SpringerLink
Log in

Microorganisms Associated with the Ambrosial Beetle Xyleborus affinis with Plant Growth-Promotion Activity in Arabidopsis Seedlings and Antifungal Activity Against Phytopathogenic Fungus Fusarium sp. INECOL_BM-06

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Plants interact with a great diversity of microorganisms or insects throughout their life cycle in the environment. Plant and insect interactions are common; besides, a great variety of microorganisms associated with insects can induce pathogenic damage in the host, as mutualist phytopathogenic fungus. However, there are other microorganisms present in the insect-fungal association, whose biological/ecological activities and functions during plant interaction are unknown. In the present work evaluated, the role of microorganisms associated with Xyleborus affinis, an important beetle species within the Xyleborini tribe, is characterized by attacking many plant species, some of which are of agricultural and forestry importance. We isolated six strains of microorganisms associated with X. affinis shown as plant growth-promoting activity and altered the root system architecture independent of auxin-signaling pathway in Arabidopsis seedlings and antifungal activity against the phytopathogenic fungus Fusarium sp. INECOL_BM-06. In addition, evaluating the tripartite interaction plant-microorganism-fungus, interestingly, we found that microorganisms can induce protection against the phytopathogenic fungus Fusarium sp. INECOL_BM-06 involving the jasmonic acid-signaling pathway and independent of salicylic acid-signaling pathway. Our results showed the important role of this microorganisms during the plant- and insect-microorganism interactions, and the biological potential use of these microorganisms as novel agents of biological control in the crops of agricultural and forestry is important.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of Data and Material

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

  1. Camarena Gutiérrez G (2009) Señales en la interacción planta insecto. Revista Cha**o. Serie ciencias forestales y del ambiente 15(1):81–85

    Google Scholar 

  2. Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55(10):2011–2027

    CAS  PubMed  Google Scholar 

  3. Heil M (2010) Ant–plant mutualisms. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester. https://doi.org/10.1002/9780470015902.a0022558

  4. Velasco YAM, Ropero MG, Armbrecht I (2010) Interacciones entre hormigas e insectos en follaje de cafetales de sol y sombra. Cauca-Colombia Revista Colombiana de Entomología 36(1):116–126

    Article  Google Scholar 

  5. Cruz LF, Menocal O, Mantilla J, Ibarra-Juarez LA, Carrillo D (2019) Xyleborus volvulus (Coleoptera: Curculionidae): biology and fungal associates. Appl Environ Microbiol 85(19):e01190-e1219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Carrillo, J. D., Dodge, C., Stouthamer, R., & Eskalen, A. (2020). Fungal symbionts of the polyphagous and Kuroshio shot hole borers (Coleoptera: Scolytinae, Euwallacea spp.) in California can support both ambrosia beetle systems on artificial media. Symbiosis 80(2):155–168.

  7. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36:563–595

    Article  Google Scholar 

  8. Castrejón-Antonio JE, Montesinos-Matías R, Acevedo-Reyes N, Tamez-Guerra P, Ayala-Zermeño MÁ, Berlanga-Padilla AM, Arredondo-Bernal HC (2017) Especies de Xyleborus (Coleoptera: Curculionidae: Scolytinae) asociados a huertos de aguacate en Colima. México Acta zoológica mexicana 33(1):146–150

    Article  Google Scholar 

  9. Carrillo D, Duncan RE, Ploetz JN, Campbell AF, Ploetz RC, Peña JE (2014) Lateral transfer of a phytopathogenic symbiont among native and exotic ambrosia beetles. Plant Pathol 63(1):54–62

    Article  Google Scholar 

  10. Granada-Giro C (2003) Xyleborus affinis (Eichh) (Coleoptera: Scolytidae) atacando plantaciones de caña de azúcar en la provincia de Santiago de Cuba. Fitosanidad 7(1):61–61

    Google Scholar 

  11. Kostovcik M, Bateman CC, Kolarik M, Stelinski LL, Jordal BH, Hulcr J (2015) The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J 9(1):126–138

    Article  CAS  PubMed  Google Scholar 

  12. Hulcr J, Rountree NR, Diamond SE, Stelinski LL, Fierer N, Dunn RR (2012) Mycangia of ambrosia beetles host communities of bacteria. Microb Ecol 64(3):784–793

    Article  CAS  PubMed  Google Scholar 

  13. Miyashita, A., Hirai, Y., Sekimizu, K., & Kaito, C. (2015). Antibiotic-producing bacteria from stag beetle mycangia. Drug Discov Therapeut 9(1):33–37. https://doi.org/10.5582/ddt.2015.01000

  14. Tanahashi M, Kubota K, Matsushita N, Togashi K (2010) Discovery of mycangia and the associated xylose-fermenting yeasts in stag beetles (Coleoptera: Lucanidae). Naturwissenschaften 97(3):311–317

    Article  CAS  PubMed  Google Scholar 

  15. Kousar B, Bano A, Khan N (2020) PGPR modulation of secondary metabolites in tomato infested with Spodoptera litura. Agronomy 10(6):778

    Article  Google Scholar 

  16. Mishra, J., Singh, R., & Arora, N. K. (2017). Plant growth-promoting microbes: diverse roles in agriculture and environmental sustainability. In Probiotics and plant health (pp. 71–111). Springer, Singapore.

  17. Tzec-Interián JA, Desgarennes D, Carrión G, Monribot-Villanueva JL, Guerrero-Analco JA, Ferrera-Rodríguez O, ... & Ortiz-Castro R (2020) Characterization of plant growth-promoting bacteria associated with avocado trees (Persea americana Miller) and their potential use in the biocontrol of Scirtothrips perseae (avocado thrips). Plos one, 15(4), e0231215.

  18. Tamura K, Peterson D, Peterson N, Stecher G, Ne M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Castillo-Esparza JF, Hernández-González I, Ibarra JE (2019) Search for Cry proteins expressed by Bacillus spp. genomes, using hidden Markov model profiles. 3 Biotech 9:13. https://doi.org/10.1007/s13205-018-1533-3

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Colón-Carmona A, You R, Haimovitch-Gal T, Doermer P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  PubMed  Google Scholar 

  22. Sieberer T, Hauser MT, Seifert GJ, Lusching C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842

    Article  CAS  PubMed  Google Scholar 

  23. Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, … & Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6(9): e230

  24. Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact 10(1):69–78

    Article  CAS  PubMed  Google Scholar 

  25. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, ... & Browse J (2007) JAZ repressor proteins are targets of the SCF COI1 complex during jasmonate signalling. Nature 448(7154): 661-665

  26. Castillo-Esparza JF, Bandala VM, Ramos A, Desgarennes D, Carrión G, César E, ... & Ortiz-Castro R (2021) Pisolithus tinctorius extract affects the root system architecture through compound production with auxin-like activity in Arabidopsis thaliana. Rhizosphere 19: 100397

  27. Ortiz-Castro R, Campos-García J, López-Bucio J (2020) Pseudomonas putida and Pseudomonas fluorescens influence Arabidopsis root system architecture through an auxin response mediated by bioactive cyclodipeptides. J Plant Growth Regul 39(1):254–265.

  28. Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, Rosa E, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci 108(17):7253–7258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jiménez‐Vázquez KR, García‐Cárdenas E, Barrera‐Ortiz S, Ortiz‐Castro R, Ruiz‐Herrera LF, Ramos‐Acosta BP, ... & López‐Bucio J (2020) The plant beneficial rhizobacterium Achromobacter sp. 5B1 influences root development through auxin signaling and redistribution. Plant J 103(5):1639–1654

  30. Lim SM, Yoon MY, Choi GJ, Choi YH, Jang KS, Shin TS, Park HW, Yu NH, Kim YH, Kim JC (2017) Diffusible and volatile antifungal compounds produced by an antagonistic Bacillus velezensis G341 against various phytopathogenic fungi. Plant Pathol J 33(5):488–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Doncel P, Pérez-Cordero A (2017) Burkholderia cepacia isolated from varieties of yam with antimicrobial activity against Colletotrichum gloeosporioides. Revista Colombiana de Ciencia Animal-RECIA 9(S1):31–38. https://doi.org/10.24188/recia.v9.nS.2017.518

  32. Elizarraraz-Martínez IJ, Navarro-Meléndez AL, Morales-Vargas AT (2015) Análisis in vitro de las interacciones entre hongos endófitos de frijol lima (Phaseolus lunatus). JÓVENES EN LA CIENCIA 2(1):60–64

    Google Scholar 

  33. Kumar S, Kaushik N (2013) Endophytic fungi isolated from oil-seed crop Jatropha curcas produces oil and exhibit antifungal activity. PloS one 8(2):e56202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    Article  CAS  PubMed  Google Scholar 

  35. Ortiz-Castro R, Pelagio-Flores R, Méndez-Bravo A, Ruiz-Herrera LF, Campos-García J, López-Bucio J (2014) Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Mol Plant Microbe Interact 27(4):364–378

    Article  CAS  PubMed  Google Scholar 

  36. Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4(8):701–712

    Article  PubMed  PubMed Central  Google Scholar 

  37. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95(5):707–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal-and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav 6(10):1554–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15(3):e2001793

    Article  PubMed  PubMed Central  Google Scholar 

  40. Ortiz-Castro R, Campos-García J, López-Bucio J (2020) Pseudomonas putida and Pseudomonas fluorescens influence Arabidopsis root system architecture through an auxin response mediated by bioactive cyclodipeptides. J Plant Growth Regul 39(1):254–265

    Article  CAS  Google Scholar 

  41. García-Cardenas E, Ortiz-Castro R, Ruiz-Herrera LF, Valencia-Cantero E, López-Bucio J (2021) Micrococcus luteus LS570 promotes root branching in Arabidopsis via decreasing apical dominance of the primary root and an enhanced auxin response. Protoplasma. https://doi.org/10.1007/s00709-021-01724-z

    Article  PubMed  Google Scholar 

  42. Meiners T (2015) Chemical ecology and evolution of plant-insect interactions: a multitrophic perspective. Current Opinion Insect Science 8:22–28

    Article  Google Scholar 

  43. Ibarra-Juarez LA, Burton MAJ, Biedermann PHW, Cruz L, Desgarennes D, Ibarra-Laclette E, Latorre A, Alonso-Sánchez A, Villafan E, Hanako-Rosas G, López L, Vázquez-Rosas-Landa M, Carrion G, Carrillo D, Moya A, Lamelas A (2020) Evidence for succession and putative metabolic roles of fungi and bacteria in the farming mutualism of the ambrosia beetle Xyleborus affinis. Msystems 5(5):e00541-20. https://doi.org/10.1128/mSystems.00541-20

  44. Saucedo-Carabez JR, Ploetz RC, Konkol JL, Carrillo D, Gazis R (2018) Partnerships between ambrosia beetles and fungi: lineage-specific promiscuity among vectors of the laurel wilt pathogen, Raffaelea lauricola. Microbial ecology 76(4):925–940

    Article  CAS  PubMed  Google Scholar 

  45. Morales-Jiménez J, Zúñiga G, Villa-Tanaca L, Hernández-Rodríguez C (2009) Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microb Ecol 58(4):879–891

    Article  PubMed  Google Scholar 

  46. Ignatova LV, Brazhnikova YV, Berzhanova RZ, Mukasheva TD (2015) Plant growth-promoting and antifungal activity of yeasts from dark chestnut soil. Microbiol Res 175:78–83. https://doi.org/10.1016/j.micres.2015.03.008

    Article  CAS  PubMed  Google Scholar 

  47. Amprayn KO, Rose MT, Kecskés M, Pereg L, Nguyen HT, Kennedy IR (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299. https://doi.org/10.1016/j.apsoil.2011.11.009

    Article  Google Scholar 

  48. Zuluaga MYA, Lima Milani KM, Azeredo Gonçalves LS, Martinez de Oliveira AL (2020) Diversity and plant growth-promoting functions of diazotrophic/N-scavenging bacteria isolated from the soils and rhizospheres of two species of Solanum. PLoS ONE 15(1):e0227422. https://doi.org/10.1371/journal.pone.0227422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Criollo PJ, Obando M, Sánchez L, Bonilla R (2012) Effect of plant growth-promoting rhizobacteria (PGPR) associated to Pennisetum clandestinum in the altiplano cundiboyacense. Ciencia y Tecnología Agropecuaria 13(2):189–195

    Article  Google Scholar 

  50. Idris HA, Labuschagne N, & Korsten L (2009) Efficacy of rhizobacteria for growth promotion in sorghum under greenhouse conditions and selected modes of action studies. https://doi.org/10.1017/S0021859608008174

  51. Arora NK, Fatima T, Mishra J, Mishra I, Verma S, Verma R, … & Bharti C (2020) Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. J Adv Res. 26: 69-82

  52. Sezen A, Ozdal M, Koc K, Algur OF (2016) Isolation and characterization of plant growth promoting rhizobacteria (PGPR) and their effects on improving growth of wheat. J Appl Biol Sci 10(1):41–46

    Google Scholar 

  53. Erturk Y, Ercisli S, Haznedar A, Cakmakci R (2010) Effects of plant growth promoting rhizobacteria (PGPR) on rooting and root growth of kiwifruit (Actinidia deliciosa) stem cuttings. Biol Res 43(1):91–98

    Article  PubMed  Google Scholar 

  54. Govindasamy V, Senthilkumar M, Magheshwaran V, Kumar U, Bose P, Sharma V, & Annapurna K (2010) Bacillus and Paenibacillus spp.: potential PGPR for sustainable agriculture. In Plant growth and health promoting bacteria (pp. 333–364). Springer, Berlin, Heidelberg

  55. Goswami D, Parmar S, Vaghela H, Dhandhukia P, Thakker JN (2015) Describing Paenibacillus mucilaginosus strain N3 as an efficient plant growth promoting rhizobacteria (PGPR). Cogent Food & Agriculture 1(1):1000714

    Article  Google Scholar 

  56. Yaoyao E, Yuan J, Yang F, Wang L, Ma J, Li J, ... & Shen Q (2017) PGPR strain Paenibacillus polymyxa SQR-21 potentially benefits watermelon growth by re-sha** root protein expression. AMB Express 7(1): 1–12

  57. Fu SF, Sun PF, Lu HY, Wei JY, **ao HS, Fang WT, ... & Chou JY (2016) Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spatulata Lab. Fungal biology, 120(3), 433–448

  58. Chen PH, Chen RY, Chou JY (2018) Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology 46(1):33–46

    Article  PubMed  PubMed Central  Google Scholar 

  59. Messiha NAS, Van Diepeningen AD, Farag NS, Abdallah SA, Janse JD, Van Bruggen AHC (2007) Stenotrophomonas maltophilia: a new potential biocontrol agent of Ralstonia solanacearum, causal agent of potato brown rot. Eur J Plant Pathol 118(3):211–225

    Article  Google Scholar 

  60. Giesler LJ, Yuen GY (1998) Evaluation of Stenotrophomonas maltophilia strain C3 for biocontrol of brown patch disease. Crop Prot 17(6):509–513

    Article  Google Scholar 

  61. Camañes G, Scalschi L, Vicedo B, González-Bosch C, García-Agustín P (2015) An untargeted global metabolomic analysis reveals the biochemical changes underlying basal resistance and priming in Solanum lycopersicum, and identifies 1-methyltryptophan as a metabolite involved in plant responses to Botrytis cinerea and Pseudomonas syringae. Plant J 84(1):125–139

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the grants no. PDCPN-2015-882, FORDECyT-PRONACES 292399. J. F. C.-E. thanks FORDECYT-PRONACES for his postdoctoral fellowship. K. A. M.-V. thanks FORDECYT-PRONACES for his bachelor fellowship. We thank Molecular Biology Laboratory of the Institute of Ecology A. C., for providing us with the strain of the phytopathogenic fungus Fusarium sp. INECOL_BM-06. We thank L. A. I.-J. for providing us with Xyleborus affinis beetle for microorganism isolation. We thank B. R.-H. for isolation of DNA and amplification of 16S rRNA gene.

Funding

This work was financed by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, grants PDCPN-2015–882 and FORDECYT-PRONACES 292399).

Author information

Author notes

  1. J. Francisco Castillo-Esparza

    Present address: Red de Biodiversidad Y Sistemática, Instituto de Ecología A.C, Carretera Antigua a Coatepec 351, El Haya, 91073, Xalapa, Veracruz, México

  2. Diana Sánchez-Rangel & Luis A. Ibarra-Juárez

    Present address: Cátedra CONACyT en el Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, El Haya, C.P. 91073, Xalapa, Veracruz, Mexico

Authors and Affiliations

  1. Red de Estudios Moleculares Avanzados, Instituto de Ecología A.C, Xalapa, 91073, Veracruz, México

    J. Francisco Castillo-Esparza, Karen A. Mora-Velasco, Greta H. Rosas-Saito, Benjamín Rodríguez-Haas, Diana Sánchez-Rangel, Luis A. Ibarra-Juárez & Randy Ortiz-Castro

  2. Cátedra CONACyT en el Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, El Haya, C.P. 91073, Xalapa, Veracruz, Mexico

    Randy Ortiz-Castro

Authors
  1. J. Francisco Castillo-Esparza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen A. Mora-Velasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Greta H. Rosas-Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamín Rodríguez-Haas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Diana Sánchez-Rangel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luis A. Ibarra-Juárez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Randy Ortiz-Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JFCE, KAMV, DSR, LAIJ, and ROC conceived and designed the experiments; JFCE, KAMV, GHRS, and BRH performed experiments; JFCE, KAMV, and ROC analyzed the data; ROC contributed reagents/materials/analysis tools; JFCE and ROC wrote the paper; and JFCE and ROC reviewed and edited the paper. DSR and ROC applied for funding.

Corresponding author

Correspondence to Randy Ortiz-Castro.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (JPG 674 kb)

Supplementary file2 (JPG 932 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castillo-Esparza, J.F., Mora-Velasco, K.A., Rosas-Saito, G.H. et al. Microorganisms Associated with the Ambrosial Beetle Xyleborus affinis with Plant Growth-Promotion Activity in Arabidopsis Seedlings and Antifungal Activity Against Phytopathogenic Fungus Fusarium sp. INECOL_BM-06. Microb Ecol 85, 1396–1411 (2023). https://doi.org/10.1007/s00248-022-01998-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-022-01998-7

Keywords

Search

Navigation