Possible role of arbuscular mycorrhizal fungi and associated bacteria in the recruitment of endophytic bacterial communities by plant roots
Tóm tắt
Arbuscular mycorrhizal fungi (AMF) represent an important group of root symbionts, given the key role they play in the enhancement of plant nutrition, health, and product quality. The services provided by AMF often are facilitated by large and diverse beneficial bacterial communities, closely associated with spores, sporocarps, and extraradical mycelium, showing different functional activities, such as N2 fixation, nutrient mobilization, and plant hormone, antibiotic, and siderophore production and also mycorrhizal establishment promotion, leading to the enhancement of host plant performance. The potential functional complementarity of AMF and associated microbiota poses a key question as to whether members of AMF-associated bacterial communities can colonize the root system after establishment of mycorrhizas, thereby becoming endophytic. Root endophytic bacterial communities are currently studied for the benefits provided to host plants in the form of growth promotion, stress reduction, inhibition of plant pathogens, and plant hormone release. Their quantitative and qualitative composition is influenced by many factors, such as geographical location, soil type, host genotype, and cultivation practices. Recent data suggest that an additional factor affecting bacterial endophyte recruitment could be AMF and their associated bacteria, even though the mechanisms allowing members of AMF-associated bacterial communities to actually establish in the root system, becoming endophytic, remain to be determined. Given the diverse plant growth–promoting properties shown by AMF-associated bacteria, further studies are needed to understand whether AMF may represent suitable tools to introduce beneficial root endophytes in sustainable and organic agriculture where the functioning of such multipartite association may be crucial for crop production.
Tài liệu tham khảo
Agnolucci M, Battini F, Cristani C, Giovannetti M (2015) Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fertil Soils 51:379–389. https://doi.org/10.1007/s00374-014-0989-5
Agnolucci M, Avio L, Pepe A, Turrini A, Cristani C, Bonini P, Cirino B, Colosimo F, Ruzzi M Giovannetti M (2019a) Bacteria associated with a commercial mycorrhizal inoculum: community composition and multifunctional activity as assessed by Illumina sequencing and culture-dependent tools Front Plant Sci 9 1956 https://doi.org/10.3389/fpls.2018.01956
Agnolucci M, Palla M, Cristani C, Cavallo N, Giovannetti M, De AM, Gobbetti M, Minervini F (2019b) Beneficial plant microorganisms affect the endophytic bacterial communities of durum wheat roots as detected by different molecular approaches. Front Microbiol 10:2500. https://doi.org/10.3389/fmicb.2019.02500
Agnolucci M, Avio L, Palla M, Sbrana C, Turrini A, Giovannetti M (2020) Health-promoting properties of plant products: the role of mycorrhizal fungi and associated bacteria. Agronomy 10:1864. https://doi.org/10.3390/agronomy10121864
Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163. https://doi.org/10.1016/j.gdata.2015.09.004
Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215. https://doi.org/10.1128/aem.69.10.6208-6215.2003
Avio L, Turrini A, Giovannetti M, Sbrana C (2018) Designing the ideotype mycorrhizal symbionts for the production of healthy food. Front Plant Sci 9:1089. https://doi.org/10.3389/fpls.2018.01089
Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. J Soil Sci Plant Nutr 15:372–396. https://doi.org/10.4067/S0718-95162015005000035
Barea JM, Azcón R, Azcón-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351. https://doi.org/10.1023/A:1020588701325
Barraza A, Castellanos C-C, T, Loera-Muro A, (2020) Bacterial community characterization of the rhizobiome of plants belonging to Solanaceae family cultivated in desert soils. Ann Microbiol 70:1–14. https://doi.org/10.1186/s13213-020-01572-x
Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79. https://doi.org/10.1016/j.micres.2015.11.012
Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci Rep 7:4686. https://doi.org/10.1038/s41598-017-04959-0
Bharadwaj DP, Lundquist PO, Alström S (2008a) Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil Biol Biochem 40:2494–2501. https://doi.org/10.1016/j.soilbio.2008.06.012
Bharadwaj DP, Lundquist PO, Persson P, Alström S (2008b) Evidence for specificity of cultivable bacteria associated with arbuscular mycorrhizal fungal spores. FEMS Microbiol Ecol 65:310–322. https://doi.org/10.1111/j.1574-6941.2008.00515.x
Bidondo LF, Colombo R, Bompadre J, Benavides M, Scorza V, Silvani V, Pérgola M, Godeas A (2016) Cultivable bacteria associated with infective propagules of arbuscular mycorrhizal fungi. Implications for mycorrhizal activity. Appl Soil Ecol 105:86–90. https://doi.org/10.1016/j.apsoil.2016.04.013
Bitterlich M, Franken P, Graefe J (2018) Arbuscular mycorrhiza improves substrate hydraulic conductivity in the plant available moisture range under root growth exclusion. Front Plant Sci 9:301. https://doi.org/10.3389/fpls.2018.00301
Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8(2):e56329. https://doi.org/10.1371/journal.pone.0056329
Bonito G, Benucci GMN, Hameed K, Weighill D, Jones P, Chen KH, Jacobson D, Schadt C, Vilgalys R (2019) Fungal-bacterial networks in the Populus rhizobiome are impacted by soil properties and host genotype. Front Microbiol 10:481. https://doi.org/10.3389/fmicb.2019.00481
Budi SW, Bakhtiar Y, May NL (2012) Bacteria associated with arbuscula mycorrhizal spores Gigaspora margarita and their potential for stimulating root mycorrhizal colonization and neem (Melia azedarach Linn) seedling growth. Microbiol Indones 6:6–6. https://doi.org/10.5454/mi.6.4.6
Bulgarelli D, Rott M, Schlaeppi K, Loren V, van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. https://doi.org/10.1038/nature11336
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403. https://doi.org/10.1016/j.chom.2015.01.011
Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7:41564. https://doi.org/10.1038/srep41564
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
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. https://doi.org/10.1016/j.soilbio.2009.11.024
Conn VM, Franco CMM (2004) Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl Environ Microbiol 70:1787–1794. https://doi.org/10.1128/AEM.70.3.1787-1794.2004
Cruz AF, Ochiai HS, S, Yasuda A, Ishii T, (2008) Isolation and analysis of bacteria associated with spores of Gigaspora margarita. J Appl Microbiol 104:1711–1717. https://doi.org/10.1111/j.1365-2672.2007.03695.x
Cruz AF, Ishii T (2011) Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens. Biol Open, 1:52–57. https://doi.org/10.1242/bio.2011014
de Novais CB, Sbrana C, da Conceição JE, Rouws LFM, Giovannetti M, Avio L, Siqueira JO, Saggin OJ Jr, Ribeiro da Silva EM, de Faria SM (2020) Mycorrhizal networks facilitate the colonization of legume roots by a symbiotic nitrogen-fixing bacterium. Mycorrhiza 30:389–396. https://doi.org/10.1007/s00572-020-00948-w
Duca D, Lorv J, Patten CL, Rose D, Glick BR (2014) Indole-3-acetic acid in plant–microbe interactions. Anton Van Leeuw 106:85–125. https://doi.org/10.1007/s10482-013-0095-y
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Ek-Ramos MJ, Gomez-Flores R, Orozco-Flores AA, Rodríguez-Padilla C, González-Ochoa G, Tamez-Guerra P (2019) Bioactive products from plant-endophytic Gram-positive bacteria. Front Microbiol 10:463. https://doi.org/10.3389/fmicb.2019.00463
Emmett BD, Lévesque-Tremblay V, Harrison MJ (2021) Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi ISME J 1–13 https://doi.org/10.1038/s41396-021-00920-2
Ferrando L, Fernández Scavino A (2015) Strong shift in the diazotrophic endophytic bacterial community inhabiting rice (Oryza sativa) plants after flooding. FEMS Microbiol Ecol 91:9, fiv104. https://doi.org/10.1093/femsec/fiv104
Filippi C, Bagnoli G, Citernesi AS, Giovannetti M (1998) Ultrastructural spatial distribution of bacteria associated with sporocarps of Glomus mosseae. Symbiosis 24:1–12
Finan TM (2002) Evolving insights: symbiosis islands and horizontal gene transfer. J Bacteriol 184:2855–2856. https://doi.org/10.1128/JB.184.11.2855-2856.2002
Fonseca-García C, Coleman-Derr D, Garrido E, Visel A, Tringe SG, Partida-Martínez LP (2016) The cacti microbiome: interplay between habitat-filtering and host-specificity. Front Microbiol 7:150. https://doi.org/10.3389/fmicb.2016.00150
Food and Agriculture Organization (2011) A policymaker’s guide to the sustainable intensification of smallholder crop production; FAO: Rome, Italy, 2011; Available online: http://www.fao.org/3/a-i2215e.pdf.
Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotech 76:1145–1152. https://doi.org/10.1007/s00253-007-1077-7
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572
Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530. https://doi.org/10.1007/s00572-010-0333-3
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. https://doi.org/10.1016/j.micres.2013.09.009
Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, Giovannetti M (2020) Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: research strategies for the selection of the best performing inocula. Agronomy 10:106. https://doi.org/10.3390/agronomy10010108
Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944. https://aem.asm.org/content/77/17/5934.short
Hameed A, Yeh MW, Hsieh YT, Chung WC, Lo CT, Sen YL (2015) Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil 394:177–197. https://doi.org/10.1007/s11104-015-2506-5
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. https://doi.org/10.1016/j.tim.2008.07.008
Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD (2011) Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154–164. https://doi.org/10.1111/j.1574-6941.2011.01092.x
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/mmbr.00050-14
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. https://doi.org/10.1007/s13213-010-0117-1
Iffis B, St-Arnaud M, Hijri M (2014) Bacteria associated with arbuscular mycorrhizal fungi within roots of plants growing in a soil highly contaminated with aliphatic and aromatic petroleum hydrocarbons. FEMS Microbiol Lett 358:44–54. https://doi.org/10.1111/1574-6968.12533
Iffis B, St-Arnaud M, Hijri M (2016) Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes. Environ Microbiol 18:2689–2704. https://doi.org/10.1111/1462-2920.13438
Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24:154–162. https://doi.org/10.1264/jsme2.ME09113
Kameoka H, Maeda T, Okuma N, Kawaguchi M (2019) Structure-specific regulation of nutrient transport and metabolism in arbuscular mycorrhizal fungi. Plant Cell Physiol 60:2272–2281. https://doi.org/10.1093/pcp/pcz122
Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593. https://doi.org/10.3389/fmicb.2017.02593
Karray F, Gargouri M, Chebaane A, Mhiri N, Mliki A, Sayadi S (2020) Climatic aridity gradient modulates the diversity of the rhizosphere and endosphere bacterial microbiomes of Opuntia ficus-indica. Front Microbiol 11:1622. https://doi.org/10.3389/fmicb.2020.01622
Krishnamoorthy R, Kim K, Subramanian P, Senthilkumar M, Anandham R, Sa T (2016) Arbuscular mycorrhizal fungi and associated bacteria isolated from salt-affected soil enhances the tolerance of maize to salinity in coastal reclamation soil. Agric Ecosyst Environ 231:233–239. https://doi.org/10.1016/j.agee.2016.05.037
Ku YS, Rehman HM, Lam HM (2019) Possible roles of rhizospheric and endophytic microbes to provide a safe and affordable means of crop biofortification. Agronomy 9:764. https://doi.org/10.3390/agronomy9110764
Lasudee K, Tokuyama S, Lumyong S, Pathom-Aree W (2018) Actinobacteria associated with arbuscular mycorrhizal Funneliformis mosseae spores, taxonomic characterization and their beneficial traits to plants: evidence obtained from mung bean (Vigna radiata) and Thai jasmine rice (Oryza sativa). Front Microbiol 9:1247. https://doi.org/10.3389/fmicb.2018.01247
Lecomte J, St-Arnaud M, Hijri M (2011) Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi. FEMS Microbiol Lett 317:43–51. https://doi.org/10.1111/j.1574-6968.2011.02209.x
Lee SA, Kim Y, Kim JM, Chu B, Joa JH, Sang MK, Song J, Weon HY (2019) A preliminary examination of bacterial, archaeal, and fungal communities inhabiting different rhizocompartments of tomato plants under real-world environments. Sci Rep 9:1–15. https://doi.org/10.1038/s41598-019-45660-8
Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017a) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552
Liu H, Carvalhais LC, Schenk PM, Dennis PG (2017b) Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci Rep 7:41776. https://doi.org/10.1038/srep41766
Long L, Zhu H, Yao Q, Ai Y (2008) Analysis of bacterial communities associated with spores of Gigaspora margarita and Gigaspora rosea. Plant Soil 310:1–9. https://doi.org/10.1007/s11104-008-9611-7
Long L, Lin Q, Yao Q, Zhu H (2017) Population and function analysis of cultivable bacteria associated with spores of arbuscular mycorrhizal fungus Gigaspora margarita. 3 Biotech, 7:8. https://doi.org/10.1007/s13205-017-0612-1
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del RTG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237
Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166. https://doi.org/10.1007/s00248-010-9658-x
Marasco R, Rolli E, Fusi M, Michoud G, Daffonchio D (2018) Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome 6:3. https://doi.org/10.1186/s40168-017-0391-2
Marques JM, da Silva TF, Vollú RE, de Lacerda JRM, Blank AF, Smalla K, Seldin L (2015) Bacterial endophytes of sweet potato tuberous roots affected by the plant genotype and growth stage. Appl Soil Ecol 96:273–281. https://doi.org/10.1016/j.apsoil.2015.08.020
Mayo K, Davis RE, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78:426–431. https://www.jstor.org/stable/3793046
Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S (2014) Rhizospheric organic compounds in the soil microorganism-plant system: their role in iron availability. Eur J Soil Sci 65:629–642. https://doi.org/10.1111/ejss.12158
Minervini F, Celano G, Lattanzi A, Tedone L, de Mastro G, Gobbetti M, de Angelis M (2015) Lactic acid bacteria in durum wheat flour are endophytic components of the plant during its entire life cycle. Appl Environ Microbiol 81:6736–6748. https://doi.org/10.1128/AEM.01852-15
Mitter EK, de Freitas JR, Germida JJ (2017) Bacterial root microbiome of plants growing in oil sands reclamation covers. Front Microbiol 8:849. https://doi.org/10.3389/fmicb.2017.00849
Mitter EK, Kataoka R, de Freitas JR, Germida JJ (2019) Potential use of endophytic root bacteria and host plants to degrade hydrocarbons. Int J Phytoremediation21:928–938. https://doi.org/10.1080/15226514.2019.1583637
Mocali S, Bertelli E, Di Cello F, Mengoni A, Sfalanga A, Viliani F, Caciotti A, Tegli S, Surico G, Fani R (2003) Fluctuation of bacteria isolated from elm tissues during different seasons and from different plant organs. Res Microbiol 154:105–114. https://doi.org/10.1016/S0923-2508(03)00031-7
Moreira FS, da Costa PB, de Souza R, Beneduzi A, Lisboa BB, Vargas LK, Passaglia LMP (2016) Functional abilities of cultivable plant growth promoting bacteria associated with wheat (Triticum aestivum L.) crops. Genet Mol Biol 39:111–121. https://doi.org/10.1590/1678-4685-GMB-2015-0140
Naylor D, Degraaf S, Purdom E, Coleman-Derr D (2017) Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J11:2691–2704. https://doi.org/10.1038/ismej.2017.118
Novello G, Gamalero E, Bona E, Boatti L, Mignone F, Massa N, Cesaro P, Lingua G, Berta G (2017). The rhizosphere bacterial microbiota of Vitis vinifera cv. Pinot Noir in an integrated pest management vineyard. Front. Microbiol. 8, 1528. https://doi.org/10.3389/fmicb.2017.01528
Pecundo MH, Chang ACG, Chen T, dela Cruz TEE, Ren H, Li N, (2021) Full-length 16S rRNA and ITS gene sequencing revealed rich microbial flora in roots of Cycas spp. in China. Evol Bioinform 17:1–16. https://doi.org/10.1177/1176934321989713
Pepe A, Sbrana C, Ferrol N, Giovannetti M (2017) An in vivo whole-plant experimental system for the analysis of gene expression in extraradical mycorrhizal mycelium. Mycorrhiza 27:659–668. https://doi.org/10.1007/s00572-017-0779-7
Pei C, Mi C, Sun L, Liu W, Li O, Hu X (2017) Diversity of endophytic bacteria of Dendrobium officinale based on culture-dependent and culture-independent methods. Biotechnol Biotechnol Equip 31:112–119. https://doi.org/10.1080/13102818.2016.1254067
Philippot L, Raaijmakers JM, Lemanceau P, Van Der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol11:789–799. https://doi.org/10.1038/nrmicro3109
Pinski A, Betekhtin A, Hupert-Kocurek K, Mur LAJ, Hasterok R (2019) Defining the genetic basis of plant–endophytic bacteria interactions. Int J Mol Sci 20:1947. https://doi.org/10.3390/ijms20081947
Rambelli A (1973) The Rhizosphere of Mycorrhizae. In: Marks GC, Kozlowski TT (eds) Ectomycorrhizae: their ecology and physiology. Academic Press, pp 299–343. https://doi.org/10.1016/b978-0-12-472850-9.50014-110.1007/s00572-021-01040-7343. https://doi.org/10.1016/b978-0-12-472850-9.50014-1
Rehman A, Farooq M, Naveed M, Nawaz A, Shahzad B (2018) Seed priming of Zn with endophytic bacteria improves the productivity and grain biofortification of bread wheat. Eur J Agron 94:98–107. https://doi.org/10.1016/j.eja.2018.01.017
Roesti D, Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M (2005) Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol 71:6673–6679. https://doi.org/10.1128/AEM.71.11.6673-6679.2005
Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act asbiostimulants in horticultural crops. Sci Hortic 196:91–108. https://doi.org/10.1016/j.scienta.2015.09.002
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
Scheublin TR, Sanders IR, Keel C, Van Der Meer JR (2010) Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J 4:752–763. https://doi.org/10.1038/ismej.2010.5
Schlaeppi K, Dombrowski N, Oter RG, Themaat VLVE, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci USA 111:585–592. https://doi.org/10.1073/pnas.1321597111
Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482. https://doi.org/10.1128/AEM.70.3.1475-1482.2004
Seipke RF, Kaltenpoth M, Hutchings MI (2012) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36:862–876. https://doi.org/10.1111/j.1574-6976.2011.00313.x
Selvakumar G, Krishnamoorthy R, Kim K, Sa TM (2016) Genetic diversity and association characters of bacteria isolated from arbuscular mycorrhizal fungal spore walls. PLoS One, 11(8):e0160356. https://doi.org/10.1371/journal.pone.0160356
Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, Van Overbeek L, Brar D, Van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. MPMI 25:28–36. https://doi.org/10.1094/MPMI-08-11-0204
Sharma S, Compant S, Ballhausen MB, Ruppel S, Franken P (2020) The interaction between Rhizoglomus irregulare and hyphae attached phosphate solubilizing bacteria increases plant biomass of Solanum lycopersicum. Microbiol Res 240:126556. https://doi.org/10.1016/j.micres.2020.126556
Shi Y, Yang H, Zhang T, Sun J, Lou K (2014) Illumina-based analysis of endophytic bacterial diversity and space-time dynamics in sugar beet on the north slope of Tianshan mountain. Appl Microbiol Biotech 98:6375–6385. https://doi.org/10.1007/s00253-014-5720-9
Sikes BA, Kottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280. https://doi.org/10.1111/j.1365-2745.2009.01557.x
Singer E, Bonnette J, Woyke T, Juenger TE (2019) Conservation of endophyte bacterial community structure across two Panicum grass species. Front Microbiol 10:2181. https://doi.org/10.3389/fmicb.2019.02181
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London
Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268. https://doi.org/10.1021/np030397v
Szymańska S, Borruso L, Brusetti L, Hulisz P, Furtado B, Hrynkiewicz K (2018) Bacterial microbiome of root-associated endophytes of Salicornia europaea in correspondence to different levels of salinity. Environ Sci Pollut Res 25:25420–25431. https://doi.org/10.1007/s11356-018-2530-0
Taktek S, Trépanier M, Servin PM, St-Arnaud M, Piché Y, Fortin JA, Antoun H (2015) Trapping of phosphate solubilizing bacteria on hyphae of the arbuscularmycorrhizal fungus Rhizophagus irregularis DAOM 197198. Soil Biol Biochem 90:1–9. https://doi.org/10.1016/j.soilbio.2015.07.016
Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254:34–40. https://doi.org/10.1111/j.1574-6968.2005.00003.x
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304. https://doi.org/10.1111/j.1574-6941.2007.00337.x
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep7:40–50. https://doi.org/10.1111/1758-2229.12181
Turrini A, Avio L, Giovannetti M, Agnolucci M (2018) Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front Plant Sci 9:1407. https://doi.org/10.3389/fpls.2018.01407
Van Overbeek L, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296. https://doi.org/10.1111/j.1574-6941.2008.00469.x
Walley FL, Germida JJ (1996) Failure to decontaminate Glomus clarum NT4 spores is due to spore wall-associated bacteria. Mycorrhiza 6:43–49
Wang Y, Zhang W, Ding C, Zhang B, Huang Q, Huang R, Su X (2019) Endophytic communities of transgenic poplar were determined by the environment and niche rather than by transgenic events. Front Microbiol 10:588. https://doi.org/10.3389/fmicb.2019.00588
Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478. https://doi.org/10.1016/S0038-0717(03)00003-8
Zheng Y, Gong X (2019) Niche differentiation rather than biogeography shapes the diversity and composition of microbiome of Cycas panzhihuaensis. Microbiome 7:152. https://doi.org/10.1186/s40168-019-0770-y