Bioprocess of Gibberellic Acid by Fusarium fujikuroi: The Challenge of Regulation, Raw Materials, and Product Yields
Abstract
:1. Introduction
2. Bakanae: From the Problem to the Opportunity
3. Fusarium fujikuroi as the Main GA3 Producer
4. Gibberellic Acid (GA3)
5. Effects of GA3 on Crops
6. GA3 Biosynthesis Regulation
7. GA3 Production
Microorganism | Substrate | Cultivation Strategy | Operation Conditions | Production (g/L) Productivity (g/L/day) | Ref. |
---|---|---|---|---|---|
G. fujikuroi CDBB H-984 | Rice flour 2 g/L Glucose 100 g/L | Fluidized immobilized mycelium Optimization temperature, pH and C:N ratio | Batch fluidized bioreactor (3.5 L) C:N 36.8 pH 5 30 °C 3 vvm 8 days | Around 3900 mg/L 487.50 mg/L/day | [8] |
G. fujikuroi NRRL 2278 | Glucose 40 g/L 30% raw rice bran/70% barley malt residue | SSF 2 Agro-industrial wastes from rice processing and brewing industry | Batch flask (50 g in 400 mL) 28 °C pH 5–5.5 70% moisture 7 days | 10,100 mg/kg 1442.85 mg/kg/day | [7] |
F. moniliforme LPB03 | Citric pulp 30 g | Different fermentation systems SSSF 1, SSF 2 and SmF 3 | Column bioreactor (30 g in 0.25 L) 75% moisture 30 mL/min air pH 5.5–5.8 29 °C 5 days | SSF 2 results: 7340 mg/kg 1468 mg/kg/day | [71] |
F. moniliforme M-7121 | Starch maize flour 800 g Wheat bran 200 g | SSF 2 Optimization moisture, water activity | Batch drum reactors (3 L) 60% initial moisture 28 °C Initial pH 5 12 days | 21,000 mg/kg 1750 mg/kg/day | [70] |
F. moniliforme NCIM 1100 | SmF 3: sucrose, 30 g/L SSF 2: jatropha seed cake, 5 g | SSF 2 and SmF 3 | Batch flask SmF 3: 30 °C 10 days 150 rpm Monitored 1 day Batcha flask SSF 2: 30–45 °C 10 days Monitored 2 days | SmF 3: 15,000 mg/L 1500 mg/L/day SSF 2: 10,500 mg/kg 1050 mg/kg/day | [79] |
G. fujikuroi DMS 893 | Glucose 120 g/L Glycine 4 g/L | Extractive SmF 3 Genapol 2822 | Fed-batch Bioreactor (6 L) 29 °C 0.8 vvm 400 rpm 20.83 days | 1050 mg/L 50.40 mg/L/day | [74] |
G. fujikuroi NRRL 5538 | Cassava flour | SSF 2 Different support (cassava flour, sugar cane bagasse and low density polyurethane) | Column fermenter (20 g cassava) 29 °C 1.5 days | 250 mg/kg 166.67 mg/kg/day | [83] |
G. fujikuroi NRRL 2284 | Glucose 80 g/L | SmF 3 Effect of C:N ratio 7.97–796.8 | Batch Fermenter (1.8 in 3 L) C:N 122 pH 5 700 rpm 30 °C 1 vvm 7.08 days | 1000 mg/L 141.24 mg/L/day | [78] |
G. fujikuroi CDBB H-984 | Glucose 50 g/L | SmF 3 Kinetic model simulation | Airlift bioreactor (3.5 L) pH 3 29 °C 1.6 vvm Around 12 days | Around 100 ppm 8.3 ppm/day | [76] |
G. fujikuroi CDBB H-984 | Glucose-corn oil | SmF 3 Mixture of carbon source | Batch bioreactor (7 L) pH 3.5 29 °C 600 rpm 1 vvm 12 days | 380 mg/L 31.67 mg/L/day | [58] |
G. fujikuroi LPB 06 | Citrus pulp Soybean hulls (5%) | SmF 3 Agroindustrial wastes, citrus pulp and soybean hulls | Stirred tank reactor (2 L) 29 °C 0.5 vvm 500 rpm 4 days | 205.2 mg/L 51.3 mg/L/day | [84] |
G. fujikuroi CDBB H-984 | Glucose Corn oil | SmF 3 Mixture carbon source | Batch bioreactor (7 L) pH 3.5 29 °C 600 rpm 1 vvm 15 days | 430 mg/L 28.3 mg/L/day | [85] |
F. moniliforme LPB06 | Coffee husk 10 g Cassava bagasse | SSF 2 Strain selection | Batch flask (10 g in 250 mL) pH 5.3 70% moisture 29 °C 7 days | 492.5 mg/kg 70.36 mg/kg/day | [86] |
Aspergillus niger | Czapek-Dox broth | SmF 3 Optimization of incubation time, temperature, pH, agitation. | Batch flask (100 mL in 250 mL) 30 °C pH 5 150 rpm 12 days | 238.7 mg/L 19.89 mg/L/day | [61] |
Aspergillus niger FüRSAN | Molasses | SmF 3 Food industry wastes (molasses, vinasse, whey, suger-beet) | Batch flask 30 °C 12 days 150 rpm | 155 mg/L 12.92 mg/L/day | [62] |
Penicillium variable | Banana peel Sucrose 2% | SSF 2 Olive oil as natural precursor | Static flask reactor 27 °C pH 5 7 days | 31.95 mg/kg 4.56 mg/kg/day | [63] |
Inonotus hipidus | Sucrose 30 g | SmF 3 Optimization, immobilization and kinetic parameters | Batch flask 4% inoculant 30 °C 150 rpm 21 days | 2990 mg/L 142.38 mg/L/day | [64] |
Pleurotus eryngii | Fructose 50 g/L | SmF 3 Optimization, incubation, temperature, pH, and agitation | Batch flask 25 °C 150 rpm pH 7 18 days | 7920 mg/L 440 mg/L/day | [65] |
Fusarium oxysporum | Sesame brak Sucrose 3 g | SSF 2 Medium components and culture conditions | Batch flask (10 g in 500 mL) 30 °C 8–10 days | 8160 mg/kg 816 mg/kg/day | [66] |
8. GA3 Production Improvement by Genetic Engineering and Bioprocess Optimization
Micro-Organism | Genetic Modification Strategy | Cultivation Mode | Operation Conditions | Production (g/L) Productivity (g/L/day) | Ref. |
---|---|---|---|---|---|
G. fujikuroi Mutant Mor-25 | Random mutagenesis after UV irradiation Selection based on morphology and pigmentation | SmF 3 Mutants does not accumulate pigments Sucrose 112.5 g/L | Batch fermenter (10-L) 8 days pH 6.8 28 °C | 720 mg/L 90 mg/L/day | [87] |
G. fujikuroi Mutant S109 | Random mutagenesis increasing the activity of 3-hydroxy-3-methylglutaryl-coenzyme A (HMG-CoA) reductase | SmF 3 Corn flour 75 g/L Rice flour 87.5 g/L Adding glycerol 10 g/L at day 5 | Batch Bioreactor (2 L in 5 L) 28 °C 600 rpm 0.5 vvm 9 days | 2800 mg/L 311.1 mg/L/day | [69] |
G. fujikuroi Mutant M27 | Random mutagenesis of protoplasts Screening during 16 rounds | SmF 3 Corn flour 7.5% Rice flour 8.75% | Batch flask (40 mL in 250 mL) 28 °C 250 rpm 7 days | Around 2380 mg/L 340 mg/L/day | [91] |
F. moniliforme Mutant γ-14 | Random mutagenesis after gamma rays irradiation Selection based on colony morphology and pigmentation | SmF 3 Milk permeate medium and optimization temperature, incubation, pH, inoculum size | Semicontinuous 30 °C 150 rpm pH 5 8 days | 2400 mg/L 300 mg/L/day | [88] |
F. fujikuroi Mutant IMI 58289 | Random mutagenesis of protoplasts Irradiated with Cobalt-60 and Lithium-chloride Genome sequencing | SmF 3 Starch 75 g/L Rice flour 87.5 g/L | Batch flask (40 mL in 250 mL) 28 °C 250 g 7 days | 2100 mg/L 300 mg/L/day | [72] |
F. fujikuroi Mutant NM | Multivariate modular metabolic engineering approach Gene overexpression of genes involved in GA3 biosynthesis | SmF 3 Corn starch 75 g/L Rice flour 87.5 g/L | Batch flask 7 days | 2890 mg/L 412.85 mg/L/day | [89] |
F. fujikuroi Mutant CGMCC No: M 2,019,378 | Regulatory modification Overexpression of AreA and Lae1 positive regulators | SmF 3 Cornstarch, 75; rice four, 87.5; soybean meal, 5; peanut powder, 5 g/L | Batch flask 28 °C 600 rpm 7 days | 3020 mg/L 431.43 mg/L/day | [90] |
9. Market Overview
10. Conclusions and Future Prospects
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Shah, S.H.; Islam, S.; Mohammad, F.; Siddiqui, M.H. Gibberellic Acid: A Versatile Regulator of Plant Growth, Development and Stress Responses. J. Plant Growth Regul. 2023, 42, 7352–7373. [Google Scholar] [CrossRef]
- Zhang, H.; Sun, X.; Dai, M. Improving Crop Drought Resistance with Plant Growth Regulators and Rhizobacteria: Mechanisms, Applications, and Perspectives. Plant Commun. 2022, 3, 100228. [Google Scholar] [CrossRef]
- Rademacher, W. Plant Growth Regulators: Backgrounds and Uses in Plant Production. J. Plant Growth Regul. 2015, 34, 845–872. [Google Scholar] [CrossRef]
- Yan, H.; Yang, Z.; Chen, S.; Wu, J. Exploration and Development of Artificially Synthesized Plant Growth Regulators. Adv. Agrochem 2023, 3, 47–56. [Google Scholar] [CrossRef]
- Wang, H.N.; Ke, X.; Zhou, J.P.; Liu, Z.Q.; Zheng, Y.G. Recent Advances in Metabolic Regulation and Bioengineering of Gibberellic Acid Biosynthesis in Fusarium Fujikuroi. World J. Microbiol. Biotechnol. 2022, 38, 131. [Google Scholar] [CrossRef] [PubMed]
- Kawaide, H. Biochemical and Molecular Analyses of Gibberellin Biosynthesis in Fungi. Biosci. Biotechnol. Biochem. 2006, 70, 583–590. [Google Scholar] [CrossRef]
- Pinheiro, U.V.; Wancura, J.H.C.; Brondani, M.; da Silva, C.M.; Mainardi, M.A.; Gai, R.M.; Jahn, S.L. Production of Gibberellic Acid by Solid-State Fermentation Using Wastes from Rice Processing and Brewing Industry. Appl. Biochem. Biotechnol. 2024, 196, 1493–1508. [Google Scholar] [CrossRef] [PubMed]
- Escamilla, S.E.M.; Dendooven, L.; Magaña, I.P.; Parra, S.R.; De la Torre, M. Optimization of Gibberellic Acid Production by Immobilized Gibberella Fujikuroi Mycelium in Fluidized Bioreactors. J. Biotechnol. 2000, 76, 147–155. [Google Scholar] [CrossRef]
- Research and Markets Global Gibberellins Market by Type (19-Carbon Gibberellins, 20-Carbon Gibberellins), Application (Fruit Production, Increasing Sugarcane Yield, Malting of Barley)—Forecast 2024–2030. Available online: https://www.researchandmarkets.com/report/gibberellins#reld0-5616193 (accessed on 23 March 2024).
- Bashyal, B.M. Etiology of an Emerging Disease: Bakanae of Rice. Indian Phytopathol. 2018, 71, 485–494. [Google Scholar] [CrossRef]
- Kharwar, R.N.; Upadhyay, R.S.; Dubey, N.K.; Raghuwanshi, R. Microbial Diversity and Biotechnology in Food Security. Microb. Divers. Biotechnol. Food Secur. 2014, 1, 1–610. [Google Scholar] [CrossRef]
- An, Y.N.; Murugesan, C.; Choi, H.; Kim, K.D.; Chun, S.C. Current Studies on Bakanae Disease in Rice: Host Range, Molecular Identification, and Disease Management. Mycobiology 2023, 51, 195–209. [Google Scholar] [CrossRef] [PubMed]
- Nirenberg, H. Untersuchungen Uber Die Morphologische Und Biologische Differenzierung in Der Fusarium-Sektion Liseola. Mycologia 1976, 69, 1247–1248. [Google Scholar]
- Ito, S.; Kimura, J. Studies on the Bakanae Disease of the Rice Plant. Rep Hokkaido Agric Exp Sta 1931, 27, 1–95. [Google Scholar]
- Wollenweber, H.; Reinking, O. Die Fusarien: Ihre Beschreibung, Schadwirkung Und Bekämpfung; Paul Parey: Berlin, Germany, 1935. [Google Scholar]
- Lee, S.B.; Lee, J.Y.; Kang, J.W.; Mang, H.; Kabange, N.R.; Seong, G.U.; Kwon, Y.; Lee, S.M.; Shin, D.; Lee, J.H.; et al. A Novel Locus for Bakanae Disease Resistance, QBK4T, Identified in Rice. Agronomy 2022, 12, 2567. [Google Scholar] [CrossRef]
- Kanjanasoon, P. Studies on the Bakanae Disease of Rice in Thai-Land. Ph.D. Thesis, Tokyo University, Tokyo, Japan, 1965. [Google Scholar]
- Shin, S.; Ryu, H.; Jung, J.Y.; Yoon, Y.J.; Kwon, G.; Lee, N.; Kim, N.H.; Lee, R.; Oh, J.; Baek, M.; et al. Past and Future Epidemiological Perspectives and Integrated Management of Rice Bakanae in Korea. Plant Pathol. J. 2023, 39, 1–20. [Google Scholar] [CrossRef] [PubMed]
- Castro-Camba, R.; Sánchez, C.; Vidal, N.; Vielba, J.M. Plant Development and Crop Yield: The Role of Gibberellins. Plants 2022, 11, 2650. [Google Scholar] [CrossRef] [PubMed]
- Wulff, E.G.; Sørensen, J.L.; Lübeck, M.; Nielsen, K.F.; Thrane, U.; Torp, J. Fusarium Spp. Associated with Rice Bakanae: Ecology, Genetic Diversity, Pathogenicity and Toxigenicity. Environ. Microbiol. 2010, 12, 649–657. [Google Scholar] [CrossRef] [PubMed]
- Mohd Zainudin, N.A.I.; Razak, A.A.; Salleh, B. Bakanae Disease of Rice in Malaysia and Indonesia: Etiology of the Causal Agent Based on Morphological, Physiological and Pathogenicity Characteristics. J. Plant Prot. Res. 2008, 48, 475–485. [Google Scholar] [CrossRef]
- Niehaus, E.M.; Münsterkötter, M.; Proctor, R.H.; Brown, D.W.; Sharon, A.; Idan, Y.; Oren-Young, L.; Sieber, C.M.; Novák, O.; Pěnčík, A.; et al. Comparative “Omics” of the Fusarium Fujikuroi Species Complex Highlights Differences in Genetic Potential and Metabolite Synthesis. Genome Biol. Evol. 2016, 8, 3574–3599. [Google Scholar] [CrossRef]
- Bashyal, B.M.; Aggarwal, R.; Sharma, S.; Gupta, S.; Singh, U.B. Single and Combined Effects of Three Fusarium Species Associated with Rice Seeds on the Severity of Bakanae Disease of Rice. J. Plant Pathol. 2016, 98, 405–412. [Google Scholar] [CrossRef]
- Jiang, H.; Wu, N.; Jin, S.; Ahmed, T.; Wang, H.; Li, B.; Wu, X.; Bao, Y.; Liu, F.; Zhang, J.Z. Identification of Rice Seed-Derived Fusarium Spp. and Development of Lamp Assay against Fusarium Fujikuroi. Pathogens 2021, 10, 1. [Google Scholar] [CrossRef]
- Shakeel, Q.; Mubeen, M.; Sohail, M.A.; Ali, S.; Iftikhar, Y.; Tahir Bajwa, R.; Aqueel, M.A.; Upadhyay, S.K.; Divvela, P.K.; Zhou, L. An Explanation of the Mystifying Bakanae Disease Narrative for Tomorrow’s Rice. Front. Microbiol. 2023, 14, 1153437. [Google Scholar] [CrossRef] [PubMed]
- Hsuan, H.M.; Salleh, B.; Zakaria, L. Molecular Identificationn of Fusarium Species in Gibberella Fujikuroi Species Complex from Rice, Sugarcane and Maize from Peninsular Malaysia. Int. J. Mol. Sci. 2011, 12, 6722–6732. [Google Scholar] [CrossRef] [PubMed]
- Leslie, J.F.; Summerell, B.A. The Fusarium Laboratory Manual; John Wiley & Sons: Hoboken, NJ, USA, 2007; ISBN 0813819199. [Google Scholar]
- Studt, L.; Wiemann, P.; Kleigrewe, K.; Humpf, H.U.; Tudzynski, B. Biosynthesis of Fusarubins Accounts for Pigmentation of Fusarium Fujikuroi Perithecia. Appl. Environ. Microbiol. 2012, 78, 4468–4480. [Google Scholar] [CrossRef] [PubMed]
- Tian, H.; Xu, Y.; Liu, S.; Jin, D.; Zhang, J.; Duan, L.; Tan, W. Synthesis of Gibberellic Acid Derivatives and Their Effects on Plant Growth. Molecules 2017, 22, 694. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharya, A. Effect of High-Temperature Stress on the Metabolism of Plant Growth Regulators; Academic Press: Cambridge, MA, USA, 2019; pp. 485–591. ISBN 9780128175620. [Google Scholar]
- Talapatra, S.K.; Talapatra, B. Chemistry of Plant Natural Products; Springer: Berlin/Heidelberg, Germany, 2015; ISBN 9783642454097. [Google Scholar]
- Camara, M.C.; Vandenberghe, L.P.S.; Rodrigues, C.; de Oliveira, J.; Faulds, C.; Bertrand, E.; Soccol, C.R. Current Advances in Gibberellic Acid (GA3) Production, Patented Technologies and Potential Applications. Planta 2018, 248, 1049–1062. [Google Scholar] [CrossRef] [PubMed]
- Cen, Y.K.; Lin, J.G.; Wang, Y.L.; Wang, J.Y.; Liu, Z.Q.; Zheng, Y.G. The Gibberellin Producer Fusarium Fujikuroi: Methods and Technologies in the Current Toolkit. Front. Bioeng. Biotechnol. 2020, 8, 232. [Google Scholar] [CrossRef]
- Valent BioSciences Ficha Técnica Activol. Available online: https://valent.mx/descargas/tecnicas/TDS_Activol.pdf (accessed on 13 April 2024).
- Arysta LifeScience Ficha Técnica BIOGIP 10, PS. Available online: https://mx.uplonline.com/download_links/yXNAEXRJvvJKqvpJYsR0uLjimHAzju0cPHzxFz1I.pdf (accessed on 13 April 2024).
- Othman, Y.A.; Leskovar, D.I. Foliar Application of Gibberellic Acid Improves Yield and Head Phenolic Compounds in Globe Artichoke. Sci. Hortic. 2022, 301, 111115. [Google Scholar] [CrossRef]
- Gupta, R.; Chakrabarty, S.K. Gibberellic Acid in Plant: Still a Mystery Unresolved. Plant Signal. Behav. 2013, 8, e25504. [Google Scholar] [CrossRef]
- Shahzad, K.; Hussain, S.; Arfan, M.; Hussain, S.; Waraich, E.A.; Zamir, S.; Saddique, M.; Rauf, A.; Kamal, K.Y.; Hano, C.; et al. Exogenously Applied Gibberellic Acid Enhances Growth and Salinity Stress Tolerance of Maize through Modulating the Morpho-Physiological, Biochemical and Molecular Attributes. Biomolecules 2021, 11, 1005. [Google Scholar] [CrossRef]
- Rady, M.M.; Boriek, S.H.K.; El-Mageed, T.A.A.; El-Yazal, M.A.S.; Ali, E.F.; Hassan, F.A.S.; Abdelkhalik, A. Exogenous Gibberellic Acid or Dilute Bee Honey Boosts Drought Stress Tolerance in Vicia Faba by Rebalancing Osmoprotectants, Antioxidants, Nutrients, and Phytohormones. Plants 2021, 10, 748. [Google Scholar] [CrossRef] [PubMed]
- Emamverdian, A.; Ding, Y.; Mokhberdoran, F. The Role of Salicylic Acid and Gibberellin Signaling in Plant Responses to Abiotic Stress with an Emphasis on Heavy Metals. Plant Signal. Behav. 2020, 15, 1777372. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Z.; Ding, Y.; Zhao, J.; Nie, Y.; Zhang, Y.; Sheng, J.; Tang, X. Effects of Postharvest Gibberellic Acid Treatment on Chilling Tolerance in Cold-Stored Tomato (Solanum lycopersicum L.) Fruit. Food Bioprocess Technol. 2016, 9, 1202–1209. [Google Scholar] [CrossRef]
- Hu, Z.; Weijian, L.; Yali, F.; Huiquan, L. Gibberellic Acid Enhances Postharvest Toon Sprout Tolerance to Chilling Stress by Increasing the Antioxidant Capacity during the Short-Term Cold Storage. Sci. Hortic. 2018, 237, 184–191. [Google Scholar] [CrossRef]
- Zhang, J.; Cao, Y.; Tang, J.; He, X.; Li, M.; Li, C.; Ren, X.; Ding, Y. Physiology and Application of Gibberellins in Postharvest Horticultural Crops. Horticulturae 2023, 9, 625. [Google Scholar] [CrossRef]
- Fàbregas, N.; Fernie, A.R. The Interface of Central Metabolism with Hormone Signaling in Plants. Curr. Biol. 2021, 31, R1535–R1548. [Google Scholar] [CrossRef]
- Araújo, W.L.; Martins, A.O.; Fernie, A.R.; Tohge, T. 2-Oxoglutarate: Linking TCA Cycle Function with Amino Acid, Glucosinolate, Flavonoid, Alkaloid, and Gibberellin Biosynthesis. Front. Plant Sci. 2014, 5, 113245. [Google Scholar] [CrossRef] [PubMed]
- Tudzynski, B. Gibberellin Biosynthesis in Fungi: Genes, Enzymes, Evolution, and Impact on Biotechnology. Appl. Microbiol. Biotechnol. 2005, 66, 597–611. [Google Scholar] [CrossRef] [PubMed]
- Bömke, C.; Tudzynski, B. Diversity, Regulation, and Evolution of the Gibberellin Biosynthetic Pathway in Fungi Compared to Plants and Bacteria. Phytochemistry 2009, 70, 1876–1893. [Google Scholar] [CrossRef]
- Tudzynski, B.; Hedden, P.; Carrera, E.; Gaskin, P. The P450-4 Gene of Gibberella Fujikuroi Encodes Ent-Kaurene Oxidase in the Gibberellin Biosynthesis Pathway. Appl. Environ. Microbiol. 2001, 67, 3514–3522. [Google Scholar] [CrossRef]
- Tudzynski, B.; Rojas, M.C.; Gaskin, P.; Hedden, P. The Gibberellin 20-Oxidase of Gibberella Fujikuroi Is a Multifunctional Monooxygenase. J. Biol. Chem. 2002, 277, 21246–21253. [Google Scholar] [CrossRef] [PubMed]
- Malonek, S.; Rojas, M.C.; Hedden, P.; Gaskin, P.; Hopkins, P.; Tudzynski, B. Functional Characterization of Two Cytochrome P450 Monooxygenase Genes, P450-1 and P450-4, of the Gibberellic Acid Gene Cluster in Fusanum Proliferatum (Gibberella Fujikuroi MP-D). Appl. Environ. Microbiol. 2005, 71, 1462–1472. [Google Scholar] [CrossRef] [PubMed]
- Keller, N.P.; Turner, G.; Bennett, J.W. Fungal Secondary Metabolism—From Biochemistry to Genomics. Nat. Rev. Microbiol. 2005, 3, 937–947. [Google Scholar] [CrossRef] [PubMed]
- Munoz, G.A.; Agosin, E. Glutamine Involvement in Nitrogen Control of Gibberellic Acid Production in Gibberella Fujikuroi. Appl. Environ. Microbiol. 1993, 59, 4317–4322. [Google Scholar] [CrossRef] [PubMed]
- Mihlan, M.; Homann, V.; Liu, T.W.D.; Tudzynski, B. AREA Directly Mediates Nitrogen Regulation of Gibberellin Biosynthesis in Gibberella Fujikuroi, but Its Activity Is Not Affected by NMR. Mol. Microbiol. 2003, 47, 975–991. [Google Scholar] [CrossRef] [PubMed]
- Schönig, B.; Brown, D.W.; Oeser, B.; Tudzynski, B. Cross-Species Hybridization with Fusarium Verticillioides Microarrays Reveals New Insights into Fusarium Fujikuroi Nitrogen Regulation and the Role of AreA and NMR. Eukaryot. Cell 2008, 7, 1831–1846. [Google Scholar] [CrossRef] [PubMed]
- Wagner, D.; Schmeinck, A.; Mos, M.; Morozov, I.Y.; Caddick, M.X.; Tudzynski, B. The BZIP Transcription Factor MeaB Mediates Nitrogen Metabolite Repression at Specific Loci. Eukaryot. Cell 2010, 9, 1588–1601. [Google Scholar] [CrossRef] [PubMed]
- Michielse, C.B.; Pfannmüller, A.; Macios, M.; Rengers, P.; Dzikowska, A.; Tudzynski, B. The Interplay between the GATA Transcription Factors AreA, the Global Nitrogen Regulator and AreB in Fusarium Fujikuroi. Mol. Microbiol. 2014, 91, 472–493. [Google Scholar] [CrossRef] [PubMed]
- Macios, M.; Caddick, M.X.; Weglenski, P.; Scazzocchio, C.; Dzikowska, A. The GATA Factors AREA and AREB Together with the Co-Repressor NMRA, Negatively Regulate Arginine Catabolism in Aspergillus Nidulans in Response to Nitrogen and Carbon Source. Fungal Genet. Biol. 2012, 49, 189–198. [Google Scholar] [CrossRef]
- Rios-Iribe, E.Y.; Flores-Cotera, L.B.; Chávira, M.M.G.; González-Alatorre, G.; Escamilla-Silva, E.M. Inductive Effect Produced by a Mixture of Carbon Source in the Production of Gibberellic Acid by Gibberella Fujikuroi. World J. Microbiol. Biotechnol. 2011, 27, 1499–1505. [Google Scholar] [CrossRef]
- Pandya, J.B.; Patani, A.N.; Raval, V.H.; Rajput, K.N.; Panchal, R.R. Understanding the Fermentation Potentiality For Gibberellic Acid (GA3) Production Using Fungi. Curr. Microbiol. 2023, 80, 385. [Google Scholar] [CrossRef] [PubMed]
- Monrroy, M.; García, J.R. Gibberellic Acid Production from Corn Cob Residues via Fermentation with Aspergillus Niger. J. Chem. 2022, 2022, 1112941. [Google Scholar] [CrossRef]
- Seyis Bilkay, I.; Karakoç, Ş.; Aksöz, N. Aspergillus Niger’den Indol Asetik Asit ve Gibberellik Asit Üretimi. Turkish J. Biol. 2010, 34, 313–318. [Google Scholar] [CrossRef]
- Cihangir, N.; Aksöza, N. Evaluation of Some Food Industry Wastes for Production of Gibberellic Acid by Fungal Source. Environ. Technol. 1997, 18, 533–537. [Google Scholar] [CrossRef]
- Isa, N.K.M.; Mat Don, M. Investigation of the Gibberellic Acid Optimization with a Statistical Tool from Penicillium Variable in Batch Reactor. Prep. Biochem. Biotechnol. 2014, 44, 572–585. [Google Scholar] [CrossRef]
- Doğan, B.; Yıldız, Z.; Aksöz, N.; Eninanç, A.B.; Dağ, İ.; Yıldız, A.; Doğan, H.H.; Yamaç, M. Flask and Reactor Scale Production of Plant Growth Regulators by Inonotus Hispidus: Optimization, Immobilization and Kinetic Parameters. Prep. Biochem. Biotechnol. 2023, 53, 1210–1223. [Google Scholar] [CrossRef] [PubMed]
- Doğan, B.; Yıldız, Z.; Aksöz, N.; Eninanç, A.B.; Korkmaz Kahveci, B.G.; Yamaç, M. Optimization and Reactor-Scale Production of Plant Growth Regulators by Pleurotus Eryngii. 3 Biotech 2023, 13, 314. [Google Scholar] [CrossRef] [PubMed]
- Ben Rhouma, M.; Kriaa, M.; Ben Nasr, Y.; Mellouli, L.; Kammoun, R. A New Endophytic Fusarium Oxysporum Gibberellic Acid: Optimization of Production Using Combined Strategies of Experimental Designs and Potency on Tomato Growth under Stress Condition. Biomed Res. Int. 2020, 2020, 4587148. [Google Scholar] [CrossRef] [PubMed]
- DARKEN, M.A.; JENSEN, A.L.; SHU, P. Production of Gibberellic Acid by Fermentation. Appl. Microbiol. 1959, 7, 301–303. [Google Scholar] [CrossRef]
- Wang, W.; Wu, Y.; Yao, Y. Construction and Analysis on the Kinetic Model of Gibberellin Acid in Batch Fermentation. Chinese J. Process Eng. 2017, 17, 605–612. [Google Scholar] [CrossRef]
- Peng, X.L.; Zhao, W.J.; Wang, Y.S.; Dai, K.L.; Cen, Y.K.; Liu, Z.Q.; Zheng, Y.G. Enhancement of Gibberellic Acid Production from Fusarium Fujikuroi by Mutation Breeding and Glycerol Addition. 3 Biotech 2020, 10, 312. [Google Scholar] [CrossRef]
- Qian, X.M.; du Preez, J.C.; Kilian, S.G. Factors Affecting Gibberellic Acid Production by Fusarium Moniliforme in Solid-State Cultivation on Starch. World J. Microbiol. Biotechnol. 1994, 10, 93–99. [Google Scholar] [CrossRef] [PubMed]
- De Oliveira, J.; Rodrigues, C.; Vandenberghe, L.P.S.; Câmara, M.C.; Libardi, N.; Soccol, C.R. Gibberellic Acid Production by Different Fermentation Systems Using Citric Pulp as Substrate/Support. Biomed Res. Int. 2017, 2017, 5191046. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Lei, Z.; Liu, Z.Q.; Zheng, Y.G. Improvement of Gibberellin Production by a Newly Isolated Fusarium Fujikuroi Mutant. J. Appl. Microbiol. 2020, 129, 1620–1632. [Google Scholar] [CrossRef] [PubMed]
- Shi, T.Q.; Shen, Y.H.; Li, Y.W.; Huang, Z.Y.; Nie, Z.K.; Ye, C.; Wang, Y.T.; Guo, Q. Improving the Productivity of Gibberellic Acid by Combining Small-Molecule Compounds-Based Targeting Technology and Transcriptomics Analysis in Fusarium Fujikuroi. Bioresour. Technol. 2024, 394, 130299. [Google Scholar] [CrossRef] [PubMed]
- Hollmann, D.; Switalski, J.; Geipel, S.; Onken, U. Extractive Fermentation of Gibberellic Acid by Gibberella Fujikuroi. J. Ferment. Bioeng. 1995, 79, 594–600. [Google Scholar] [CrossRef]
- Gökdere, M.; Ateş, S. Extractive Fermentation of Gibberellic Acid with Free and Immobilized Gibberella Fujikuroi. Prep. Biochem. Biotechnol. 2014, 44, 80–89. [Google Scholar] [CrossRef] [PubMed]
- Chavez-Parga, M.d.C.; Gonzalez-Ortega, O.; Negrete-Rodríguez, M.d.l.L.X.; Vallarino, I.G.; Alatorre, G.G.; Escamilla-Silva, E.M. Kinetic of the Gibberellic Acid and Bikaverin Production in an Airlift Bioreactor. Process Biochem. 2008, 43, 855–860. [Google Scholar] [CrossRef]
- Shukla, R.; Chand, S.; Srivastava, A.K. Improvement of Gibberellic Acid Production Using a Model Based Fed-Batch Cultivation of Gibberella Fujikuroi. Process Biochem. 2005, 40, 2045–2050. [Google Scholar] [CrossRef]
- Shukla, R.; Chand, S.; Srivastava, A.K. Batch Kinetics and Modeling of Gibberellic Acid Production by Gibberella Fujikuroi. Enzyme Microb. Technol. 2005, 36, 492–497. [Google Scholar] [CrossRef]
- Rangaswamy, V. Improved Production of Gibberellic Acid by Fusarium moniliforme. J. Microbiol. Res. 2012, 2, 51–55. [Google Scholar] [CrossRef]
- Dinolfo, M.I.; Martínez, M.; Castañares, E.; Arata, A.F. Fusarium in Maize during Harvest and Storage: A Review of Species Involved, Mycotoxins, and Management Strategies to Reduce Contamination. Eur. J. Plant Pathol. 2022, 164, 151–166. [Google Scholar] [CrossRef]
- Bacon, C.W.; Nelson, P.E. Fumonisin Production in Corn by Toxigenic Strains of Fusarium Moniliforme and Fusarium Proliferatum. J. Food Prot. 1994, 57, 514–521. [Google Scholar] [CrossRef] [PubMed]
- Shier, W.T. The Fumonisin Paradox: A Review of Research on Oral Bioavailability of Fumonisin B1, a Mycotoxin Produced by Fusarium Moniliforme. J. Toxicol.-Toxin Rev. 2000, 19, 161–187. [Google Scholar] [CrossRef]
- Tomasini, A.; Fajardo, C.; Barrios-González, J. Gibberellic Acid Production Using Different Solid-State Fermentation Systems. World J. Microbiol. Biotechnol. 1997, 13, 203–206. [Google Scholar] [CrossRef]
- Camara, M.C.; Vandenberghe, L.P.S.; Sextos, G.C.; Tanobe, V.O.A.; Magalhães Junior, A.I.; Soccol, C.R. Alternative Methods for Gibberellic Acid Production, Recovery and Formulation: A Case Study for Product Cost Reduction. Bioresour. Technol. 2020, 309, 123295. [Google Scholar] [CrossRef] [PubMed]
- Rios-Iribe, E.Y.; Hernández-Calderón, O.M.; Reyes-Moreno, C.; Contreras-Andrade, I.; Flores-Cotera, L.B.; Escamilla-Silva, E.M. A Possible Mechanism of Metabolic Regulation in Gibberella Fujikuroi Using a Mixed Carbon Source of Glucose and Corn Oil Inferred from Analysis of the Kinetics Data Obtained in a Stirrer Tank Bioreactor. Biotechnol. Prog. 2013, 29, 1169–1180. [Google Scholar] [CrossRef] [PubMed]
- Machado, C.M.M.; Soccol, C.R.; De Oliveira, B.H.; Pandey, A. Gibberellic Acid Production by Solid-State Fermentation in Coffee Husk. Appl. Biochem. Biotechnol.-Part A Enzym. Eng. Biotechnol. 2002, 102–103, 179–191. [Google Scholar] [CrossRef]
- Lale, G.; Jogdand, V.V.; Gadre, R.V. Morphological Mutants of Gibberella Fujikuroi for Enhanced Production of Gibberellic Acid. J. Appl. Microbiol. 2006, 100, 65–72. [Google Scholar] [CrossRef]
- Meleigy, S.A.; Khalaf, M.A. Biosynthesis of Gibberellic Acid from Milk Permeate in Repeated Batch Operation by a Mutant Fusarium Moniliforme Cells Immobilized on Loofa Sponge. Bioresour. Technol. 2009, 100, 374–379. [Google Scholar] [CrossRef]
- Wang, H.N.; Ke, X.; Jia, R.; Huang, L.G.; Liu, Z.Q.; Zheng, Y.G. Multivariate Modular Metabolic Engineering for Enhanced Gibberellic Acid Biosynthesis in Fusarium Fujikuroi. Bioresour. Technol. 2022, 364, 128033. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Ke, X.; Jia, R.; Huang, L.; Liu, Z.; Zheng, Y. Gibberellic Acid Overproduction in Fusarium Fujikuroi Using Regulatory Modification and Transcription Analysis. Appl. Microbiol. Biotechnol. 2023, 107, 3071–3084. [Google Scholar] [CrossRef] [PubMed]
- Cen, Y.K.; Li, M.H.; Wang, Q.; Zhang, J.M.; Yuan, J.C.; Wang, Y.S.; Liu, Z.Q.; Zheng, Y. Evolutionary Engineering of Fusarium Fujikuroi for Enhanced Production of Gibberellic Acid. Process Biochem. 2023, 125, 7–14. [Google Scholar] [CrossRef]
- Grand View Research, Gibberellins Market Size, Share & Trends Analysis Report By Application (Malting of Barley, Increasing Sugarcane Yield, Fruit Production, Seed Production), By Region, And Segment Forecasts, 2020–2025. Available online: https://www.grandviewresearch.com/industry-analysis/gibberellins-market (accessed on 28 March 2024).
- Reports and Data. Materials and Chemicals—Gibberellins Market. Available online: https://www.reportsanddata.com/report-detail/gibberellins-market (accessed on 9 April 2024).
- Fruugo, Jinzhaolai Gibberellic Acid, Plant Growth Regulator, Root Plant, Gibberellin, Ga4+7. Available online: https://www.fruugonorge.com/jinzhaolai-gibberellsyre-plantevekstregulator-rotplante-gibberellin-ga4-7-10g-100g/p-175467144-375020069?language=no (accessed on 10 April 2024).
- Plant Hormones, Foliar Fertilizer Gibberellin Gibberellic Acid Ga4 7 Uses in Agriculture. Available online: https://planthormones.en.made-in-china.com/product/eSbJOsTvllUo/China-Foliar-Fertilizer-Gibberellin-Gibberellic-Acid-Ga4-7-Uses-in-Agriculture.html (accessed on 10 April 2024).
- Zhejian Rayfull Chemicals Co LTD. Raw Material Gibberellins Ga4+7 Plant Hormones. Available online: https://www.rayfull.net/showroom/raw-material-gibberellins-ga4-7-plant-hormones-price.html (accessed on 10 April 2024).
- Verified Market Reports, Gibberellic Acid Market Insights. Available online: https://www.verifiedmarketreports.com/product/gibberellic-acid-market/ (accessed on 24 March 2024).
- Global Industry Analysts Inc. Gibberellins-Global Strategic Business Report. Available online: https://www.researchandmarkets.com/report/gibberellins#reld0-5616193%0D%0A%0D%0A (accessed on 30 March 2024).
- Agropages. Anaconda Fusheng: Based on the Advantages of Technology and Production to Build the Ecology of Plant Conditioner Industry Represented by Gibberellin. Available online: https://cn.agropages.com/News/NewsDetail---24071.htm (accessed on 12 April 2024).
- Meng Dong Feng. Gibberellic Acid Market Research. Available online: https://rstudio-pubs-static.s3.amazonaws.com/1004724_e78c72207fc8488eb9e5e56ce6d774b9.html (accessed on 16 April 2024).
- SEAIR Gibberellic Acid Import Data in USA—Updated Shipment Details Report. Available online: https://www.seair.co.in/us-import/product-gibberellic-acid.aspx (accessed on 16 April 2024).
- Fortune Business Insights Gibberellic Acid Market Size, Share & Industry Analysis, By Type (Powder, Tablets, Others), By Application (Agricultural, Laboratory, Others) and Regional Forecast, 2024–2032. Available online: https://www.fortunebusinessinsights.com/gibberellic-acid-market-104192 (accessed on 20 April 2024).
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
Hernández Rodríguez, A.; Díaz Pacheco, A.; Martínez Tolibia, S.E.; Melendez Xicohtencatl, Y.; Granados Balbuena, S.Y.; López y López, V.E. Bioprocess of Gibberellic Acid by Fusarium fujikuroi: The Challenge of Regulation, Raw Materials, and Product Yields. J. Fungi 2024, 10, 418. https://doi.org/10.3390/jof10060418
Hernández Rodríguez A, Díaz Pacheco A, Martínez Tolibia SE, Melendez Xicohtencatl Y, Granados Balbuena SY, López y López VE. Bioprocess of Gibberellic Acid by Fusarium fujikuroi: The Challenge of Regulation, Raw Materials, and Product Yields. Journal of Fungi. 2024; 10(6):418. https://doi.org/10.3390/jof10060418
Chicago/Turabian StyleHernández Rodríguez, Aranza, Adrián Díaz Pacheco, Shirlley Elizabeth Martínez Tolibia, Yazmin Melendez Xicohtencatl, Sulem Yali Granados Balbuena, and Víctor Eric López y López. 2024. "Bioprocess of Gibberellic Acid by Fusarium fujikuroi: The Challenge of Regulation, Raw Materials, and Product Yields" Journal of Fungi 10, no. 6: 418. https://doi.org/10.3390/jof10060418