Advertisement

A volatile producing endophytic Bacillus siamensis YC7012 promotes root development independent on auxin or ethylene/jasmonic acid pathway

  • Mohammad Tofajjal Hossain
  • Ajmal Khan
  • Md. Harun-Or-Rashid
  • Young Ryun ChungEmail author
Regular Article
  • 140 Downloads

Abstract

Background & aims

Endophytic Bacillus species with plant growth promoting activities have been used in the last decade. The mechanism of their activities has been partially elucidated recently. Plant growth regulatory hormones that interact with volatiles emitted by endophytic Bacillus siamensis YC7012 have not been well defined yet. To elucidate the mechanism involved in the promoting effect of endophytic Bacillus siamensis YC7012 on root development of plants, the objective of this study was to investigate potential factors involved in interaction between Arabidopsis and strain YC7012.

Methods

Bioassay was conducted by co-cultivating Arabidopsis mutants of auxin (axr4–2, aux1–7 and eir1–1), ethylene (etr1), and jasmonic acid (jar1, coi1–1) with strain YC7012 in petri dishes compared to exogenous MeJA treatment. Auxin response was further determined by using transgenic line DR5::GUS. Volatile experiments were conducted in central partition plates (I-plates). Cell wall modification genes were investigated using qRT-PCR.

Results

All tested mutants showed significantly increased biomass with more lateral roots in the treated seedlings compared with the untreated mutants. Moreover, the co-cultivation of the strain YC7012 with the auxin response transgenic AtDR5::GUS did not distinctly show any visualized GUS signalling. Co-treatment of YC7012 with MeJA increased the number of lateral roots and biomass of Arabidopsis jar1. However, application of MeJA only failed to promote the growth of lateral root or biomass. Expression levels of cell wall modification genes EXPANSIN, EXPA5, and EXPB1, CHLOROPLAST LUMEN PROTIEN (CLP), and carbohydrate and cell wall biosynthesis gene REB1 were significantly up regulated by co-cultivation with strain YC7012. Strain YC7012 significantly increased plant biomass. Its effect was similar to volatile producing strains B. subtilis GBO3 and B. siamensis (KACC 15859T).

Conclusions

Strain YC7012 can promote the growth of Arabidopsis by producing volatile organic compounds independent of auxin, ethylene, or jasmonic acid signalling pathway.

Keywords

Auxin independent Bacillus siamensis Root development Volatile compound Ethylene-jasmonic acid independent 

Notes

Acknowledgments

This work was supported by the Brain Korea (BK) 21 Plus project funded by the Ministry of Education, Science and Technology. It was also supported by Cooperative Research Program for Agriculture Science & Technology Development (PJ 01104901) funded by Rural Development Administration, Republic of Korea. We thank J. Y. Kim (Gyeongsang National University) for providing Arabidopsis mutants of jar1, etr1, and transgenic construct DR5::GUS. We also thank M. J. Bennett (University of Nottingham) for providing auxin mutants aux1-7, axr4-2, and eir1-1. We are also thankful to C. M. Ryu for providing strain B. subtilis GB03.

Supplementary material

11104_2019_4015_MOESM1_ESM.doc (353 kb)
Supplementary Fig. S1 Effect of strain YC7012 on root system development in Arabidopsis ABA mutant (abi2–2) and SA degrading transgenic NahG inoculated with the strain or 10 mM MgSO4 as control at 8 days after co-cultivation. (a) Lateral root number/seedling. (b) Fresh weight/seedling. (c) Representative pictorial views. Data represent mean values ± SE of three replicates, each consisting of 10 seedlings. Different letters indicate statistically significant differences (P < 0.01) by Tukey’s HSD test. (DOC 353 kb)

References

  1. Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPRI. Mol Plant-Microbe Interact 20:759–768CrossRefGoogle Scholar
  2. Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudyarova GR (2005) Ability of bacterium Bacillus subtilis produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209CrossRefGoogle Scholar
  3. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319CrossRefGoogle Scholar
  4. Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252CrossRefGoogle Scholar
  5. Bennet MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schuluz B, Feldmann KA (1996) Arabidopsis Aux1 gene: a permease like regulator of root gravitropism. Science 273:948–950CrossRefGoogle Scholar
  6. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058CrossRefGoogle Scholar
  7. Bouizgarne B (2013) Bacteria for plant growth promotion and disease management. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, New York, pp 15–47CrossRefGoogle Scholar
  8. Chung EJ, Hossain MT, Khan A, Kim KH, Jeon CO, Chung YR (2015) Bacillus oryzicola sp. nov., an endophytic bacterium isolated from the roots of rice with anti-microbial, plant-growth-promoting, and systemic resistance-inducing activities in rice. Plant Pathol J 31:152–164CrossRefGoogle Scholar
  9. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693CrossRefGoogle Scholar
  10. Crane JM, Gibson DM, Vaughan RH, Bergstrom GC (2013) Iturin levels on wheat spikes linked to biological control of Fusarium head blight by Bacillus amyloliquefaciens. Phytopathology 103:146–155CrossRefGoogle Scholar
  11. D'Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TC (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37:813–826CrossRefGoogle Scholar
  12. Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M, Marchant A, Milli S, Sandberg G, Bennet MJ, Estelle M (2006) AXR4 is required for localization of the auxin influx facilitator Aux1. Science 312:1218–1220CrossRefGoogle Scholar
  13. Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interations between bacteria and fungi in the soil. J Chem Ecol 38:665–703CrossRefGoogle Scholar
  14. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clement C, Barka EA, Jacquard C, Dorey S (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:177–187CrossRefGoogle Scholar
  15. Franche C, Lindström K, Elmerich C (2009) Nitrogen fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59CrossRefGoogle Scholar
  16. Gnanamanickam SS (2009) An overview of progress in biological control. In: Gnanamanickam SS (ed) Biological control of rice diseases, progress in biological control. Springer, Dordrecht, pp 43–51Google Scholar
  17. Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbe Interact 20:619–626CrossRefGoogle Scholar
  18. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347CrossRefGoogle Scholar
  19. Jeong H, Jeong DE, Kim SH, Song GC, Park SY, Ryu CM, Park SH, Choi SK (2012) Draft genome sequence of the plant growth-promoting bacterium Bacillus siamensis KCTC 13613T. J Bacteriol 194:4148–4149CrossRefGoogle Scholar
  20. Joo GJ, Kim YM, Kim JT, Rhee IK, Kim JH, Lee IJ (2005) Gibberellins producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J Microbiol 43:510–515Google Scholar
  21. Khan A, Hossain MT, Park HC, Yun DJ, Shim SH, Chung YR (2016) Development of root system architecture of Arabidopsis thaliana in response to colonization by Martelella endophytica YC6887 depends on auxin signaling. Plant Soil 405:81–96.  https://doi.org/10.1007/s11104-015-2775-z CrossRefGoogle Scholar
  22. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102CrossRefGoogle Scholar
  23. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266CrossRefGoogle Scholar
  24. Kwon YS, Ryu CM, Lee S, Park HB, Han KS, Lee JH, Lee K, Chung WS, Jeong MJ, Kim HK, Bae DW (2010) Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232:1355–1370CrossRefGoogle Scholar
  25. Lee DS, Nioche P, Hamberg M, Raman CS (2008) Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455:363–368CrossRefGoogle Scholar
  26. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012) Induced resistance by a long chain bacterial volatile: elicitation of plant systemic defense by a C-13 volatile produced by Paenibacillus polymyxa. PLoS One 7:e48744CrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (−Delta Delta C (T)) method. Methods 25:402–408CrossRefGoogle Scholar
  28. López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin-and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant-Microbe Interact 20:207–217CrossRefGoogle Scholar
  29. Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root specific protein involved in auxin transport is required for gravitotropism in Arabidopsis thaliana. Genes Dev 12:2175–2187CrossRefGoogle Scholar
  30. Lynch J, Marschner P, Rengel Z (2012) Effect of internal and external factors on root growth and development. In: Marschner H (ed) Mineral nutrition of higher plants, Academic press, London, pp331–345Google Scholar
  31. Madhaiyan M, Poonguzhali S, Kwon SW, Sa TM (2010) Bacillus methylotrophicus sp. nov., a methanol utilizing, plant growth promoting bacterium isolated from rice rhizosphere soil. Int J Syst Evol Microbiol 60:2490–2495CrossRefGoogle Scholar
  32. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefGoogle Scholar
  33. Malamy JE, Benfey PN (1997) Organisation and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44Google Scholar
  34. Mantelin S, Touraine B (2004) Plant growth promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 55:27–34CrossRefGoogle Scholar
  35. McSpadden Gardener B (2010) Biocontrol of plant pathogens and plant growth promotion by Bacillus. In: Gishi U, Chet I, Lodovica Gullino M (eds) Recent developments in management of plant diseases, plant pathology in the 21st century. Springer, Amsterdam, pp 71–79CrossRefGoogle Scholar
  36. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100CrossRefGoogle Scholar
  37. Niinemetes Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:1–15Google Scholar
  38. Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate-and jasmonate/ethylene-dependent signaling pathways. Mol Plant-Microbe Interact 24:533–542CrossRefGoogle Scholar
  39. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125CrossRefGoogle Scholar
  40. Ortiz-Castro R, Valencia-Cantero E, Lopez-Bucio J (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signalling. Plant Signal Behav 3:263–265CrossRefGoogle Scholar
  41. Piechulla B, Schnitzler JP (2016) Circumvent CO2 effects in volatile-based microbe–plant interactions. Trends Plant Sci 21:541–543CrossRefGoogle Scholar
  42. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062CrossRefGoogle Scholar
  43. Rashid M, Khan A, Hossain MT, Chung YR (2017) Induction of systemic resistance against aphids by endophytic Bacillus velezensis YC7010 via expressing PHYTOALEXIN DEFICIENT4 in Arabidopsis. Front Plant Sci 8:211Google Scholar
  44. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9CrossRefGoogle Scholar
  45. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932CrossRefGoogle Scholar
  46. Sanchez L, Courteaux B, Hubert J, Kauffmann S, Renault JH, Clément C, Baillieul F, Dorey S (2012) Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol 160:1630–1641CrossRefGoogle Scholar
  47. Schrey SD, Erkenbrack E, Früh E, Fengler S, Hommel K, Horlacher N, Schulz D, Ecke M, Kulik A, Fiedler HP, Hampp R, Tarkka MT (2012) Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza associated streptomycetes. BMC Microbiol 12:1–14CrossRefGoogle Scholar
  48. Shi CL, Park HB, Lee JS, Ryu S, Ryu CM (2010) Inhibition of primary roots and stimulation of lateral root development in Arabidopsis thaliana by the rhizobacterium Serratia marcescens 90-166 is through both auxin-dependent and independent-signaling pathways. Mol Cells 29:251–258CrossRefGoogle Scholar
  49. Spaepen S (2015) Plant hormones produced by microbes. In: Lugtenberg B (ed) Principles of plant-microbe interaction. Springer, Cham, pp 247–256Google Scholar
  50. Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511CrossRefGoogle Scholar
  51. Sun L, Zhu L, Xu L, Yuan D, Min L, Zhang X (2014) Cotton cytochrome P450 CYP82D regulates systemic cell death by modulating the octadecanoid pathway. Nat Commun 5.  https://doi.org/10.1038/ncomms6372
  52. Timmusk S, Wagner EGH (1999) The plant growth promoting rhizobacteria Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant-Microbe Interact 12:951–959Google Scholar
  53. Vazquez P, Holguin G, Puente ME, Lopoz-Cortes A, Bashan Y (2000) Phosphate solubilizing microorganisms associated with rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468CrossRefGoogle Scholar
  54. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51CrossRefGoogle Scholar
  55. Weid I, Alviano DS, Santos ALS, Soares RMA, Alviano CS, Seldin L (2003) Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J Appl Microbiol 95:1143–1151CrossRefGoogle Scholar
  56. Yu JH, Keller N (2005) Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 43:437–458CrossRefGoogle Scholar
  57. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318CrossRefGoogle Scholar
  58. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mohammad Tofajjal Hossain
    • 1
    • 2
  • Ajmal Khan
    • 1
    • 3
  • Md. Harun-Or-Rashid
    • 1
    • 2
  • Young Ryun Chung
    • 1
    Email author
  1. 1.Division of Applied Life Science (BK21 Plus), Plant Molecular Biology and Biotechnology Research CenterGyeongsang National UniversityJinjuSouth Korea
  2. 2.Bangladesh Agricultural Research InstituteGazipurBangladesh
  3. 3.Department of BiotechnologyBacha Khan UniversityCharsaddaPakistan

Personalised recommendations