed]
- Han, Q.Q.; Lü, X.P.; Bai, J.P.; Qiao, Y.; Paré, P.W.; Wang, S.M.; Zhang, J.L.; Wu, Y.N.; Pang, X.P.; Xu, W.B.; et al. Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover. Front. Plant Sci. 2014, 5, 525. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Liu, Y.; Wu, G.; Veronican Njeri, K.; Shen, Q.; Zhang, N.; Zhang, R. Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol. Plant. 2016, 158, 34–44. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.-M.; Shahzad, R.; Bilal, S.; Khan, A.L.; Park, Y.-G.; Lee, K.-E.; Asaf, S.; Khan, M.A.; Lee, I.-J. Indole-3-acetic-acid and ACC deaminase producing Leclercia adecarboxylata MO1 improves Solanum lycopersicum L. growth and salinity stress tolerance by endogenous secondary metabolites regulation. BMC Microbiol. 2019, 19, 80. [Google Scholar] [CrossRef] [PubMed]
- Sunita, K.; Mishra, I.; Mishra, J.; Prakash, J.; Arora, N.K. Secondary Metabolites from Halotolerant Plant Growth Promoting Rhizobacteria for Ameliorating Salinity Stress in Plants. Front. Microbiol. 2020, 11, 567768. [Google Scholar] [CrossRef] [PubMed]
- Aluko, O.O.; Li, C.; Wang, Q.; Liu, H. Sucrose utilization for improved crop yields: A review article. Int. J. Mol. Sci. 2021, 22, 4704. [Google Scholar] [CrossRef] [PubMed]
- de Faria, R.T.; Rodrigues, F.N.; do V., R. Oliveira, L.; Müller, C. In vitro Dendrobium nobile plant growth and rooting in different sucrose concentrations. Hortic. Bras. 2004, 22, 780–783. [Google Scholar] [CrossRef]
- Bonaventure, G.; Salas, J.J.; Pollard, M.R.; Ohlrogge, J.B. Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 2003, 15, 1020–1033. [Google Scholar] [CrossRef] [PubMed]
- Singh, P.; Arif, Y.; Bajguz, A.; Hayat, S. The role of quercetin in plants. Plant Physiol. Biochem. 2021, 166, 10–19. [Google Scholar] [CrossRef] [PubMed]
- Zuluaga, M.Y.A.; Milani, K.M.L.; Miras-Moreno, B.; Lucini, L.; Valentinuzzi, F.; Mimmo, T.; Pii, Y.; Cesco, S.; Rodrigues, E.P.; de Oliveira, A.L.M. Inoculation with plant growth-promoting bacteria alters the rhizosphere functioning of tomato plants. Appl. Soil Ecol. 2021, 158, 103784. [Google Scholar] [CrossRef]
- Peer, W.A.; Murphy, A.S. Flavonoids and auxin transport: Modulators or regulators? Trends Plant Sci. 2007, 12, 556–563. [Google Scholar] [CrossRef] [PubMed]
- Hann, E.C.; Overa, S.; Harland-Dunaway, M.; Narvaez, A.F.; Le, D.N.; Orozco-Cárdenas, M.L.; Jiao, F.; Jinkerson, R.E. A hybrid inorganic–biological artificial photosynthesis system for energy-efficient food production. Nat. Food 2022, 3, 461–471. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.-C.; Zhang, S.-L.; Wu, K.-J.; Li, R.; He, X.-R.; He, D.-N.; Huang, C.; Wei, H. The effects of exogenous organic acids on the growth, photosynthesis and cellular ultrastructure of Salix variegata Franch. Under Cd stress. Ecotoxicol. Environ. Saf. 2020, 187, 109790. [Google Scholar] [CrossRef] [PubMed]
- Rekha, K.; Baskar, B.; Srinath, S.; Usha, B. Plant-growth-promoting rhizobacteria Bacillus subtilis RR4 isolated from rice rhizosphere induces malic acid biosynthesis in rice roots. Can. J. Microbiol. 2018, 27, 20–27. [Google Scholar] [CrossRef] [PubMed]
- De Boeck, H.J.; Vicca, S.; Roy, J.; Nijs, I.; Milcu, A.; Kreyling, J.; Jentsch, A.; Chabbi, A.; Campioli, M.; Callaghan, T.; et al. Global Change Experiments: Challenges and Opportunities. Bioscience 2015, 65, 922–931. [Google Scholar] [CrossRef]
- He, M.; Ding, N.Z. Plant Unsaturated Fatty Acids: Multiple Roles in Stress Response. Front. Plant Sci. 2020, 11, 562785. [Google Scholar] [CrossRef] [PubMed]
- Ayala, A.; Muñoz, M.F.; Argüelles, S. Lipid Peroxidation: Production, Metabolism, and Signaling Mechanisms of Malondialdehyde and 4-Hydroxy-2-Nonenal. Oxidative Med. Cell. Longev. 2014, 2014, 360438. [Google Scholar] [CrossRef] [PubMed]
- Magni, N.N.; Veríssimo, A.C.S.; Silva, H.; Pinto, D.C.G.A. Metabolomic Profile of Salicornia perennis Plant’s Organs under Diverse In Situ Stress: The Ria de Aveiro Salt Marshes Case. Metabolites 2023, 13, 280. [Google Scholar] [CrossRef] [PubMed]
- Ali, M.S.; Baek, K.H. Jasmonic acid signaling pathway in response to abiotic stresses in plants. Int. J. Mol. Sci. 2020, 21, 621. [Google Scholar] [CrossRef] [PubMed]
- Rehman, M.; Saeed, M.S.; Fan, X.; Salam, A.; Munir, R.; Yasin, M.U.; Khan, A.R.; Muhammad, S.; Ali, B.; Ali, I.; et al. The Multifaceted Role of Jasmonic Acid in Plant Stress Mitigation: An Overview. Plants 2023, 12, 3982. [Google Scholar] [CrossRef] [PubMed]
- Mathesius, U. Flavonoid functions in plants and their interactions with other organisms. Plants 2018, 7, 30. [Google Scholar] [CrossRef] [PubMed]
- Laoué, J.; Fernandez, C.; Ormeño, E. Plant Flavonoids in Mediterranean Species: A Focus on Flavonols as Protective Metabolites under Climate Stress. Plants 2022, 11, 172. [Google Scholar] [CrossRef] [PubMed]
- Ameixa, O.M.C.C.; Rebelo, J.; Silva, H.; Pinto, D.C.G.A. Gall midge Baldratia salicorniae Kieffer (Diptera: Cecidomyiidae) infestation on Salicornia europaea L. induces the production of specialized metabolites with biotechnological potential. Phytochemistry 2022, 200, 113207. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Beisson, F.; Ohlrogge, J.; Pollard, M. Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin-associated acyltransferase. Plant Physiol. 2007, 144, 1267–1277. [Google Scholar] [CrossRef] [PubMed]
- Deng, Y.; Lu, S. Biosynthesis and Regulation of Phenylpropanoids in Plants. CRC Crit. Rev. Plant Sci. 2017, 36, 257–290. [Google Scholar] [CrossRef]
- Ferreira, M.J.; Sierra-Garcia, I.N.; Louvado, A.; Gomes, N.C.M.; Figueiredo, S.; Patinha, C.; Pinto, D.C.G.A.; Cremades, J.; Silva, H.; Cunha, Â. Domestication shapes the endophytic microbiome and metabolome of Salicornia europaea. J. Appl. Microbiol. 2023, 134, lxad178. [Google Scholar] [CrossRef] [PubMed]
- Lephatsi, M.; Nephali, L.; Meyer, V.; Piater, L.A.; Buthelezi, N.; Dubery, I.A.; Opperman, H.; Brand, M.; Huyser, J.; Tugizimana, F. Molecular mechanisms associated with microbial biostimulant-mediated growth enhancement, priming and drought stress tolerance in maize plants. Sci. Rep. 2022, 12, 10450. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, M.J.; Pinto, D.C.G.A.; Cunha, Â.; Silva, H. Halophytes as Medicinal Plants against Human Infectious Diseases. Appl. Sci. 2022, 12, 7493. [Google Scholar] [CrossRef]
- Patel, S. Salicornia: Evaluating the halophytic extremophile as a food and a pharmaceutical candidate. 3 Biotech 2016, 6, 104. [Google Scholar] [CrossRef] [PubMed]
- Cárdenas-Pérez, S.; Rajabi Dehnavi, A.; Leszczyński, K.; Lubińska-Mielińska, S.; Ludwiczak, A.; Piernik, A. Salicornia europaea L. Functional Traits Indicate Its Optimum Growth. Plants 2022, 11, 1051. [Google Scholar] [CrossRef] [PubMed]
- Sun, W.; Shahrajabian, M.H. Therapeutic Potential of Phenolic Compounds in Medicinal Plants—Natural Health Products for Human Health. Molecules 2023, 28, 1845. [Google Scholar] [CrossRef] [PubMed]
- Kumar, N.; Goel, N. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnol. Rep. 2019, 24, e00370. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Li, J.; Zhang, X.; Zu, Y.; Yang, Y.; Liu, W.; Xu, Z.; Gao, H.; Sun, X.; Jiang, X.; et al. Current Advances in Naturally Occurring Caffeoylquinic Acids: Structure, Bioactivity, and Synthesis. J. Agric. Food Chem. 2020, 68, 10489–10516. [Google Scholar] [CrossRef] [PubMed]
- Hur, S.; Park, G.; Joo, S.-T. Biological activities of conjugated linoleic acid (CLA) and effects of CLA on animal products. Livest. Sci. 2007, 110, 221–229. [Google Scholar] [CrossRef]
- Natali, F.; Siculella, L.; Salvati, S.; Gnoni, G. V Oleic acid is a potent inhibitor of fatty acid and cholesterol synthesis in C6 glioma cells. J. Lipid Res. 2007, 48, 1966–1975. [Google Scholar] [CrossRef] [PubMed]
- Dilika, F.; Bremner, P.D.; Meyer, J.J.M. Antibacterial activity of linoleic and oleic acids isolated from Helichrysum pedunculatum: A plant used during circumcision rites. Fitoterapia 2000, 71, 450–452. [Google Scholar] [CrossRef] [PubMed]
- Kusumah, D.; Wakui, M.; Murakami, M.; Xie, X.; Yukihito, K.; Maeda, I. Linoleic acid, α-linolenic acid, and monolinolenins as antibacterial substances in the heat-processed soybean fermented with Rhizopus oligosporus. Biosci. Biotechnol. Biochem. 2020, 84, 1285–1290. [Google Scholar] [CrossRef] [PubMed]
- Zheng, C.J.; Yoo, J.-S.; Lee, T.-G.; Cho, H.-Y.; Kim, Y.-H.; Kim, W.-G. Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Lett. 2005, 579, 5157–5162. [Google Scholar] [CrossRef] [PubMed]
- Kolar, M.J.; Konduri, S.; Chang, T.; Wang, H.; McNerlin, C.; Ohlsson, L.; Härröd, M.; Siegel, D.; Saghatelian, A. Linoleic acid esters of hydroxy linoleic acids are anti-inflammatory lipids found in plants and mammals. J. Biol. Chem. 2019, 294, 10698–10707. [Google Scholar] [CrossRef] [PubMed]
- Youssef, A.M.M.; Maaty, D.A.M.; Al-Saraireh, Y.M. Phytochemical Analysis and Profiling of Antitumor Compounds of Leaves and Stems of Calystegia silvatica (Kit.) Griseb. Molecules 2023, 28, 630. [Google Scholar] [CrossRef] [PubMed]
- Novotny, L.; Mahmoud, F.; Abdel-Hamid, M.; Hunakova, L. Anticancer potential of β-sitosterol. Int. J. Clin. Pharmacol. Pharmacother. 2017, 2, 2456–3501. [Google Scholar] [CrossRef] [PubMed]
- Shankar, E.; Goel, A.; Gupta, K.; Gupta, S. Plant Flavone Apigenin: An Emerging Anticancer Agent. Curr. Pharmacol. Reports 2017, 3, 423–446. [Google Scholar] [CrossRef] [PubMed]
- Tian, J.; Wang, X.-Q.; Tian, Z. Focusing on Formononetin: Recent Perspectives for its Neuroprotective Potentials. Front. Pharmacol. 2022, 13, 905898. [Google Scholar] [CrossRef] [PubMed]
- Di Rienzo, J.A.; Casanoves, F.; Balzarini, M.; Gonzalez, L.; Tablada, M.; Robledo, C.W. “INFOSTAT.” Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. 2020.
- Hammer, Ø.; Harper, D.A.T.; Ryan, P.D. Past: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4, 11. [Google Scholar]
- El-Sayed, M.A.; Abbas, F.A.; Refaat, S.; El-Shafae, A.M.; Fikry, E. UPLC-ESI-MS/MS Profile of the Ethyl Acetate Fraction of Aerial Parts of Bougainvillea “scarlett o’hara” Cultivated in Egypt. Egypt. J. Chem. 2021, 64, 793–806. [Google Scholar] [CrossRef]
- Ivan, I.; Jungfer, E.; Ritter, C.; Santiago-schübel, B.; Thiele, B.; Fett, R.; Galensa, R. Characterization of Fl Avan-3-Ols in Seeds of Grape Pomace by CE, HPLC-DAD-MS n and LC-ESI-FTICR-MS. FRIN 2012, 48, 848–855. [Google Scholar] [CrossRef]
- Llorent-Martínez, E.J.; Gouveia, S.; Castilho, P.C. Analysis of Phenolic Compounds in Leaves from Endemic Trees from Madeira Island. A Contribution to the Chemotaxonomy of Laurisilva Forest Species. Ind. Crops Prod. 2015, 64, 135–151. [Google Scholar] [CrossRef]
- Clifford, M.N.; Johnston, K.L.; Knight, S.; Kuhnert, N. Hierarchical Scheme for LC-MSn Identification of Chlorogenic Acids. J. Agric. Food Chem. 2003, 51, 2900–2911. [Google Scholar] [CrossRef] [PubMed]
- Llorent-Martinez, E.J.; Spinola, V.; Gouveia, S.; Castilho, P.C. HPLC-ESI-MSn Characterization of Phenolic Compounds, Terpenoid Saponins, and Other Minor Compounds in Bituminaria Bituminosa. Ind. Crops Prod. 2015, 69, 80–90. [Google Scholar] [CrossRef]
- Singh, A.; Kumar, S.; Kumar, B. LC-MS Identification of Proanthocyanidins in Bark and Fruit of Six Terminalia Species. Nat. Prod. Commun. 2018, 13, 555–560. [Google Scholar] [CrossRef]
- Di Lecce, G.; Arranz, S.; Jáuregui, O.; Tresserra-Rimbau, A.; Quifer-Rada, P.; Lamuela-Raventós, R.M. Phenolic Profiling of the Skin, Pulp and Seeds of Albariño Grapes Using Hybrid Quadrupole Time-of-Flight and Triple-Quadrupole Mass Spectrometry. Food Chem. 2014, 145, 874–882. [Google Scholar] [CrossRef]
- Clifford, M.N.; Knight, S.; Kuhnert, N. Discriminating between the Six Isomers of Dicaffeoylquinic Acid by LC-MSn. J. Agric. Food Chem. 2005, 53, 3821–3832. [Google Scholar] [CrossRef]
- Zhang, Y.; Xiong, H.; Xu, X.; Xue, X.; Liu, M.; Xu, S.; Liu, H.; Gao, Y.; Zhang, H.; Li, X. Compounds Identification in Semen Cuscutae by Ultra-High-Performance Liquid Chromatography (Uplcs) Coupled to Electrospray Ionization Mass Spectrometry. Molecules 2018, 23, 1199. [Google Scholar] [CrossRef] [PubMed]
- Gouveia, S.; Castilho, P.C. Characterisation of Phenolic Acid Derivatives and Flavonoids from Different Morphological Parts of Helichrysum obconicum by a RP-HPLC-DAD-(−)-ESI-MSn Method. Food Chem. 2011, 129, 333–344. [Google Scholar] [CrossRef] [PubMed]
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
Ferreira, M.J.; Veríssimo, A.C.S.; Pinto, D.C.G.A.; Sierra-Garcia, I.N.; Granada, C.E.; Cremades, J.; Silva, H.; Cunha, Â. Engineering the Rhizosphere Microbiome with Plant Growth Promoting Bacteria for Modulation of the Plant Metabolome. Plants 2024, 13, 2309. https://doi.org/10.3390/plants13162309
Ferreira MJ, Veríssimo ACS, Pinto DCGA, Sierra-Garcia IN, Granada CE, Cremades J, Silva H, Cunha Â. Engineering the Rhizosphere Microbiome with Plant Growth Promoting Bacteria for Modulation of the Plant Metabolome. Plants. 2024; 13(16):2309. https://doi.org/10.3390/plants13162309
Chicago/Turabian StyleFerreira, Maria J., Ana C. S. Veríssimo, Diana C. G. A. Pinto, Isabel N. Sierra-Garcia, Camille E. Granada, Javier Cremades, Helena Silva, and Ângela Cunha. 2024. "Engineering the Rhizosphere Microbiome with Plant Growth Promoting Bacteria for Modulation of the Plant Metabolome" Plants 13, no. 16: 2309. https://doi.org/10.3390/plants13162309