Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-29T19:02:02.416Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization and diversity of seed endophytic bacteria of the endemic holoparasitic plant Cistanche armena (Orobanchaceae) from a semi-desert area in Armenia

Published online by Cambridge University Press:  18 October 2022

Kristine Petrosyan Open the ORCID record for Kristine Petrosyan [Opens in a new window] ,
Sofie Thijs Open the ORCID record for Sofie Thijs [Opens in a new window] ,
Renata Piwowarczyk Open the ORCID record for Renata Piwowarczyk [Opens in a new window] ,
Karolina Ruraż Open the ORCID record for Karolina Ruraż [Opens in a new window] ,
Jaco Vangronsveld Open the ORCID record for Jaco Vangronsveld [Opens in a new window]  and
Wiesław Kaca Open the ORCID record for Wiesław Kaca [Opens in a new window]
Kristine Petrosyan*
Affiliation:
Department of Microbiology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, Kielce 25-406, Poland Centre for Environmental Sciences, Environmental Biology Research Group, Hasselt University, Agoralaan Building D, Diepenbeek 3590, Belgium
Sofie Thijs
Affiliation:
Centre for Environmental Sciences, Environmental Biology Research Group, Hasselt University, Agoralaan Building D, Diepenbeek 3590, Belgium
Renata Piwowarczyk
Affiliation:
Center for Research and Conservation of Biodiversity, Department of Environmental Biology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, Kielce 25-406, Poland
Karolina Ruraż
Affiliation:
Center for Research and Conservation of Biodiversity, Department of Environmental Biology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, Kielce 25-406, Poland
Jaco Vangronsveld
Affiliation:
Centre for Environmental Sciences, Environmental Biology Research Group, Hasselt University, Agoralaan Building D, Diepenbeek 3590, Belgium Institute of Biological Sciences, Department of Plant Physiology and Biophysics, Faculty of Biology and Biotechnology, Maria Curie-Skłodowska University, 19 Akademicka, Lublin 20-033, Poland
Wiesław Kaca
Affiliation:
Department of Microbiology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7, Kielce 25-406, Poland
*
*Author for Correspondence: Kristine Petrosyan, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We explored the seed-associated bacterial endophytic microbiome in seeds of the endemic holoparasitic species Cistanche armena from a saline and arid habitat in Armenia. A combination of culture-dependent and molecular techniques was employed for identifying the seed endomicrobiome (culturable and unculturable). From surface-sterilized seeds, 10 phyla, comprising 256 endophytic bacterial genera, were identified. Of the culturable strains, we also investigated the plant growth-promoting (PGP) traits. Most of the isolates were spore forming, halotolerant and alkaliphile Bacillus spp., indicating that the endophytic bacteria of C. armena seeds own traits related to the natural habitat of their host plant. Our results confirm that Bacillus species are common and dominated endophytes from plants growing on saline and arid soils. Pantoea spp. and Stenotrophomonas spp. are more favourable PGP endophytes in seeds of C. armena. The PGP traits of these bacteria, such as production of indole, a precursor of auxin, ACC-deaminase and organic acids have the potential to improve the tolerance of their host plants against the abiotic stresses present in their natural habitat. To the best of our knowledge, this is the first report concerning bacterial seed endophytes of the C. armena.

Keywords

abiotic stressBacillusdust seedsPantoeaparasitic plantsPGP traitsseed microbiome
Type
Research Paper
Information
Seed Science Research , Volume 32 , Issue 4 , December 2022 , pp. 264 - 273
Check for updates
Copyright
Copyright © The Author(s), 2022. 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

Ambawade, MS and Pathade, GR (2015) Production of indole acetic acid (IAA) by Stenotrophomonas maltophilia BE25 isolated from roots of banana (Musa spp). International Journal of Science and Research 4, 2644–2650.Google Scholar
Asaf, S, Aaqil Khan, M, Latif Khan, A, Waqas, M, Shahzad, R, Kim, A-Y, Kang, S-M and Lee, I-J (2017) Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. Journal of Plant Interactions 12, 31–38. doi:10.1080/17429145.2016.1274060CrossRefGoogle Scholar
Barret, M, Guimbaud, J-F, Darrasse, A and Jacques, M-A (2016) Plant microbiota affects seed transmission of phytopathogenic microorganisms. Molecular Plant Pathology 17, 791–795. doi:10.1111/mpp.12382CrossRefGoogle ScholarPubMed
Barthlott, W (1981) Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic Journal of Botany 1, 345–355. doi:10.1111/j.1756-1051.1981.tb00704.xCrossRefGoogle Scholar
Belimov, AA, Hontzeas, N, Safronova, VI, Demchinskaya, SV, Piluzza, G, Bullitta, S and Glick, BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biology and Biochemistry 37, 241–250. doi:10.1016/j.soilbio.2004.07.033CrossRefGoogle Scholar
Callahan, BJ, McMurdie, PJ, Rosen, MJ, Han, AW, Johnson, AJ and Holmes, SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583. doi:10.1038/nmeth.3869CrossRefGoogle ScholarPubMed
Compant, S, Samad, A, Faist, H and Sessitsch, A (2019) A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. Journal of Advanced Research 19, 29–37. doi:10.1016/j.jare.2019.03.004CrossRefGoogle ScholarPubMed
Cunningham, JE and Kuiack, C (1992) Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaii. Applied Environmental Microbiology 58, 1451–1458. https://journals.asm.org/doi/10.1128/aem.58.5.1451-1458.1992CrossRefGoogle ScholarPubMed
Davis, NM, Proctor, DM, Holmes, SP, Relman, DA and Callahan, BJ (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226. doi:10.1186/s40168-018-0605-2CrossRefGoogle ScholarPubMed
Dinesh, R, Anandaraj, M, Kumar, A, Bini, YK, Subila, KP and Aravind, R (2015) Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting and disease suppressing effects on ginger. Microbiological Research 173, 34–43. doi:10.1016/j.micres.2015.01.014CrossRefGoogle ScholarPubMed
Durlik, K, Żarnowiec, P, Piwowarczyk, R and Kaca, W (2021) Culturable endophytic bacteria from Phelipanche ramosa (Orobanchaceae) seeds. Seed Science Research 31, 69–75. doi:10.1017/S0960258520000343CrossRefGoogle Scholar
Eevers, N, Gielen, M, Sánchez-López, A, Jaspers, S, White, JC, Vangronsveld, J and Weyens, N (2015) Optimization of isolation and cultivation of bacterial endophytes through addition of plant extract to nutrient media. Microbial Biotechnology 8, 707–715. doi:10.1111/1751-7915.12291CrossRefGoogle ScholarPubMed
Eriksson, O and Kainulainen, K (2011) The evolutionary ecology of dust seeds. Perspectives in Plant Ecology, Evolution and Systematics 13, 73–87. doi:10.1016/j.ppees.2011.02.002CrossRefGoogle Scholar
Etesami, H and Beattie, GA (2018) Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Frontiers in Microbiology 9, 148. doi:10.3389/fmicb.2018.00148CrossRefGoogle ScholarPubMed
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/erz572CrossRefGoogle Scholar
Frank, AC, Saldierna Guzmán, JP and Shay, JE (2017) Transmission of bacterial endophytes. Microorganisms 5, 70. doi:10.3390/microorganisms5040070CrossRefGoogle ScholarPubMed
Glassner, H, Zchori-Fein, E, Yaron, S, Sessitsch, A, Sauer, U and Compant, S (2018) Bacterial niches inside seeds of Cucumis melo L. Plant and Soil 422, 101–113. doi:10.1007/s11104-017-3175-3CrossRefGoogle Scholar
Grobelak, A, Kokot, P, Świątek, J, Jaskulak, M and Rorat, A (2018) Bacterial ACC deaminase activity in promoting plant growth on areas contaminated with heavy metals. Journal of Ecological Engineering 19, 150–157. doi:10.12911/22998993/89818CrossRefGoogle Scholar
Hallmann, J, Quadt-Hallmann, A, Mahaffee, WF and Kloepper, JW (1997) Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology 43, 895–914. doi:10.1139/m97-131CrossRefGoogle Scholar
Hassan, TU and Bano, A (2016) Comparative effects of wild type Stenotrophomonas maltophilia and its indole acetic acid-deficient mutants on wheat. Plant Biology (Stuttgart, Germany) 18, 835–841. doi:10.1111/plb.12477CrossRefGoogle Scholar
Hemida, KA and Reyad, AM (2019) Improvement salt tolerance of safflower plants by endophytic bacteria. Journal of Horticulture and Plant Research 5, 38–56. doi:10.18052/www.scipress.com/JHPR.5.38CrossRefGoogle Scholar
Herrera, SD, Grossi, C, Zawoznik, M and Groppa, MD (2016) Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiological Research 186-187, 37–43. doi:10.1016/j.micres.2016.03.002CrossRefGoogle Scholar
Hrynkiewicz, K, Patz, S and Ruppel, S (2019) Salicornia europaea L. as an underutilized saline-tolerant plant inhabited by endophytic diazotrophs. Journal of Advanced Research 19, 49–56. doi:10.1016/j.jare.2019.05.002CrossRefGoogle ScholarPubMed
Huet, S, Pouvreau, J-B, Delage, E, Delgrange, S, Marais, C, Bahut, M, Delavault, P, Simier, P and Poulin, L (2020) Populations of the parasitic plant Phelipanche ramosa influence their seed microbiota. Frontiers in Plant Science 11, 1075. doi:10.3389/fpls.2020.01075CrossRefGoogle 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, 269. doi:10.3389/fpls.2017.00269CrossRefGoogle ScholarPubMed
Joel, DM, Hershenhorn, Y, Eizenberg, H, Aly, R, Ejeta, G, Rich, PJ, Ransom, JK, Sauerborn, J and Rubiales, D (2007) Biology and management of weedy root parasites, pp. 267–349 in Janick, J. (Ed.) Horticultural reviews, vol. 33. New York, John Wiley & Sons. doi:10.1002/9780470168011.ch4CrossRefGoogle Scholar
Johnston-Monje, D, Gutiérrez, JP and Lopez-Lavalle, LAB (2021) Seed-transmitted bacteria and fungi dominate juvenile plant microbiomes. Frontiers in Microbiology 12, 737616. doi:10.3389/fmicb.2021.737616CrossRefGoogle ScholarPubMed
Jonkers, W, Gundel, PE, Verma, SK and White, JF (2022) Editorial: seed microbiome research. Frontiers in Microbiology 13, 943329. doi:10.3389/fmicb.2022.943329CrossRefGoogle ScholarPubMed
Kusstatscher, P, Adam, E, Wicaksono, WA, Bernhart, M, Olimi, E, Müller, H and Berg, G (2021) Microbiome-assisted breeding to understand cultivar-dependent assembly in Cucurbita pepo. Frontiers in Plant Science 12, 642027. doi:10.3389/fpls.2021.642027CrossRefGoogle ScholarPubMed
Li, Z, Lin, H, Gu, L, Gao, J and Tzeng, C-M (2016) Herba Cistanche (Rou Cong-Rong): one of the best pharmaceutical gifts of traditional Chinese medicine. Frontiers in Pharmacology 7. doi:10.3389/fphar.2016.00041CrossRefGoogle ScholarPubMed
Lumactud, R and Fulthorpe, RR (2018) Endophytic bacterial community structure and function of herbaceous plants from petroleum hydrocarbon contaminated and non-contaminated sites. Frontiers in Microbiology 9, 1926. doi:10.3389/fmicb.2018.01926CrossRefGoogle ScholarPubMed
Luziatelli, F, Ficca, AG, Bonini, P, Muleo, R, Gatti, L, Meneghini, M, Tronati, M, Melini, F and Ruzzi, M (2020) A genetic and metabolomic perspective on the production of indole-3-acetic acid by Pantoea agglomerans and use of their metabolites as biostimulants in plant nurseries. Frontiers in Microbiology 11, 1475. doi:10.3389/fmicb.2020.01475CrossRefGoogle ScholarPubMed
Manasa, KM, Vasanthakumari, MM, Nataraja, KN and Uma Shaanker, R (2020) Endophytic fungi of salt adapted Ipomea pes-caprae L. R. Br: their possible role in inducing salinity tolerance in paddy (Oryza sativa L.). Current Science 118, 1448–1453. doi:10.18520/cs/v118/i9/1448-1453CrossRefGoogle Scholar
Manjunatha, BS, Asha, AD, Nivetha, N, Bandeppa, , Govindasamy, V, Rathi, MS and Sangeeta, P (2017) Evaluation of endophytic bacteria for their influence on plant growth and seed germination under water stress conditions. International Journal of Current Microbiology and Applied Sciences 6, 4061–4067. doi:10.20546/ijcmas.2017.611.475CrossRefGoogle Scholar
McMurdie, PJ and Holmes, S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217. doi:10.1371/journal.pone.0061217CrossRefGoogle Scholar
Metwaly, A, Salama, GMY and Ali, GA (2018) Using hydrogen peroxide for reducing bacterial contamination in date palm tissue culture. International Journal of Advances in Agricultural Science and Technology 5, 25–33.Google Scholar
Murali, A, Bhargava, A and Wright, ES (2018) IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome 6, 140. doi:10.1186/s40168-018-0521-5CrossRefGoogle ScholarPubMed
Nickrent, DL (2020) Parasitic angiosperms: how often and how many? Taxon 69, 5–27. doi:10.1002/tax.12195CrossRefGoogle Scholar
Panosyan, H, Hakobyan, A, Birkeland, N-K and Trchounian, A (2018) Bacilli community of saline-alkaline soils from the Ararat Plain (Armenia) assessed by molecular and culture-based methods. Systematic and Applied Microbiology 41, 232–240. doi:10.1016/j.syapm.2017.12.002CrossRefGoogle ScholarPubMed
Parte, AC (2018) LPSN — list of prokaryotic names with standing in Nomenclature (bacterio.net), 20 years on. International Journal of Systematic and Evolutionary Microbiology 68, 1825–1829. doi:10.1099/ijsem.0.002786CrossRefGoogle Scholar
Patten, CL and Glick, BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Applied and Environmental Microbiology 68, 3795–3801. doi:10.1128/AEM.68.8.3795-3801.2002CrossRefGoogle ScholarPubMed
Petrosyan, K, Piwowarczyk, R, Ruraż, K, Thijs, S, Vangronsveld, J and Kaca, W (2022) Seed associated microbial communities of holoparasitic Cistanche species from Armenia and Portugal, p. 125 in Proceedings from XVI International Conference on Plant Physiology and Plant Science, January 2022, Zurich, Switzerland.Google Scholar
Piwowarczyk, R (2013) Seed productivity in relation to other shoot features for endangered parasitic plant Orobanche picridis F.W. Schultz (Orobanchaceae). Polish Journal of Ecology 61, 55–64.Google Scholar
Piwowarczyk, R, Kwolek, D, Góralski, G, Denysenko, M, Joachimiak, AJ and Aleksanyan, A (2017) First report of the holoparasitic flowering plant Cistanche armena on Caspian Manna (Alhagi maurorum) in Armenia. Plant Disease 101, 512–512. doi:10.1094/PDIS-10-16-1469-PDNCrossRefGoogle Scholar
Piwowarczyk, R, Sánchez Pedraja, Ó, Moreno Moral, G, Fayvush, G, Zakaryan, N, Kartashyan, N and Aleksanyan, A (2019) Holoparasitic Orobanchaceae (Cistanche, Diphelypaea, Orobanche, Phelipanche) in Armenia: distribution, habitats, host range and taxonomic problems. Phytotaxa 386, 001–106. doi:10.11646/phytotaxa.386.1.1CrossRefGoogle Scholar
Piwowarczyk, R, Ochmian, I, Lachowicz, S, Kapusta, I, Sotek, Z and Błaszak, M (2020a) Phytochemical parasite-host relations and interactions: a Cistanche armena case study. Science of The Total Environment 716, 137071. doi:10.1016/j.scitotenv.2020.137071CrossRefGoogle ScholarPubMed
Piwowarczyk, R, Ruraż, K, Krasylenko, Y, Kasińska, J and Sánchez-Pedraja, Ó (2020b) Seed micromorphology of representatives of holoparasitic Orobanchaceae genera from the Caucasus region and its taxonomic significance. Phytotaxa 432, 223–251. doi:10.11646/phytotaxa.432.3.1CrossRefGoogle Scholar
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596. doi:10.1093/nar/gks1219CrossRefGoogle ScholarPubMed
Raj, PS, Sasikala, C, Ramaprasad, EVV, Subhash, Y, Busse, H-J, Schumann, P and Ramana, C (2013) Chryseomicrobium amylolyticum sp. nov., isolated from a semi-arid tropical soil, and emended descriptions of the genus Chryseomicrobium and Chryseomicrobium imtechense. International Journal of Systematic and Evolutionary Microbiology 63, 2612–2617. doi:10.1099/ijs.0.044552-0CrossRefGoogle ScholarPubMed
Ruraż, K, Piwowarczyk, R, Gajdoš, P, Krasylenko, Y and Čertík, M (2020) Fatty acid composition in seeds of holoparasitic Orobanchaceae from the Caucasus region: relation to species, climatic conditions and nutritional value. Phytochemistry 179, 112510. doi:10.1016/j.phytochem.2020.112510CrossRefGoogle ScholarPubMed
Sánchez-López, AS, Pintelon, I, Stevens, V, Imperato, V, Timmermans, J-P, González-Chávez, C, Carrillo-González, R, Van Hamme, J, Vangronsveld, J and Thijs, S (2018) Seed endophyte microbiome of Crotalaria pumila unpeeled: identification of plant-beneficial Methylobacteria. International Journal of Molecular Sciences 19, 291. doi:10.3390/ijms19010291CrossRefGoogle ScholarPubMed
Schneider, AC and Moore, AJ (2017) Parallel Pleistocene amphitropical disjunctions of a parasitic plant and its host. American Journal of Botany 104, 1745–1755. doi:10.3732/ajb.1700181CrossRefGoogle ScholarPubMed
Schwyn, B and Neilands, JB (1987) Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry 160, 47–56. doi:10.1016/0003-2697(87)90612-9CrossRefGoogle ScholarPubMed
Shahzad, R, Khan, AL, Bilal, S, Asaf, S and Lee, I-J (2017) Plant growth-promoting endophytic bacteria versus pathogenic infections: an example of Bacillus amyloliquefaciens RWL-1 and Fusarium oxysporum f. sp. lycopersici in tomato. PeerJ 5, e3107. doi:10.7717/peerj.3107CrossRefGoogle ScholarPubMed
Shameer, S and Prasad, TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regulation 84, 603–615. doi:10.1007/s10725-017-0365-1CrossRefGoogle Scholar
Shrivastava, P and Kumar, R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences 22, 123–131. doi:10.1016/j.sjbs.2014.12.001CrossRefGoogle ScholarPubMed
Singh, RP and Jha, PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Frontiers in Microbiology 8, 1945. doi:10.3389/fmicb.2017.01945CrossRefGoogle ScholarPubMed
Soussi, A, Ferjani, R, Marasco, R, Guesmi, A, Cherif, H, Rolli, E, Mapelli, F, Ouzari, HI, Daffonchio, D and Cherif, A (2016) Plant-associated microbiomes in arid lands: diversity, ecology and biotechnological potential. Plant and Soil 405, 357–370. doi:10.1007/s11104-015-2650-yCrossRefGoogle Scholar
Szymańska, S, Borruso, L, Brusetti, L, Hulisz, P, Furtado, B and Hrynkiewicz, K (2018) Bacterial microbiome of root-associated endophytes of Salicornia europaea in correspondence to different levels of salinity. Environmental Science and Pollution Research 25, 25420–25431. doi:10.1007/s11356-018-2530-0CrossRefGoogle ScholarPubMed
Truyens, S, Weyens, N, Cuypers, A and Vangronsveld, J (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biology 15, 971–981. doi:10.1111/j.1438-8677.2012.00711.xCrossRefGoogle ScholarPubMed
Truyens, S, Jambon, I, Croes, S, Janssen, J, Weyens, N, Mench, M, Carleer, R, Cuypers, A and Vangronsveld, J (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. International Journal of Phytoremediation 16, 643–659. doi:10.1080/15226514.2013.837027CrossRefGoogle ScholarPubMed
Truyens, S, Beckers, B, Thijs, S, Weyens, N, Cuypers, A and Vangronsveld, J (2016) The effects of the growth substrate on cultivable and total endophytic assemblages of Arabidopsis thaliana. Plant and Soil 405, 325–336. doi:10.1007/s11104-015-2761-5CrossRefGoogle Scholar
Ulrich, K, Ulrich, A and Ewald, D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiology Ecology 63, 169–180. doi:10.1111/j.1574-6941.2007.00419.xCrossRefGoogle ScholarPubMed
Walters, W, Hyde, ER, Berg-Lyons, D, Ackermann, G, Humphrey, G, Parada, A, Gilbert, JA, Jansson, JK, Caporaso, JG, Fuhrman, JA, Apprill, A and Knight, R (2016) Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1, e00009–15. doi:10.1128/mSystems.00009-15CrossRefGoogle ScholarPubMed
Watts, JE, de Villiers, OT and Watts, L (1993) Sterilization of wheat seeds for tissue culture purposes. South African Journal of Botany 59, 641–642. doi:10.1016/s0254-6299(16)30683-4CrossRefGoogle Scholar
Yilmaz, P, Parfrey, LW, Yarza, P, Gerken, J, Pruesse, E, Quast, C, Schweer, T, Peplies, J, Ludwig, W and Glöckner, FO (2014) The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Research 42, D643–D648. doi:10.1093/nar/gkt1209CrossRefGoogle ScholarPubMed
Yoneyama, K, Xiaonan, X, Sekimoto, H, Takeuchi, Y, Ogasawara, S, Akiyama, K, Hayashi, H and Yoneyama, K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytologist 179, 484–494. doi:10.1111/j.1469-8137.2008.02462.xCrossRefGoogle ScholarPubMed
Supplementary material: File

Petrosyan et al. supplementary material

Figure S1

Download Petrosyan et al. supplementary material(File)
File 95.1 KB
Supplementary material: File

Petrosyan et al. supplementary material

Figure S2

Download Petrosyan et al. supplementary material(File)
File 218.3 KB