Mikrobiol. Z. 2019; 81(2):90-109. Ukrainian.
doi: https://doi.org/10.15407/microbiolj81.02.090

Synthesis of Biologically Active Gibberellins GA4 and GA7 by Microorganisms

Pirog T.P.1,2, Havrylkina D.V.1, Leonova N.O.2, Shevchuk T.A.2, Iutynska G.O.2

1National University of Food Technologies
68 Volodymyrska Str., Kyiv, 01601, Ukraine

2Zabolotny Institute of Microbiology and Virology, NAS of Ukraine
154 Akad. Zabolotny Str., Kyiv, 03143, Ukraine

Among the great variety (over 130) of gibberellins (GA), biological activity is possessed by GA1, GA3, GA4 and GA7, but in literature much less attention is paid to the microbial synthesis of the last two as compared with GA3. One of the reasons for this is a low concentration of GA4 and GA7 gibberellins synthesized by microorganisms (on orders of magnitude lower than GA3, whose microbial synthesis is realized on industrial scale). At the same time, the high biological activity of GA4 and GA7 (in some cases higher than GA3) has led in recent years to increase the interest of researchers in these gibberellins. The review summarizes the literature data on the formation of GA4 and GA7 as plant-associated bacteria and fungi and microorganisms that are not in this interaction, also on the synthesis of these gibberellins by mutant and genetically engineered strains of Fusarium moniliforme (Gibberella fujikuroi). The few reports for now on the intensification of microbial synthesis of gibberellins GA4 and GA7 (increasing the concentration to 500‒700 mg/l, which is on orders of magnitude higher than the original strains) indicate the potential for the realization of technologies for the production of these biologically active gibberellins on industrial scale.

Keywords: phytohormones, microbial synthesis, gibberellins GA4 and GA7.

Full text (PDF, in Ukrainian)

  1. Singh R, Kumar M, Mittal A, Mehta PK. Microbial metabolites in nutrition, healthcare and agriculture. 3 Biotech. 2017; 7(1):15. https://doi.org/10.1007/s13205-016-0586-4
  2. The Gibberellins. In: Annual plant reviews. Ed. Hedden P, Thomas GS. Vol. 49. Wiley Blackwell; 2016. https://doi.org/10.1002/9781119210436
  3. Shi TQ, Peng H, Zeng SY, Ji RY, Shi K, Huang H, et al. Microbial production of plant hormones: Opportunities and challenges. Bioengineered. 2017; 8(2):124−8. https://doi.org/10.1080/21655979.2016.1212138
  4. Rangaswamy V. Improved production of gibberellic acid by Fusarium moniliforme. J Microbiol Res. 2012; 2(3):51−5. https://doi.org/10.5923/j.microbiology.20120203.02
  5. Lale G, Gadre R. Enhanced production of gibberellin A4 (GA4) by a mutant of Gibberella fujikuroi in wheat gluten medium. Ind Microbiol Biotechnol. 2010; 37(3):297–306. https://doi.org/10.1007/s10295-009-0673-1
  6. Makeeva A. [Research of microbial synthesis individual gibberellins and abscisic acid]. Thesis for the degree of candidate of biological sciences by speciality 03.00.23 – biotechnology. Moscow; 1996. Russian.
  7. Pirog TP, Iutynska GO, Leonova NO, Beregova KA, Schevchuk TA. Microbial synthesis of phytohormones. Biotechnologia Acta. 2018; 11(1):5−24. https://doi.org/10.15407/biotech11.01.005
  8. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L. Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech. 2015; 5(4):355−77.
  9. Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A. Role of plant growth promoting rhizobacteria in agricultural sustainability − a review. Molecules. 2016; 21(5):E573. https://doi.org/10.3390/molecules21050573
  10. Atzorn R, Crozier A, Wheeler CT, Sandberg G. Production of gibberellins and indole-3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots. Planta. 1988; 175(4):532–8. https://doi.org/10.1007/BF00393076
  11. Méndez C, Baginsky C, Hedden P, Gong F, Carú M, Rojas MC. Gibberellin oxidase activities in Bradyrhizobium japonicum bacteroids. Phytochemistry. 2014; 98:101–9. https://doi.org/10.1016/j.phytochem.2013.11.013
  12. Nett RS, Contreras T, Peters RJ. Characterization of CYP115 as a gibberellin 3-oxidase indicates that certain rhizobia can produce bioactive gibberellin A4. ACS Chem Biol. 2017; 12(4):912‒917. https://doi.org/10.1021/acschembio.6b01038
  13. Gutiérrez‐Ma-ero FJ, Ramos‐Solano B, Mehouachi J, Tadeo FR, Talon M. The plant‐growth‐promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plantarum. 2001; 111(2):206–11. https://doi.org/10.1034/j.1399-3054.2001.1110211.x
  14. Joo GJ, Kim YM, Lee IJ, Song KS, Rhee IK. Growth promotion of red pepper plug seedlings and the production of gibberellins by Bacillus cereus, Bacillus macroides and Bacillus pumilus. Biotechnol Lett. 2004; 26(6):487–91. https://doi.org/10.1023/B:BILE.0000019555.87121.34
  15. Park YG, Mun BG, Kang SM, Hussain A, Shahzad R, Seo CW, et al. Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PloS one. 2017; 12(3):e0173203. https://doi.org/10.1371/journal.pone.0173203
  16. Kang SM, Radhakrishnan R, Khan AL, Kim MJ, Park JM, Kim BR, et al. Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem. 2014; 84:115–24. https://doi.org/10.1016/j.plaphy.2014.09.001
  17. Lee KE, Radhakrishnan R, Kang SM, You YH, Joo GJ, Lee IJ, et al. Enterococcus faecium LKE12 cell-free extract accelerates host plant growth via gibberellin and indole-3-acetic acid secretion. J Microbiol Biotechnol. 2015; 25(9):1467–75. https://doi.org/10.4014/jmb.1502.02011
  18. Kang SM, Khan AL, Waqas M, You YH, Hamayun M, Joo GJ, et al. Gibberellinproducing Serratia nematodiphila PEJ1011 ameliorates low temperature stress in Capsicum annuum L. Eur J Soil Biol. 2015; 68:85–93. https://doi.org/10.1016/j.ejsobi.2015.02.005
  19. Schulz B, Boyle C. The endophytic continuum. Mycological research. 2005; 109(6):661–86. https://doi.org/10.1017/S095375620500273X
  20. Shahzad R, Waqas M, Khan AL, Asaf S, Khan MA, Kang SM, et al. Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol. Biochem. 2016; 106:236–43. https://doi.org/10.1016/j.plaphy.2016.05.006
  21. Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A et al. Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol. 2014; 52(8):689–95. https://doi.org/10.1007/s12275-014-4002-7
  22. Xu X, van Lammeren AA, Vermeer E, Vreugdenhil D. The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol. 1998; 117(2):575–84. https://doi.org/10.1104/pp.117.2.575
  23. Leonova NO, Dankevich LA, Dragovoz I.V. [Synthesis of extracellular phytohormonesstimulants with nodule and phytopathogenic soybean bacteria]. The report of the National Academy of Sciences of Ukraine, 2013; 3:165–71. Ukrainian.
  24. Joo GJ, Kang SM, Hamayun M, Kim SK, Na CI, Shin DH et al. Burkholderia sp. KCTC 11096BP as a newly isolated gibberellin producing bacterium. J Microbiol. 2009; 47(2):167–71. https://doi.org/10.1007/s12275-008-0273-1
  25. Kang SM, Joo GJ, Hamayun M, Na CI, Shin DH, Kim HY, et al. Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol. Lett. 2009; 31(2):277–81. https://doi.org/10.1007/s10529-008-9867-2
  26. Kang SM, Khan AL, Hamayun M, Hussain J, Joo GJ, You YH, et al. Gibberellin producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J Microbiol. 2012; 50(6):902–9. https://doi.org/10.1007/s12275-012-2273-4
  27. Kang SM, Khan AL, You YH, Kim JG, Kamran M, Lee IJ. Gibberellin production by newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J Microbiol Biotechnol. 2014; 2 4(1):106–12.
  28. Ullah I, Khan AR, Jung BK, Khan AL, Lee IJ, Shin JH. Gibberellins synthesized by the entomopathogenic bacterium, Photorhabdus temperata M1021 as one of the factors of rice plant growth promotion. J Plant Interact. 2014; 9(1):775–82. https://doi.org/10.1080/17429145.2014.942956
  29. Hamayun M, Khan SA, Ahmad N, Tang DS, Kang SM, Na CI, et al. Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max (L.) Merr. World J Microbiol Biotechnol. 2009; 25(4):627–32. https://doi.org/10.1007/s11274-009-9982-9
  30. Choi WY, Rim SO, Lee JH, Lee JM, Lee IJ, Cho KJ, et al. Isolation of gibberellinsproducing fungi from the root of several Sesamum indicum plants. J Microbiol Biotechnol. 2005; 15(1):22–8.
  31. Khan SA, Hamayun M, Yoon H, Kim HY, Suh SJ, Hwang SK, et al. Plant growth promotion and Penicillium citrinum. BMC Microbiol. 2008; 8(1):231. https://doi.org/10.1186/1471-2180-8-231
  32. Khan SA, Hamayun M, Kim HY, Yoon HJ, Seo JC, Choo YS, et al. A new strain of Arthrinium phaeospermum isolated from Carex kobomugi Ohwi is capable of gibberellin production. Biotechnol. Lett. 2009; 31(2):283–7. https://doi.org/10.1007/s10529-008-9862-7
  33. Khan SA, Hamayun M, Kim HY, Yoon HJ, Lee IJ, Kim JG. Gibberellin production and plant growth promotion by a newly isolated strain of Gliomastix murorum. World J Microbiol Biotechnol. 2009; 25(5):829–33. https://doi.org/10.1007/s11274-009-9981-x
  34. Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, et al. Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH–6 isolated from cucumber (Cucumis sativus L.). Mycologia. 2010; 102(5):989–95. https://doi.org/10.3852/09-261
  35. Ahmad N, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH. Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J Microbiol Biotechnol. 2010; 20(12):1744–9.
  36. Hamayun M, Khan SA, Iqbal I, Ahmad B, Lee IJ. Isolation of a gibberellin-producing fungus (Penicillium sp. MH7) and growth promotion of Crown daisy (Chrysanthemum coronarium). J Microbiol Biotechnol. 2010; 20(1):202–7. https://doi.org/10.4014/jmb.0905.05040
  37. You YH, Yoon H, Kang SM, Woo JR, Choo YS, Lee IJ, et al. Cadophora malorum Cs‐8‐1 as a new fungal strain producing gibberellins isolated from Calystegia soldanella. J Basic Microbiol. 2013; 53(7):630–4. https://doi.org/10.1002/jobm.201200002
  38. Khan AL, Waqas M, Hussain J, Al-Harrasi A, Al-Rawahi A, Al-Hosni K, et al. Endophytes Aspergillus caespitosus LK12 and Phoma sp. LK13 of Moringa peregrina produce gibberellins and improve rice plant growth. J Plant Interact. 2014; 9(1):731–7. https://doi.org/10.1080/17429145.2014.917384
  39. Yurieva OM, Dragovoz IV, Leonova NO, Ostapchyk AM, Kharkhota MA, Syrchin SO, et al. [Gibberellins of endophytic and saprotrophic Penicillium funiculosum strains]. Mikrobiol Z. 2017; 79(5):57-69. Ukrainian. https://doi.org/10.15407/microbiolj79.05.057
  40. Leitão AL, Enguita FJ. Gibberellins in Penicillium strains: Challenges for endophyteplant host interactions under salinity stress. Microbiol Res. 2016; 183:8−18. https://doi.org/10.1016/j.micres.2015.11.004
  41. Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ. Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol. 2015; 35(1):62−74. https://doi.org/10.3109/07388551.2013.800018
  42. Bilal L, Asaf S, Hamayun M, Gul H, Iqbal A, Ullah I, et al. Plant growth promoting endophytic fungi Aspergillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis. 2018; 76(2):117–27. https://doi.org/10.1007/s13199-018-0545-4
  43. Al-Hosni K, Shahzad R, Latif Khan A, Muhammad Imran Q, Al Harrasi A, Al Rawahi A, et al. Preussia sp. BSL-10 producing nitric oxide, gibberellins, and indole acetic acid and improving rice plant growth. J Plant Interact. 2018; 13(1):112–8. https://doi.org/10.1080/17429145.2018.1432773
  44. Hamayun M, Khan SA, Khan AL, Rehman G, Sohn EY, Shah AA, et al. Phoma herbarum as a new gibberellin-producing and plant growth-promoting fungus. J Microbiol Biotechnol. 2009; 19(2):1244–49.
  45. Hamayun M, Khan SA, Iqbal I, Na CI, Khan AL, Hwang YH, et al. Chrysosporium pseudomerdarium produces gibberellins and promotes plant growth. J Microbiol. 2009; 47(4):425–30. https://doi.org/10.1007/s12275-009-0268-6
  46. Khan AL, Shinwari ZK, Kim Y, Waqas MU, Hamayun M, Kamran MU, et al. Role of endophyte Chaetomium globosum LK4 in growth of Capsicum annuum by producion of gibberellins and indole acetic acid. Pak J Bot. 2012; 44(5):1601–7.
  47. Hamayun M, Khan SA, Kim HY, Chaudhary MF, Hwang YH, Shin DH, et al. Gibberellin production and plant growth enhancement by newly isolated strain of Scolecobasidium tshawytschae. J Microbiol Biotechnol. 2009; 19(6):560–5.
  48. Tejesvi MV, Kini KR, Prakash HS, Subbiah V, Shetty HS. Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Diversity. 2007; 24(3):37–54.
  49. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, et al. Fungal endophytes limit pathogen damage in a tropical tree. PNAS. 2003; 100(26):15649–54. https://doi.org/10.1073/pnas.2533483100
  50. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS. 2005; 102(38):13386–91. https://doi.org/10.1073/pnas.0504423102
  51. Khan AL, Hamayun M, Kim YH, Kang SM, Lee JH, Lee IJ. Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. Proc Biochem. 2011; 46(2):440–7. https://doi.org/10.1016/j.procbio.2010.09.013
  52. Khan AL, Hamayun M, Ahmad N, Hussain J, Kang SM, Kim YH, et al. Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max L. J Microbiol Biotechnol. 2011; 21(9):893–902. https://doi.org/10.4014/jmb.1103.03012
  53. Khan AL, Hamayun M, Ahmad N, Waqas M, Kang SM, Kim YH, et al. Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiol Plantarum. 2011; 143(4):329–43. https://doi.org/10.1111/j.1399-3054.2011.01508.x
  54. Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, et al. Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol. 2012; 12(1):3. https://doi.org/10.1186/1471-2180-12-3
  55. Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, et al. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 2012; 17(9):10754–73. https://doi.org/10.3390/molecules170910754
  56. Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem. 2011; 49:852–62. https://doi.org/10.1016/j.plaphy.2011.03.005
  57. Khan AL, Lee IJ. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol. 2013; 13:86. https://doi.org/10.1186/1471-2229-13-86
  58. Radhakrishnan R, Khan AL, Lee IJ. Endophytic fungal pre-treatments of seeds alleviates salinity stress effects in soybean plants. J Microbiol. 2013; 51(6):850–7. https://doi.org/10.1007/s12275-013-3168-8
  59. Muromtsev GS, Krasnopolskaya L.M. [Micromycetes strain Fusarium moniliforme − producer of phytohormons gibberellins A4, A7]. RF Patent 2084531. Publ. 20.07.1997. Russian.
  60. Tudzynski B, Mihlan M, Rojas MC, Linnemannstöns P, Gaskin P, Hedden P. Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi: des and P450–3 encode GA4 desaturase and the 13-hydroxylase, respectively. J Biol Chem. 2003; 278(31):28635–43. https://doi.org/10.1074/jbc.M301927200
  61. Albermann S, Elter T, Teubner A, Krischke W, Hirth T, Tudzynski B. Characterization of novel mutants with an altered gibberellin spectrum in comparison to different wildtype strains of Fusarium fujikuroi. Appl Microbiol Biotechnol. 2013; 97(17):7779–90. https://doi.org/10.1007/s00253-013-4917-7
  62. Doaa Abd El monem Emam Sleem. Studies on the bioproduction of gibberellic acid from fungi. A Thesis for the degree of Doctor Philosophy of Science in Botany (Microbiology). Egypt: Benha University; 2013.
  63. Muddapur UM, Gadkari MV, Kulkarni SM, Sabannavar PG, Niyonzima FN, More SS. Isolation and characterization of gibberellic acid 3 producing Fusarium sp. from Belgaum agriculture land Andits impact on green pea and rice growth promotion. Aperito J Adv Plant Biol. 2015; 1(2):106.
  64. de Oliveira J, Rodrigues C, Vandenberghe LPS, Câmara MC, Libardi N, Soccol CR. Gibberellic acid production by different fermentation systems using citric pulp as substrate/support. Biomed Res Int. 2017; 2017:5191046. https://doi.org/10.1155/2017/5191046
  65. Hedden P, Sponsel V. A century of gibberellin research. J Plant Growth Regul. 2015; 34(4):740–60. https://doi.org/10.1007/s00344-015-9546-1