Abstract
Endophytes are microorganisms that live inside plants without causing disease. Maize endophytes collectively encode roughly twenty times as many genes as maize itself, giving the plant access to incredible genetic diversity. They can affect their host plant by altering growth, nutrient acquisition, disease resistance, insect resistance, and abiotic stress tolerance. Despite the richness of these communities, the rules that govern their assembly and their functions within the maize plant are complex and poorly understood. We outline what is known about maize endophytes, including which organisms are known to live inside maize, how they are transmitted, what genomic functions they encode, what effects they have on their host, and how they interact with each other and the maize plant. Many questions still remain about maize endophytes, including what makes a healthy endophyte community, how that community is assembled and develops, and how endophytes can be harnessed to improve agriculture.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Adejumo TO, Orole OO (2010) Effect of pH and moisture content on endophytic colonization of maize roots. Sci Res Essays 5:1655–1661
Akhtar SS, Andersen MN, Naveed M et al (2015) Interactive effect of biochar and plant growth-promoting bacterial endophytes on ameliorating salinity stress in maize. Funct Plant Biol 42:770
Ali S, Kandasamy S, Saldias S, Lazarovits G (2017) Corn and its interactions with bacterial communities. Rhizotrophs: plant growth promotion to bioremediation. Springer, Singapore, pp 145–163
Amin N (2013) Diversity of endophytic fungi from root of Maize var. Pulut (waxy corn local variety of South Sulawesi, Indonesia). Int J Curr Microbiol App Sci 2:148–154
Arnold AE, Mejía LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654
Arnold AE, Miadlikowska J, Higgins KL et al (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297
Arruda L, Beneduzi A, Martins A et al (2013) Screening of rhizobacteria isolated from maize (Zea mays L.) in Rio Grande do Sul State (South Brazil) and analysis of their potential to improve plant growth. Appl Soil Ecol 63:15–22
Bacon CW, Glenn AE, Yates IE (2008) Fusarium verticillioides: managing the endophytic association with maize for reduced fumonisins accumulation. Toxin Rev 27:411–446
Bacon CW, Hinton DM (2002) Endophytic and biological control potential of Bacillus mojavensis and related species. Biol Control 23:274–284
Bacon CW, Hinton DM (1996) Symptomless endophytic colonization of maize by Fusarium moniliforme. Can J Bot Can De Botanique 74:1195–1202
Bacon CW, Hinton DM (2011) In planta reduction of maize seedling stalk lesions by the bacterial endophyte Bacillus mojavensis. Can J Microbiol 57:485–492
Baldani JI, Baldani VLD, Seldin L, Döbereiner J (1986) Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a Root-Associated Nitrogen-Fixing Bacterium. Int J Syst Evol Microbiol 36:86–93
Baldotto MA, Borges Baldotto LE, Santana RB, Marciano CR (2012) Initial performance of maize in response to NPK fertilization combined with Herbaspirillum seropedicae. Revista Ceres 59
Ban Y, Xu Z, Yang Y et al (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27:283–292
Bary A (1866) Morphologie und physiologie der pilze. Flechten und myxomyceten. W Engelmann
Benbrook CM (2016) Trends in glyphosate herbicide use in the united states and globally. Environ Sci Eur 28:3
Besserer A, Puech-Pagès V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226
Bodhankar S, Grover M, Hemanth S et al (2017) Maize seed endophytic bacteria: dominance of antagonistic, lytic enzyme-producing Bacillus spp 3. Biotech 7:232
Bokati D, Herrera J, Poudel R (2016) Soil influences colonization of root-associated fungal endophyte communities of maize, wheat, and their progenitors. J Mycol Plant Pathol 2016:1–9
Brader G, Compant S, Vescio K et al (2017) ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol 55:61–83
Brookes JJ (2017) Endophytes in maize (Zea mays) in New Zealand. Lincoln University
Brusamarello-Santos LC, Gilard F, Brule L et al (2017) Metabolic profiling of two maize (Zea mays L.) inbred lines inoculated with the nitrogen fixing plant-interacting bacteria Herbaspirillum seropedicae and Azospirillum brasilense. PLoS One 12:e0174576
Busby PE, Peay KG, Newcombe G (2016) Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol 209:1681–1692
Busby PE, Soman C, Wagner MR et al (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15
Canellas LP, Balmori DM, Médici LO et al (2012) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366:119–132
Casanovas EM, Barassi CA, Sueldo RJ (2002) azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350
Chelius MK, Triplett EW (2001) The diversity of Archaea and Bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263
Chelius MK, Triplett EW (2000) Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 66:783–787
Chelius MK, Triplett EW, Others (2000) Diazotrophic endophytes associated with maize. Prokaryotic nitrogen fixation: a model system for the analysis of a biological process, pp 779–791
Chen L, Xin X, Zhang J et al (2017) Soil characteristics overwhelm cultivar effects on the structure and assembly of root-associated microbiomes of modern maize. Pedosphere. https://doi.org/10.1016/S1002-0160(17)60370-9
Cherry AJ, Banito A, Djegui D, Lomer C (2004) Suppression of the stem-borer Sesamia calamistis (Lepidoptera; Noctuidae) in maize following seed dressing, topical application and stem injection with African isolates of Beauveria bassiana. Int J Pest Manage 50:67–73
Cherry AJ, Lomer CJ, Djegui D, Schulthess F (1999) Pathogen incidence and their potential as microbial control agents in IPM of maize stem borers in West Africa. Biocontrol 44:301–327
Chulze SN, Palazzini JM, Torres AM et al (2015) Biological control as a strategy to reduce the impact of mycotoxins in peanuts, grapes and cereals in Argentina. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:471–479
Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462
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
Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2017) The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2017.10.004
da Silva DAF, Cotta SR, Vollú RE et al (2014) Endophytic microbial community in two transgenic maize genotypes and in their near-isogenic non-transgenic maize genotype. BMC Microbiol 14:332
David AS, Seabloom EW, May G (2016) Plant host species and geographic distance affect the structure of aboveground fungal symbiont communities, and environmental filtering affects belowground communities in a coastal dune ecosystem. Microb Ecol 71:912–926
de Araujo JM, da Silva AC, Azevedo JL (2000) Isolation of endophytic actinomycetes from roots and leaves of maize (Zea may L.). Braz Arch Biol Technol 43:447–451
Ding T, Su B, Chen X et al (2017) an endophytic bacterial strain isolated from Eucommia ulmoides inhibits southern corn leaf blight. Front Microbiol 8:903
do Amaral FP, Bueno JCF, Hermes VS, Arisi ACM (2014) Gene expression analysis of maize seedlings (DKB240 variety) inoculated with plant growth promoting bacterium Herbaspirillum seropedicae. Symbiosis 62:41–50
ENCODE Project Consortium (2004) The ENCODE (ENCyclopedia Of DNA Elements) project. Science 306:636–640
Estrada P, Mavingui P, Cournoyer B et al (2002) A N2-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico. Can J Microbiol 48:285–294
Ettinger CL, Shehata HR, Johnston-Monje D et al (2015) Draft genome sequence of Burkholderia gladioli strain UCD-UG_CHAPALOTE (Phylum Proteobacteria). Genome Announc 3. https://doi.org/10.1128/genomea.01462-14
Ferrari CS, Amaral FP, Bueno JCF et al (2014) Expressed proteins of Herbaspirillum seropedicae in maize (DKB240) roots-bacteria interaction revealed using proteomics. Appl Biochem Biotechnol 174:2267–2277
Figueiredo JEF, Gomes EA, Guimarães CT et al (2009) Molecular analysis of endophytic bacteria from the genus Bacillus isolated from tropical maize (Zea mays L.). Braz J Microbiol 40:522–534
Fisher PJ, Petrini O, Scott HML (1992) The distribution of some fungal and bacterial endophytes in maize (Zea-Mays L). New Phytol 122:299–305
Flandrois J-P, Perrière G, Gouy M (2015) leBIBIQBPP: a set of databases and a webtool for automatic phylogenetic analysis of prokaryotic sequences. BMC Bioinform 16:251
Food and Agriculture Organization of the United Nations (2017) FAOSTAT statistics database
Fouts DE, Tyler HL, DeBoy RT et al (2008) Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4:e1000141
Frank AC (2011) The genomes of endophytic bacteria. Endophytes of forest trees. Springer, Dordrecht, pp 107–136
Funke T, Han H, Healy-Fried ML et al (2006) Molecular basis for the herbicide resistance of Roundup Ready crops. Proc Natl Acad Sci U S A 103:13010–13015
Gams W (1971) Cephalosporium-artige schimmelpilze (Hyphomycetes). Gustav Fischer Verlag, Stuttgart, West Germany, p 262
Gao J-L, Sun P, Wang X-M et al (2017) Microbacterium zeae sp. nov., an endophytic bacterium isolated from maize stem. Antonie Van Leeuwenhoek 110:697–704
Gao Z, Zhuang J, Chen J et al (2004) Population of entophytic bacteria in maize roots and its dynamic analysis. Ying Yong Sheng Tai Xue Bao 15:1344–1348
Giauque H, Hawkes CV (2013) Climate affects symbiotic fungal endophyte diversity and performance. Am J Bot 100:1435–1444
Glenn AE, Gold SE, Bacon CW (2002) Fdb1 and Fdb2, Fusarium verticillioides loci necessary for detoxification of preformed antimicrobials from corn. Mol Plant Microbe Interact 15:91–101
Glenn AE, Hinton DM, Yates IE, Bacon CW (2001) Detoxification of corn antimicrobial compounds as the basis for isolating Fusarium verticillioides and some other Fusarium species from corn. Appl Environ Microbiol 67:2973–2981
Gold SE, Blacutt AA, Meinersmann RJ, Bacon CW (2014) Whole-genome shotgun sequence of Bacillus mojavensis strain RRC101, an endophytic bacterium antagonistic to the mycotoxigenic endophytic fungus Fusarium verticillioides. Genome Announc 2. https://doi.org/10.1128/genomea.01090-14
Gond SK, Bergen MS, Torres MS, White JF Jr (2015) Endophytic Bacillus spp. Produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87
Goodfellow P (1995) A big book of the human genome. Complement Endeav Nat 377:285–286
Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126
Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154:131–145
Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320
Harman GE, Petzoldt R, Comis A, Chen J (2004) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94:147–153
Hart MM, Powell JR, Gulden RH et al (2009) Separating the effect of crop from herbicide on soil microbial communities in glyphosate-resistant corn. Pedobiologia 52:253–262
Hawkes CV, Connor EW (2017) Translating phytobiomes from theory to practice: ecological and evolutionary considerations. Phytobiomes 1:57–69
Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480
He Y, Yang Z, Li M et al (2017) Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress. Environ Sci Pollut Res Int 24:18494–18504
Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117–125
Hodgson S, de Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208
Hollowell AC, Regus JU, Turissini D et al (2016) Metapopulation dominance and genomic-island acquisition of Bradyrhizobium with superior catabolic capabilities. Proc Biol Sci 283. https://doi.org/10.1098/rspb.2016.0496
Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331:413–425
Ikeda AC, Bassani LL, Adamoski D et al (2013) Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microb Ecol 65:154–160
Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant Microbe Interact 17:1078–1085
Jiao Y, Peluso P, Shi J et al (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527
Johnston-Monje D, Lundberg DS, Lazarovits G et al (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405:337–355
Johnston-Monje D, Mousa WK, Lazarovits G, Raizada MN (2014) Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize. BMC Plant Biol 14
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
Knoth JL, Kim S-H, Ettl GJ, Doty SL (2013) Effects of cross host species inoculation of nitrogen-fixing endophytes on growth and leaf physiology of maize. GCB Bioenerg 5:408–418
Krause A, Ramakumar A, Bartels D et al (2006) Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. Strain BH72. Nat Biotechnol 24:1385–1391
Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31:153–161
Kroll S, Agler MT, Kemen E (2017) Genomic dissection of host–microbe and microbe–microbe interactions for advanced plant breeding. Curr Opin Plant Biol 36:71–78
Kuldau GA, Yates IE (2000) Evidence for Fusarium endophytes in cultivated and wild plants. Microb Endophytes 85–117
Lamb TG, Tonkyn DW, Kluepfel DA (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120
Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Lee K, Pan JJ, May G (2009) Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. FEMS Microbiol Lett 299:31–37
Leggett HC, Buckling A, Long GH, Boots M (2013) Generalism and the evolution of parasite virulence. Trends Ecol Evol 28:592–596
Leslie JF, Pearson CAS, Nelson PE, Toussoun TA (1990) Fusarium spp. From corn, sorghum, and soybean fields in the central and eastern United States. Ecol Stud 44:66
Levy A, Salas Gonzalez I, Mittelviefhaus M et al (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150
Lewis a LC, Berry b EC, Obrycki c JJ, Bing c LA (1996) Aptness of insecticides (Bacillus thuringiensis and carbofuran) with endophytic Beauveria bassiana, in suppressing larval populations of the European corn borer. ELSEVIER Agric Ecosyst Environ 57:27–34
Lewis LC, Cossentine JE (1986) Season long intraplant epizootics of entomopathogens, Beauveria bassiana and Nosema pyrausta, in a corn agroecosystem. Biocontrol 31:363–369
Li T, Liu MJ, Zhang XT et al (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074
Liu X, Hao L, Li D et al (2015a) Long non-coding RNAs and their biological roles in plants. Genomics Proteomics Bioinform 13:137–147
Liu Y, Wang R, Cao Y et al (2015b) Identification and antagonistic activity of endophytic bacterial strain Paenibacillus sp. 5 L8 isolated from the seeds of maize (Zea mays L., Jingke 968). Ann Microbiol 66:653–660
Liu X, Zhao H, Chen S (2006) Colonization of maize and rice plants by strain Bacillus megaterium C4. Curr Microbiol 52:186–190
Liu Y, Wang R, Li Y et al (2017) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of “Beijing” hybrid maize planted in China. Plant Growth Regul 81:317–324
Liu Y, Zuo S, Xu L et al (2012a) 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 et al (2012b) 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
López-Guerrero MG, Ormeño-Orrillo E, Velázquez E et al (2012) Rhizobium etli taxonomy revised with novel genomic data and analyses. Syst Appl Microbiol 35:353–358
Lucangeli C, Bottini R (1997) Effects of Azospirillum spp. On endogenous gibberellin content and growth of maize (Zea mays L.) treated with uniconazole. Symbiosis 23:63–71
Ludueña LM, Anzuay MS, Angelini JG et al (2018) Strain Serratia sp. S119: a potential biofertilizer for peanut and maize and a model bacterium to study phosphate solubilization mechanisms. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2017.12.024
Ludueña LM, Anzuay MS, Angelini JG et al (2017) Role of bacterial pyrroloquinoline quinone in phosphate solubilizing ability and in plant growth promotion on strain Serratia sp. S119. Symbiosis 72:31–43
Madmony A, Chernin L, Pleban S et al (2005) Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol 50:209–216
Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117
Mashiane RA, Ezeokoli OT, Adeleke RA, Bezuidenhout CC (2017) Metagenomic analyses of bacterial endophytes associated with the phyllosphere of a Bt maize cultivar and its isogenic parental line from South Africa. World J Microbiol Biotechnol 33:80
Matsumura EE, Secco VA, Moreira RS et al (2015) Composition and activity of endophytic bacterial communities in field-grown maize plants inoculated with Azospirillum brasilense. Ann Microbiol 65:2187–2200
McInroy JA, Kloepper JW (1991) Endophytic bacteria from field-grown corn and cotton
McInroy JA, Kloepper JW (1995a) Population dynamics of endophytic bacteria in field-grown sweet corn and cotton. Can J Microbiol 41:895–901
McInroy JA, Kloepper JW (1995b) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342
Medini D, Donati C, Tettelin H et al (2005) The microbial pan-genome. Curr Opin Genet Dev 15:589–594
Menéndez E, Ramirez-Bahena MH, Peix A et al (2016) Analysis of cultivable endophytic bacteria in roots of maize in a soil from león province in mainland spain. Biological nitrogen fixation and beneficial plant-microbe interaction. Springer, Cham, pp 45–53
Messing J, Bharti AK, Karlowski WM et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354
Michael TP, Jackson S (2013) The first 50 plant genomes. Plant Genome 6
Mitter B, Petric A, Shin MW et al (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120
Mohanty SR, Dubey G, Kollah B (2017) Endophytes of Jatropha curcas promote growth of maize. Rhizosphere 3:20–28
Montañez A, Abreu C, Gill PR et al (2008) Biological nitrogen fixation in maize (Zea mays L.) by 15 N isotope-dilution and identification of associated culturable diazotrophs. Biol Fertil Soils 45:253–263
Montañez A, Blanco AR, Barlocco C et al (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28
Monteiro RA, Schmidt MA, de Baura VA et al (2008) Early colonization pattern of maize (Zea mays L. Poales, Poaceae) roots by Herbaspirillum seropedicae (Burkholderiales, Oxalobacteraceae). Genet Mol Biol 31:932–937
Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13
Mousa WK, Shearer CR, Limay-Rios V et al (2015) Bacterial endophytes from wild maize suppress Fusarium graminearum in modern maize and inhibit mycotoxin accumulation. Front Plant Sci 6:805
Nassar AH, El-Tarabily KA, Sivasithamparam K (2005) Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 42:97–108
Naveed M, Mitter B, Reichenauer TG et al (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39
Nelson PG, May G (2017) Coevolution between Mutualists and parasites in symbiotic communities may lead to the evolution of lower virulence. Am Nat 190:803–817
Nettles R, Watkins J, Ricks K, et al (2016) Influence of pesticide seed treatments on rhizosphere fungal and bacterial communities and leaf fungal endophyte communities in maize and soybean. Appl Soil Ecol 102:61–69
Nolan BLF (2016) The effects of tillage, glyphosate, and genetic modification on bacterial root endophyte composition in Zea mays. Undergraduate, The University of Mississippi
Orole OO, Adejumo TO (2009) Activity of fungal endophytes against four maize wilt pathogens. Afr J Microbiol Res 3:969–973
Orole OO, Adejumo TO (2011) Bacterial and fungal endophytes associated with grains and roots of maize. J Ecol Nat Environ 3:298–303
Palma L, Muñoz D, Berry C et al (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6:3296–3325
Palus JA, Borneman J, Ludden PW, Triplett EW (1996) A diazotrophic bacterial endophyte isolated from stems of Zea mays L. and Zea luxurians Iltis and Doebley. Plant Soil 186:135–142
Pan JJ, Baumgarten AM, May G (2008) Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays). New Phytol 178:147–156
Pan JJ, May G (2009) Fungal-fungal associations affect the assembly of endophyte communities in maize (Zea mays). Microb Ecol 58:668–678
Pedrosa FO, Monteiro RA, Wassem R et al (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7:e1002064
Pereira P, Ibáñez F, Rosenblueth M, et al (2011) Analysis of the bacterial diversity associated with the roots of maize (Zea mays L.) through culture-dependent and culture-independent methods. ISRN Ecol 2011
Pertea M, Salzberg SL (2010) Between a chicken and a grape: estimating the number of human genes. Genome Biol 11:206
Peterson SW, Jurjević Ž (2017) New species of Talaromyces isolated from maize, indoor air, and other substrates. Mycologia 109:537–556
Petrini O (1991) Fungal Endophytes of Tree Leaves. Microbial ecology of leaves. Springer, New York, NY, pp 179–197
Poling SM, Wicklow DT, Rogers KD, Gloer JB (2008) Acremonium zeae, a protective endophyte of maize, produces dihydroresorcylide and 7-hydroxydihydroresorcylides. J Agric Food Chem 56:3006–3009
Potshangbam M, Devi SI, Sahoo D, Strobel GA (2017) Functional Characterization of Endophytic Fungal Community Associated with Oryza sativa L and Zea maysL. Front Microbiol 8:325
Pray L (2008) Eukaryotic genome complexity. Nature. Education 1:96
Prischl M, Hackl E, Pastar M et al (2012) Genetically modified Bt maize lines containing cry3Bb1, cry1A105 or cry1Ab2 do not affect the structure and functioning of root-associated endophyte communities. Appl Soil Ecol 54:39–48
Proença DN, Schwab S, Baldani JI, Morais PV (2017) Diversity and function of endophytic microbial community of plants with economical potential. In: de Azevedo JL, Quecine MC (eds) Diversity and benefits of microorganisms from the tropics. Springer International Publishing, Cham, pp 209–243
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
Riggs PJ, Chelius MK, Iniguez AL et al (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:829–836
Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802–808
Rodriguez Estrada AE, Hegeman A, Corby Kistler H, May G (2011) In vitro interactions between Fusarium verticillioides and Ustilago maydis through real-time PCR and metabolic profiling. Fungal Genet Biol 48:874–885
Roesch LFW, Camargo FAO, Bento FM, Triplett EW (2008) Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302:91–104
Roesch LFW, Olivares FL, Pereira Passaglia LM et al (2006) Characterization of diazotrophic bacteria associated with maize: effect of plant genotype, ontogeny and nitrogen-supply. World J Microbiol Biotechnol 22:967–974
Roncato-Maccari LDB, Ramos HJO, Pedrosa FO et al (2003) Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants. FEMS Microbiol Ecol 45:39–47
Roos IMM, Hattingh MJ (1983) Scanning electron microscopy of Pseudomonas syringae pv, morsprunorum on sweet cherry leaves. J Phytopathol 108:18–25
Rosenblueth M, Martinez-Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181:337–344
Sandhya V, Shrivastava M, Ali SZ, Sai Shiva V (2017) Endophytes from maize with plant growth promotion and biocontrol activity under drought stress. Russ Agric Sci 43:22–34
Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767
Santos F, Peñaflor MFGV, Paré PW et al (2014) A novel interaction between plant-beneficial rhizobacteria and roots: colonization induces corn resistance against the root herbivore Diabrotica speciosa. PLoS One 9:e113280
Saunders M, Glenn AE, Kohn LM (2010) Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537
Saunders M, Kohn LM (2009) Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytol 182:229–238
Saunders M, Kohn LM (2008) Host-synthesized secondary compounds influence the in vitro interactions between fungal endophytes of maize. Appl Environ Microbiol 74:136–142
Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol 33:69–82
Seghers D, Wittebolle L, Top EM et al (2004) Impact of agricultural practices on the Zea mays L. Endophytic community. Appl Environ Microbiol 70:1475–1482
Sessitsch A, Coenye T, Sturz AV et al (2005) Burkholderia phytofirmans sp. nov, a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192
Shehata H (2016) Molecular and physiological mechanisms underlying the antifungal and nutrient acquisition activities of beneficial microbes
Shehata HR, Griffiths MW, Raizada MN (2017) seeds of the wild progenitor of maize possess bacteria that antagonize foodborne pathogens. Foodborne Pathog Dis 14:202–209
Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016) Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J Appl Microbiol 120:756–769
Shehata HR, Raizada MN (2017) A Burkholderia endophyte of the ancient maize landrace Chapalote utilizes c-di-GMP-dependent and independent signaling to suppress diverse plant fungal pathogen targets. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx138
Sheibani-Tezerji R, Naveed M, Jehl M-A et al (2015) The genomes of closely related Pantoea ananatis maize seed endophytes having different effects on the host plant differ in secretion system genes and mobile genetic elements. Front Microbiol 6:440
Siegel MR, Johnson MC, Varney DR et al (1984) A fungal endophyte in tall fescue: incidence and dissemination. Phytopathology 74:932–937
Sobowale AA, Cardwell KF, Odebode AC et al (2007) Persistence of Trichoderma species within maize stem against Fusarium verticillioides. Arch Phytopathol Plant Prot 40:215–231
Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 117–143
Sun C, Geng L, Wang M, et al (2017) No adverse effects of transgenic maize on population dynamics of endophytic Bacillus subtilis strain B916-gfp. Microbiologyopen 6. https://doi.org/10.1002/mbo3.404
Syed NH, Kalyna M, Marquez Y et al (2012) Alternative splicing in plants–coming of age. Trends Plant Sci 17:616–623
Szilagyi-Zecchin VJ, Ikeda AC, Hungria M, et al (2014) Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4:26
Takenaka M, Zehrmann A, Verbitskiy D et al (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352
Taurian T, Anzuay MS, Angelini JG et al (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431
Thiebaut F, Rojas CA, Grativol C et al (2014) Genome-wide identification of microRNA and siRNA responsive to endophytic beneficial diazotrophic bacteria in maize. BMC Genom 15:766
Toruño TY, Stergiopoulos I, Coaker G (2016) Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu Rev Phytopathol 54:419–441
U’Ren JM, Lutzoni F, Miadlikowska J et al (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914
Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448
Venter JC, Adams MD, Myers EW et al (2001) The sequence of the human genome. Science 291:1304–1351
Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24
Wagner BL, Lewis LC (2000) Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 66:3468–3473
Wang J-L, Li T, Liu G-Y et al (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Rep 6:22028
Weilharter A, Mitter B, Shin MV et al (2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol 193:3383–3384
Wicklow DT, Poling SM (2009) Antimicrobial activity of pyrrocidines from Acremonium zeae against endophytes and pathogens of maize. Phytopathology 99:109–115
Wicklow DT, Roth S, Deyrup ST, Gloer JB (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109:610–618
Williams WP, Paul Williams W, Ozkan S et al (2011) Ear rot, aflatoxin accumulation, and fungal biomass in maize after inoculation with Aspergillus flavus. Field Crops Res 120:196–200
Xia Y, DeBolt S, Dreyer J et al (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci 6:490
Yang X, Xie L, Li Y, Wei C (2009) More than 9,000,000 unique genes in human gut bacterial community: estimating gene numbers inside a human body. PLoS One 4:e6074
Young L-S, Hameed A, Peng S-Y et al (2013) Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74 enhances growth and P-utilization rate in maize (Zea mays L.). Appl Soil Ecol 66:40–47
Zhang S (2016) Good riddance, chemicals: microbes are farming’s hot new pesticides. https://www.wired.com/2016/03/good-riddance-chemicals-microbes-farmings-hot-new-pesticides/
Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci USA 109:13022–13027
Zinniel DK, Lambrecht P, Harris NB et al (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Wallace, J.G., May, G. (2018). Endophytes: The Other Maize Genome. In: Bennetzen, J., Flint-Garcia, S., Hirsch, C., Tuberosa, R. (eds) The Maize Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-97427-9_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-97427-9_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-97426-2
Online ISBN: 978-3-319-97427-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)