The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacteriumspp. and Staphylococcus spp. with potential plant-growth promoting activities

Pasquale Alibrandi1, Massimiliano Cardinale2, MD Mahafizur Rahman2, Francesco Strati3, Paolo Ciná1, Marta L. de Viana4, Eugenia M. Giamminola4, Giuseppe Gallo1, Sylvia Schnell2, Carlotta De Filippo5,6, Mirella Ciaccio7, Anna Maria Puglia1
1Laboratory of Molecular Microbiology and Biotechnology, STEBICEF Department, University of Palermo, Palermo, Italy
2Institute of Applied Microbiology, Justus Liebig University Giessen, Giessen, Germany
3Computational Biology Research Unit, Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’ Adige, Italy
4Banco de Germoplasma de Especies Nativas, Instituto de Ecología y Ambiente Humano, Universidad Nacional de Salta, UNSA, Salta, Argentina
5Institute of Agricultural Biology and Biotechnology, National Research Council (IBBA-CNR), Pisa, Italy
6Institute of Biometeorology – National Research Council (IBIMET-CNR), Florence, Italy
7Istituto di Biomedicina e Immunologia Molecolare “A. Monroy” Consiglio Nazionale delle Ricerche CNR, Palermo, Italy

Tóm tắt

Plant seeds are emerging micro–habitats, whose importance as reservoir and vector of beneficial microbes just begins to be recognized. Here we aimed to characterize the bacterial microbiota of the Anadenanthera colubrina seed endosphere, with special focus to beneficial traits and to the colonization pattern. Cultivation–dependent (isolation from surface–sterilized seeds) and cultivation–independent (pyrosequencing of 16S rRNA gene from metagenomic seed DNA) analyses, functional tests and microscopical investigations (fluorescence in situ hybridization coupled with confocal laser scanning microscopy (FISH-CLSM) were performed. We isolated several Methylobacterium and Staphylococcus spp., exhibiting both plant growth promotion and antimicrobial activities. The two taxonomic groups showed complementary traits, which supports a functional selection. Both genera were detected also by pyrosequencing, together with further taxa. The genera Friedmaniella, Bifidobacterium, Delftia, Anaerococcus and Actinomyces appeared here for the first time as seed endophytes. We detected bacterial cells and micro–colonies in seed cryosections by FISH-CLSM. Alphaproteobacteria, Firmicutes and other bacteria colonized intercellular spaces of the parenchyma and associated to transport vessels. This work sheds light onto the diversity, functions and colonization pattern of the Anadenanthera colubrina seed endophytes, and strongly suggest a role as beneficial partners for seed-associated microbiota.

Từ khóa


Tài liệu tham khảo

Acevedo E, Galindo-Castaneda T, Prada F, Navia M, Romero HM (2014) Phosphate-solubilizing microorganisms associated with the rhizosphere of oil palm (Elaeis guineensis Jacq.) in Colombia. Appl Soil Ecol 80:26–33

Albanese D, Fontana P, De Filippo C, Cavalieri D, Donati C (2015) MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Sci Rep 5:9743

Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

Ali B, Sabri AN, Hasnain S (2010) Rhizobacterial potential to alter auxin content and growth of Vigna radiata (L.). W J Microbiol Biotechnol 26:1379–1384

Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA–targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

Azevedo JL, Maccheroni W Jr, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:15–16

Baig KS, Arshad M, Zahir ZA, Cheema MA (2010) Comparative efficacy of qualitative and quantitative methods for rock phosphate solubilization with phosphate solubilizing rhizobacteria. Soil Environ 29:82–86

Baldi F, Daniele S, Gallo M, Paganelli S, Battistel D, Piccolo O, Faleri C, Puglia AM, Gallo G (2016) Polysaccharide–based silver nanoparticles synthesized by Klebsiella oxytoca DSM 29614 cause DNA fragmentation in E. coli cells. Biometals 29:321–331

Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co–operation in the rhizosphere. J Exp Bot 56:1761–1778

Barrandeguy ME, García MV, Prinz K, Pomar RR, Finkeldey R (2014) Genetic structure of disjunct Argentinean populations of the subtropical tree Anadenanthera colubrina Var. cebil (Fabaceae). Plant Syst Evol 300:1693–1705

Barret M, Briand M, Bonneau S, Préveaux A, Valière S, Bouchez O, Hunault G, Simoneau P, Marie-Agnès J (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81:1257–1266

Bashan Y, Kamnev AA, de Bashan LE (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate–solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479

Beasley FC, Heinrichs DE (2010) Siderophore–mediated iron acquisition in the staphylococci. J Inorg Biochem 104:282–288

Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

Brenan JP (1955) Notes on Mimosoideae: I. Kew Bull 10:161–192

Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. PNAS 108:14288–14293

Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

Cardinale M (2014) Scanning a microhabitat: plant–microbe interactions revealed by confocal laser microscopy. Front Microbiol 5:94

Cardinale M, Berg G (2015) Visualization of plant–microbe interactions. In: Lugtenberg B (ed) Principles of plant–microbe interactions. Springer International Publishing, Switzerland, pp 299–306

Cardinale M, de Castro JV, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71

Cardinale M, Ratering S, Suarez C, Montoya AMZ, Geissler-Plaum R, Schnell S (2015) Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiol Res 181:22–32

Chaudhry V, Baindara P, Pal VK, Chawla N, Patil PB, Korpole S (2015) Methylobacterium indicum sp. nov., a facultative methylotrophic bacterium isolated from rice seed. Syst Appl Microbiol 39:25–32

Chavez MD, Berentsen PBM, Oenema O, Lansink AGJMO (2014) Potential for increasing soil nutrient availability via soil organic matter improvement using pseudo panel data. Agric Sci 5:743–753

Chee-Sanford JC, Williams MM, Davis AS, Sims GK (2006) Do microorganisms influence seed-bank dynamics? Weed Sci 54:575–587

Cialdella AM (2000) Flora Fanerogámica Argentina, Fascículo 67: Fabaceae Subfamilia Mimosoideae, pp 1–10. Profl ora–CONICET, Córdoba, Argentina

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 71:1685–1693

Compant S, Clément C, Sessitsch A (2010) Plant growth–promoting bacteria in the rhizo–and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197

Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain–specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

de Viana ML, Giamminola E, Russo R, Ciaccio M (2014) Morphology and genetics of Anadenanthera colubrina Var. cebil (Fabaceae) tree from Salta (northwestern Argentina). Rev Biol Trop 62:757–767

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera–checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

Donachie SP, Foster JS, Brown MV (2007) Culture clash: challenging the dogma of microbial diversity. ISME J 1:97–102

Doornbos RF, van Loon LC, Bakker PA (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243

Fankem H, Nwaga D, Deubel A, Dieng L, Merbach W, Etoa FX (2006) Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr J Biotechnol 5:2450–2460

Fedorov DN, Ekimova GA, Doronina NV, Trotsenko YA (2013) 1–aminocyclopropane–1–carboxylate (ACC) deaminases from Methylobacterium radiotolerans and Methylobacterium nodulans with higher specificity for ACC. FEMS Microbiol Lett 343:70–76

Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14

Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470

Gadagi RS, Sa T (2002) New isolation method for microorganisms solulbilizing iron and aluminum phosphates using dyes. Soil Sci Plant Nutr 48:615–618

Gagne-Bourgue F, Aliferis KA, Seguin P, Rani M, Samson R, Jabaji S (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114:836–853

Gallo G, Baldi F, Renzone G, Gallo M, Cordaro A, Scaloni A, Puglia AM (2012) Adaptative biochemical pathways and regulatory networks in Klebsiella oxytoca BAS-10 producing a biotechnologically relevant exopolysaccharide during Fe (III)-citrate fermentation. Microb Cell Fact 11:152

Gaskins MH, Albrecht SL, Hubbell DH (1985) Rhizosphere bacteria and their use to increase plant productivity: a review. Agric Ecosyst Environ 12:99–116

Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

Gourion B, Rossignol M, Vorholt JA (2006) A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. PNAS 103:13186–13191

Granér G, Persson P, Meijer J, Alström S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224:269–227

Hallmann J (2001) Plant interactions with endophytic bacteria. CABI Publishing, New York, pp 87–119

Hamdali H, Smirnov A, Esnault C, Ouhdouch Y, Virolle MJ (2010) Physiological studies and comparative analysis of rock phosphate solubilization abilities of Actinomycetales originating from Moroccan phosphate mines and of Streptomyces lividans. Appl Soil Ecol 44:24–31

Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

Hardoim PR, Hardoim CC, Van Overbeek LS, Van Elsas JD (2012) Dynamics of seed–borne rice endophytes on early plant growth stages. PLoS One 7:e30438

Holland MA, Polacco JC (1994) PPFMs and other covert contaminants: is there more to plant physiology than just plant? Annu Rev Plant Biol 45:197–209

Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3:1–0003

Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture–independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774

Hung PQ, Annapurna K (2004) Isolation and characterization of endophytic bacteria in soybean (Glycine sp.). Omonrice 12:92–101

Jayashree S, Vadivukkarasi P, Anand K, Kato Y, Seshadri S (2011) Evaluation of pink–pigmented facultative methylotrophic bacteria for phosphate solubilization. Arch Microbiol 193:543–552

Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396

Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P (2004) Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root–nodule–forming and nitrogen–fixing bacteria. Int J Syst Evol Microbiol 54:2269–2273

Justiniano MJ, Fredericksen TS (1998) Ecología y Silvicultura de Especies Menos Conocidas – Curupaú Anadenanthera colubrina (Vell. Conc.) Benth, Mimosoideae. Santa Cruz: BOLFOR

Kieser Y, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich

Kirchhof G, Reis VM, Baldani JI, Eckert B, Döbereiner J, Hartmann A (1997) Occurrence, physiological and molecular analysis of endophytic diazotrophic bacteria in gramineous energy plants. In: Ladha JK, de Bruijn FJ, Malik KA (eds) Opportunities for biological nitrogen fixation in Rice and other non–legumes. Springer, The Netherlands, pp 45–55

Kumar K, Amaresan N, Bhagat S, Madhuri K, Srivastava RC (2011) Isolation and characterization of rhizobacteria associated with coastal agricultural ecosystem of rhizosphere soils of cultivated vegetable crops. W J Microbiol Biotechnol 27:1625–1632

Kutschera U (2007) Plant–associated methylobacteria as co–evolved phytosymbionts: a hypothesis. Plant Signal Behav 2:74–78

Lacava PT, Li WB, Araújo WL, Azevedo JL, Hartung JS (2006) Rapid, specific and quantitative assays for the detection of the endophytic bacterium Methylobacterium mesophilicum in plants. J Microbiol Methods 65:535–541

Larenas Parada G, De Viana ML, Chafatinos T, Escobar NE (2004) Relación suelo–especie invasora (Tithonia tubaeformis) en el sistema ribereño del río Arenales, Salta, Argentina. Ecología Austral 14:19–29

Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

Lindow SE, Leveau JH (2002) Phyllosphere microbiology. Curr Opin Biotechnol 13:238–243

Lindsay JA, Riley TV (1994) Staphylococcal iron requirements, siderophore production, and iron–regulated protein expression. Infect Immun 62:2309–2314

Lisiecki P, Tkacz B, Sobiś M, Mikucki J (1993) The occurrence of siderophores in staphylococci. Acta Microbiol Pol 43:21–31

Liu Y, Zuo S, Xu L, Zou Y, Song W (2012) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012

Liu Y, Zuo S, Zou Y, Wang J, Song W (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L, Nongda108) at different growth stages. Ann Microbiol 63:71–79

Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock–colonizing cactus of the southern Sonoran Desert. Arch Microbiol 193:527–541

López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris Seed–borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327

Madhaiyan M, Poonguzhali S, Senthilkumar M, Seshadri S, Chung H, Jinchul YANG, Sundaram S, Tongmin SA (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium spp. Bot Bull Acad Sin 45:315–324

Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 21:86–100

Maude RB (1996) Seedborne diseases and their control: principles and practice. CAB international, UK

McDonald IR, Murrell JC (1997) The methanol dehydrogenase structural gene mxaF and its use as a functional gene probe for methanotrophs and methylotrophs. Appl Environ Microbiol 63:3218–3224

McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Ac Res 32(suppl 2):W20–W25

Mcinroy JA, Kloepper JW (1995) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342

McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217

Meena KK, Kumar M, Kalyuzhnaya MG, Yandigeri MS, Singh DP, Saxena AK, Arora DK (2012) Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (Triticum aestivum) by producing phytohormone. Antonie Van Leeuwenhoek 101:777–786

Meier H, Amann R, Ludwig W, Schleifer KH (1999) Specific oligonucleotide probes for in situ detection of a major group of gram–positive bacteria with low DNA G+ C content. Syst Appl Microbiol 22:186–196

Milagres AM, Machuca A, Napoleao D (1999) Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J Microbiol Methods 37:1–6

Milanesi C, Cresti M, Costantini L, Gallo M, Gallo G, Crognale S, Faleri C, Gradi A, Baldi F (2015) Spoilage of oat bran by sporogenic microorganisms revived from soil buried 4000 years ago in Iranian archaeological site. Int Biodeter Biodegr 104:83–91

Müller T, Ruppel S (2014) Progress in cultivation–independent phyllosphere microbiology. FEMS Microbiol Ecol 87:2–17

Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction–amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

Neef A (1997) Anwendung der in situ Einzelzell–Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. Doctoral Thesis (Technische Universität München)

Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726

Nichols D (2007) Cultivation gives context to the microbial ecologist. FEMS Microbiol Ecol 60:351–357

Panchal H, Ingle S (2011) Isolation and characterization of endophytes from the root of medicinal plant Chlorophytum borivilianum (Safed musli). J Adv Dev Res 2:205–209

Partida-Martinez LPP, Heil M (2011) The microbe–free plant: fact or artifact? Front Plant Sci 2:100

Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth–promoting rhizobacteria. Physiol Plant 118:10–15

Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth–promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415

Pirttilä AM, Laukkanen H, Pospiech H, Myllylä R, Hohtola A (2000) Detection of intracellular bacteria in the buds of scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077

Price MN, Dehal PS, Arkin AP (2010) FastTree 2––approximately maximum–likelihood trees for large alignments. PloS One 5:e9490

Raimam MP, Albino U, Cruz MF, Lovato GM, Spago F, Ferracin TP, Lima DS, Goulart T, Bernardi CM, Miyauchi M, Nogueira MA (2007) Interaction among free-living N-fixing bacteria isolated from Drosera villosa Var. villosa and AM fungi (Glomus clarum) in rice (Oryza sativa). Appl Soil Ecol 35:25–34

Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas spp. that utilize inositol phosphates. Can J Microbiol 43:509–516

Rosenblueth M, López-López A, Martínez J, Rogel MA, Toledo I, Martínez-Romero I (2010) Seed bacterial endophytes: common genera, seed–to–seed variability and their possible role in plants. In: XXVIII International Horticultural Congress on Science and Horticulture for People (IHC2010): International Symposium on 938, p 39–48

Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbial Lett 278:1–9

Scaffaro R, Botta L, Gallo G, Puglia AM (2015) Influence of drawing on the antimicrobial and physical properties of chlorhexidine-compounded poly (caprolactone) monofilaments. Macromol Mater Eng 300:1268–1277

Schaad NW, Jones JB, Chun W (1980) Laboratory guide for identification of plant pathogenic bacteria. Amer Phytopathol Soc, St. Paul

Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1601:47–56

Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346

Surette MA, Sturz AV, Lada RR, Nowak J (2003) Bacterial endophytes in processing carrots (Daucus carota L. Var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant Soil 253:381–390

Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

Tiwari R, Awasthi A, Mall M, Shukla AK, Srinivas KS, Syamasundar KV, Kalra A (2013) Bacterial endophyte–mediated enhancement of in planta content of key terpenoid indole alkaloids and growth parameters of Catharanthus roseus. Ind Crop Prod 43:306–310

Torres CM, Repke DB (2006) Anadenanthera: visionary plant of ancient South America. Psychology Press, Hove

Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50

Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126

van Overbeek LS, Saikkonen K (2016) Impact of bacterial–fungal interactions on the colonization of the endosphere. Trends Plant Sci 21:230–242

Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206

Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48:559–565

Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840

Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143

Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755

Wohl DL, Arora S, Gladstone JR (2004) Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85:1534–1540

Xu M, Sheng J, Chen L, Men Y, Gan L, Guo S, Shen L (2014) Bacterial community compositions of tomato (Lycopersicum esculentum mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT–12–1) on tomato seedlings. W J Microbiol Biotechnol 30:835–845

Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735