Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T01:08:28.601Z Has data issue: false hasContentIssue false
  • English
  • Français

Culturable endophytic bacteria from Phelipanche ramosa (Orobanchaceae) seeds

Published online by Cambridge University Press:  17 November 2020

Katarzyna Durlik Open the ORCID record for Katarzyna Durlik [Opens in a new window] ,
Paulina Żarnowiec ,
Renata Piwowarczyk  and
Wiesław Kaca
Katarzyna Durlik*
Affiliation:
Department of Microbiology and Parasitology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, 25-406Kielce, Poland
Paulina Żarnowiec
Affiliation:
Department of Microbiology and Parasitology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, 25-406Kielce, Poland
Renata Piwowarczyk
Affiliation:
Department of Microbiology and Parasitology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, 25-406Kielce, Poland
Wiesław Kaca
Affiliation:
Department of Microbiology and Parasitology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, 25-406Kielce, Poland
*
Author for Correspondence: Katarzyna Durlik, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Endophytic microbiomes play a beneficial role in the development and protection of plants. However, seed-borne endophytic bacteria have not yet been fully explored. Investigation of parasitic plants, whose existence depends on yet poorly understood and complicated relationships with microorganisms and hosts, is particularly crucial. Endophytic bacteria promote seed conservation and facilitate seed germination in soil. Several root holoparasites from the Orobanchaceae family are the most aggressive broomrape species, often causing serious yield losses in important crops. Parasitic plants are characterized by the production of a large number of some of the smallest seeds in the world's flora, allowing them to stay viable in the soil for several dozen years. This study's aim was to isolate and characterize the seed endophyte and surface bacteria of the most aggressive and widespread broomrape weed, Phelipanche ramosa. We isolated two endophytic bacteria from within the seeds which are closely related to Brevibacterium frigoritolerans and Bacillus simplex described as soil bacteria, highly resistant to environmental conditions, and as plant growth-promoting rhizobacteria. Moreover, we isolated three strains from the surface of non-sterile seeds; all three isolates were related to the Bacillus cereus group.

Keywords

BacillusBrevibacterium frigoritoleransbroomrapeholoparasitesPhelipanche ramosaseed endophytes
Type
Research Paper
Information
Seed Science Research , Volume 31 , Issue 1 , March 2021 , pp. 69 - 75
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bargabus, RL, Zidack, NK, Sherwood, JE and Jacobsen, BJ (2002) Characterisation of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiological and Molecular Plant Pathology 61, 289–298. doi:10.1006/pmpp.2003.0443.CrossRefGoogle Scholar
Bulgarelli, D, Schlaeppi, K, Spaepen, S, van Themaat, EVL and Schulze-Lefert, P (2013) Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology 64, 807–838. doi:10.1146/annurev-arplant-050312-120106.CrossRefGoogle Scholar
Dereeper, A, Audic, S, Claverie, JM and Blanc, G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology 10, 8–13. doi:10.1186/1471-2148-10-8.CrossRefGoogle ScholarPubMed
Du, E, Chen, X, Li, Q, Chen, F, Xu, H and Zhang, F (2020) Rhizoglomus intraradices and associated Brevibacterium frigoritolerans enhance the competitive growth of Flaveria bidentis. Plant and Soil. doi:10.1007/s11104-020-04594-1.CrossRefGoogle Scholar
Fitzpatrick, CR and Schneider, AC (2020) Unique bacterial assembly, composition, and interactions in a parasitic plant and its host. Journal of Experimental Botany 71, 2198–2209. doi:10.1093/jxb/erz572.CrossRefGoogle Scholar
Gadhave, KR, Devlin, PF, Ebertz, A, Ross, A and Gange, AC (2018) Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness, and community composition in a context-specific manner. Microbial Ecology 76, 741–750. doi:10.1007/s00248-018-1160-x.CrossRefGoogle Scholar
Huet, S, Pouvreau, J, Delage, E, Delgrange, S, Marais, C, Bahut, M, Delavault, P, Simier, P and Poulin, L (2020) Populations of the parasitic plant Phelipanche ramosa in fluence their seed microbiota. Frontiers in Plant Science 11, 1–16. doi:10.3389/fpls.2020.01075.CrossRefGoogle Scholar
Hyakumachi, M, Nishimura, M, Arakawa, T, Asano, S, Yoshida, S, Tsushima, S and Takahashi, H (2013) Bacillus thuringiensis suppresses bacterial wilt disease caused by Ralstonia solanacearum with systemic induction of defense-related gene expression in tomato. Microbes and Environments 28, 128–134. doi:10.1264/jsme2.ME12162.CrossRefGoogle ScholarPubMed
Iasur Kruh, L, Lahav, T, Abu-Nassar, J, Achdari, G, Salami, R, Freilich, S and Aly, R (2017) Host-parasite-bacteria triangle: the microbiome of the parasitic weed Phelipanche aegyptiaca and tomato-Solanum lycopersicum (Mill.) as a host. Frontiers in Plant Science 8, 1–9. doi:10.3389/fpls.2017.00269.CrossRefGoogle ScholarPubMed
Jarocki, P, Podleśny, M, Komoń-Janczara, E, Kucharska, J, Glibowska, A and Targoński, Z (2016) Comparison of various molecular methods for rapid differentiation of intestinal bifidobacteria at the species, subspecies and strain level. BMC Microbiology 16, 1–11. doi:10.1186/s12866-016-0779-3.CrossRefGoogle ScholarPubMed
Jiang, H, Dong, H, Zhang, G, Yu, B, Chapman, LR and Fields, MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Applied and Environmental Microbiology 72, 3832–3845. doi:10.1128/AEM.02869-05.CrossRefGoogle ScholarPubMed
Joel, DM, Bar, H, Mayer, AM, Verdoucq, V and Westwood, JH (2007) Characterization of a leading to germination Orobanche aegyptiaca, pp. 296–306 in Adkins, S and Ashmore, SCN (Eds), Seeds: biology, development and ecology. Wallingford, CAB International.Google Scholar
Joel, DM, Bar, H, Mayer, AM, Plakhine, D, Ziadne, H, Westwood, JH and Welbaum, GE (2012) Seed ultrastructure and water absorption pathway of the root-parasitic plant Phelipanche aegyptiaca (Orobanchaceae). Annals of Botany 109, 181–195. doi:10.1093/aob/mcr261.CrossRefGoogle Scholar
Johnston-Monje, D and Raizada, MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6, doi:10.1371/journal.pone.0020396.CrossRefGoogle ScholarPubMed
Klein, O and Kroschel, J (2002) Biological control of Orobanche spp. with Phytomyza orobanchia, a review. BioControl 47, 245–277. doi:10.1023/A:1014862302818.CrossRefGoogle Scholar
Köhl, J, Medeiros, FHV, Lombaers-van der Plas, C, Groenenboom-de Haas, L and van den Bosch, T (2020) Efficacies of bacterial and fungal isolates in biocontrol of Botrytis cinerea and Pseudomonas syringae pv. tomato and growth promotion in tomato do not correlate. Biological Control 150, 104375. doi:10.1016/j.biocontrol.2020.104375.CrossRefGoogle Scholar
Linke, KH, Sauerborne, J and Saxena, MC (1992) Options for biological control of the parasitic weed Orobanche, pp. 633–40 in Delfosse ES and Scott RR (Eds) Proceedings of the Eight International Symposium on Biological Control of Weeds, 2–7 February 1992, DSIR/CSIRO, Melbourne. Canterbury, New Zealand: Lincoln University. https://www.invasive.org/proceedings/pdfs/8_633-640.pdfGoogle Scholar
Liu, YH, Guo, JW, Salam, N, Li, L, Zhang, YG, Han, J, Mohamad, OA and Li, WJ (2016) Culturable endophytic bacteria associated with medicinal plant Ferula songorica: molecular phylogeny, distribution and screening for industrially important traits. Biotech 6, doi:10.1007/s13205-016-0522-7.Google ScholarPubMed
Liu, Y, Du, J, Lai, Q, Zeng, R, Ye, D, Xu, J and Shao, Z (2017) Proposal of nine novel species of the Bacillus cereus group. International Journal of Systematic and Evolutionary Microbiology 67, 2499–2508. doi:10.1099/ijsem.0.001821.CrossRefGoogle ScholarPubMed
Malfanova, N, Lugtenberg, BJJ and Berg, G (2013) Bacterial endophytes: who and where, and what are they doing there? Molecular Microbial Ecology of the Rhizosphere 1, 391–403. doi:10.1002/9781118297674.ch36.CrossRefGoogle Scholar
Meena, TN and Saharan, BS (2017) Plant growth promoting traits shown by bacteria Brevibacterium frigrotolerans SMA23 isolated from Aloe vera rhizosphere. Agricultural Science Digest 37, 226–231. doi:10.18805/asd.v37i03.9223.Google Scholar
Méndez-Bravo, A, Cortazar-Murillo, EM, Guevara-Avendaño, E, Ceballos-Luna, O, Rodríguez-Haas, B, Kiel-Martínez, AL, Hernández-Cristóbal, O, Guerrero-Analco, JA and Reverchon, F (2018) Plant growth-promoting rhizobacteria associated with avocado display antagonistic activity against Phytophthora cinnamomi through volatile emissions. PLoS One 13, 1–18. doi:10.1371/journal.pone.0194665.CrossRefGoogle ScholarPubMed
Meulenbeld, GH and Hartmans, S (2001) Thioglucosidase activity from Sphingo bacterium sp. strain OTG1. Applied Microbiology and Biotechnology 56, 700–706. doi:10.1007/s002530100726.CrossRefGoogle Scholar
Neher, OT, Johnston, MR, Zidack, NK and Jacobsen, BJ (2009) Evaluation of Bacillus mycoides isolate BmJ and B. mojavensis isolate 203-7 for the control of anthracnose of cucurbits caused by Glomerella cingulata var. orbiculare. Biological Control 48, 140–146. doi:10.1016/j.biocontrol.2008.08.012.CrossRefGoogle Scholar
Pal, G, Kumar, K, Verma, A, White, JF and Verma, SK (2019) Functional roles of seed-inhabiting endophytes of rice, pp. 213–236 in Kumar, S; James, V and White, F Jr (Eds) Seed endophytes, Cham, Springer. Nature Switzerland. doi:10.1007/978-3-030-10504-4_11.CrossRefGoogle Scholar
Piwowarczyk, R (2015) Seed micromorphology of central European Orobanche and Phelipanche (Orobanchaceae) in relation to preferred hosts and systematic implications. Australian Systematic Botany 28, 124–136. doi:10.1071/SB15007.CrossRefGoogle Scholar
Piwowarczyk, R, Mielczarek, Ł and Guzikowski, S (2018) First report of Phytomyza orobanchia (Diptera: Agromyzidae) from Poland and Chymomyza amoena (Diptera: Drosophilidae) on Phelipanche ramosa (Orobanchaceae). Florida Entomologist 101, 540–542. doi:10.1653/024.101.0333.CrossRefGoogle Scholar
Raymond, B and Federici, BA (2017) In defense of Bacillus thuringiensis, the safest and most successful microbial insecticide available to humanity – a response to EFSA. FEMS Microbiology Ecology 93, fix084. doi:10.1093/femsec/fix084.CrossRefGoogle ScholarPubMed
Román-Ponce, B, Li, YH, Vásquez-Murrieta, MS, Sui, XH, Chen, WF, Estrada-de los Santos, P and Wang, ET (2015) Brevibacterium metallicus sp. nov., an endophytic bacterium isolated from roots of Prosopis laegivata grown at the edge of a mine tailing in Mexico. Archives of Microbiology 197, 1151–1158. doi:10.1007/s00203-015-1156-6.CrossRefGoogle ScholarPubMed
Sánchez-López, AS, Thijs, S, Beckers, B, González-Chávez, MC, Weyens, N, Carrillo-González, R and Vangronsveld, J (2018) Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues. Plant and Soil 422, 51–66. doi:10.1007/s11104-017-3176-2.CrossRefGoogle Scholar
Selvakumar, G, Sushil, SN, Stanley, J, Mohan, M, Deol, A, Rai, D, Ramkewal, , Bhatt, JC and Gupta, HS (2011) Brevibacterium frigoritolerans a novel entomopathogen of Anomala dimidiata and Holotrichia longipennis (Scarabaeidae: Coleoptera). Biocontrol Science and Technology 21, 821–827. doi:10.1080/09583157.2011.586021.CrossRefGoogle Scholar
Shahzad, R, Khan, AL, Bilal, S, Asaf, S and Lee, IJ (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Frontiers in Plant Science 9, 1–10. doi:10.3389/fpls.2018.00024.CrossRefGoogle ScholarPubMed
Tomassetti, MC, Cirigliano, A, Arrighi, C, Negri, R, Mura, F, Maneschi, ML, Gentili, MD, Stirpe, M, Mazzoni, C and Rinaldi, T (2017) A role for microbial selection in frescoes’ deterioration in Tomba degli Scudi in Tarquinia, Italy. Scientific Reports 7, 1–8. doi:10.1038/s41598-017-06169-0.CrossRefGoogle ScholarPubMed
Truyens, S, Weyens, N, Cuypers, A and Vangronsveld, J (2015) Bacterial seed endophytes: Genera, vertical transmission and interaction with plants. Environmental Microbiology Reports 7, 40–50. doi:10.1111/1758-2229.12181.CrossRefGoogle Scholar
Truyens, S, Beckers, B, Thijs, S, Weyens, N, Cuypers, A and Vangronsveld, J (2016) Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana. Plant Biology 18, 376–381. doi:10.1111/plb.12415.CrossRefGoogle ScholarPubMed
Turnau, K, Jędrzejczyk, R, Domka, A, Anielska, T and Piwowarczyk, R (2018) Expansion of a holoparasitic plant, Orobanche lutea (Orobanchaceae), in post-industrial areas – a possible Zn effect. Science of the Total Environment 639, 714–724. doi:10.1016/j.scitotenv.2018.05.189.CrossRefGoogle Scholar
Walitang, DI, Kim, K, Madhaiyan, M, Kim, YK, Kang, Y and Sa, T (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of rice. BMC Microbiology 17, 1–13. doi:10.1186/s12866-017-1117-0.CrossRefGoogle ScholarPubMed
Wang, JP, Liu, B, Liu, GH, Chen, Q, Pan, Z, Zheng, XF and Chen, M (2016) Draft genome sequence of Bacillus muralis LMG 20238 T (DSM 16288), a spore-forming bacterium isolated from deteriorated mural paintings. Genome Announcements 4, 20238. doi:10.1128/genomeA.01691-15.Google Scholar
Wright, E and Wang, ZY (2014) Medicago truncatula transformation using cotyledonary explants. Agrobacterium Protocols: third Edition 1, 35–41. doi:10.1007/978-1-4939-1695-5_3.Google Scholar
Yi, Y, de Jong, A, Frenzel, E and Kuipers, OP (2017) Comparative transcriptomics of Bacillus mycoides root exudates reveals different genetic adaptation of endophytic and soil isolates. Frontiers in Microbiology 8, 1–14. doi:10.3389/fmicb.2017.01487.CrossRefGoogle ScholarPubMed
Zwanenburg, B, Pospíšil, T and Ćavar Zeljković, S (2016) Strigolactones: new plant hormones in action. Planta 243, 1311–1326. doi:10.1007/s00425-015-2455-5.CrossRefGoogle ScholarPubMed