Skip to main content

Endophytes: The Other Maize Genome

  • Chapter
  • First Online:
The Maize Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bacon CW, Glenn AE, Yates IE (2008) Fusarium verticillioides: managing the endophytic association with maize for reduced fumonisins accumulation. Toxin Rev 27:411–446

    Article  CAS  Google Scholar 

  • Bacon CW, Hinton DM (2002) Endophytic and biological control potential of Bacillus mojavensis and related species. Biol Control 23:274–284

    Article  CAS  Google Scholar 

  • Bacon CW, Hinton DM (1996) Symptomless endophytic colonization of maize by Fusarium moniliforme. Can J Bot Can De Botanique 74:1195–1202

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Bary A (1866) Morphologie und physiologie der pilze. Flechten und myxomyceten. W Engelmann

    Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the united states and globally. Environ Sci Eur 28:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besserer A, Puech-Pagès V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Brookes JJ (2017) Endophytes in maize (Zea mays) in New Zealand. Lincoln University

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busby PE, Peay KG, Newcombe G (2016) Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol 209:1681–1692

    Article  CAS  PubMed  Google Scholar 

  • Busby PE, Soman C, Wagner MR et al (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Casanovas EM, Barassi CA, Sueldo RJ (2002) azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • ENCODE Project Consortium (2004) The ENCODE (ENCyclopedia Of DNA Elements) project. Science 306:636–640

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (2017) FAOSTAT statistics database

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank AC (2011) The genomes of endophytic bacteria. Endophytes of forest trees. Springer, Dordrecht, pp 107–136

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gams W (1971) Cephalosporium-artige schimmelpilze (Hyphomycetes). Gustav Fischer Verlag, Stuttgart, West Germany, p 262

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Giauque H, Hawkes CV (2013) Climate affects symbiotic fungal endophyte diversity and performance. Am J Bot 100:1435–1444

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Goodfellow P (1995) A big book of the human genome. Complement Endeav Nat 377:285–286

    CAS  Google Scholar 

  • Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hawkes CV, Connor EW (2017) Translating phytobiomes from theory to practice: ecological and evolutionary considerations. Phytobiomes 1:57–69

    Article  Google Scholar 

  • Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117–125

    Article  CAS  PubMed  Google Scholar 

  • Hodgson S, de Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant Microbe Interact 17:1078–1085

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Peluso P, Shi J et al (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31:153–161

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kuldau GA, Yates IE (2000) Evidence for Fusarium endophytes in cultivated and wild plants. Microb Endophytes 85–117

    Google Scholar 

  • Lamb TG, Tonkyn DW, Kluepfel DA (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120

    Article  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Leggett HC, Buckling A, Long GH, Boots M (2013) Generalism and the evolution of parasite virulence. Trends Ecol Evol 28:592–596

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Levy A, Salas Gonzalez I, Mittelviefhaus M et al (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Lewis LC, Cossentine JE (1986) Season long intraplant epizootics of entomopathogens, Beauveria bassiana and Nosema pyrausta, in a corn agroecosystem. Biocontrol 31:363–369

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liu X, Zhao H, Chen S (2006) Colonization of maize and rice plants by strain Bacillus megaterium C4. Curr Microbiol 52:186–190

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McInroy JA, Kloepper JW (1991) Endophytic bacteria from field-grown corn and cotton

    Google Scholar 

  • McInroy JA, Kloepper JW (1995a) Population dynamics of endophytic bacteria in field-grown sweet corn and cotton. Can J Microbiol 41:895–901

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Medini D, Donati C, Tettelin H et al (2005) The microbial pan-genome. Curr Opin Genet Dev 15:589–594

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michael TP, Jackson S (2013) The first 50 plant genomes. Plant Genome 6

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Mohanty SR, Dubey G, Kollah B (2017) Endophytes of Jatropha curcas promote growth of maize. Rhizosphere 3:20–28

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Nolan BLF (2016) The effects of tillage, glyphosate, and genetic modification on bacterial root endophyte composition in Zea mays. Undergraduate, The University of Mississippi

    Google Scholar 

  • Orole OO, Adejumo TO (2009) Activity of fungal endophytes against four maize wilt pathogens. Afr J Microbiol Res 3:969–973

    Google Scholar 

  • Orole OO, Adejumo TO (2011) Bacterial and fungal endophytes associated with grains and roots of maize. J Ecol Nat Environ 3:298–303

    Google Scholar 

  • Palma L, Muñoz D, Berry C et al (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6:3296–3325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pan JJ, May G (2009) Fungal-fungal associations affect the assembly of endophyte communities in maize (Zea mays). Microb Ecol 58:668–678

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Pertea M, Salzberg SL (2010) Between a chicken and a grape: estimating the number of human genes. Genome Biol 11:206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson SW, Jurjević Ž (2017) New species of Talaromyces isolated from maize, indoor air, and other substrates. Mycologia 109:537–556

    PubMed  Google Scholar 

  • Petrini O (1991) Fungal Endophytes of Tree Leaves. Microbial ecology of leaves. Springer, New York, NY, pp 179–197

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Pray L (2008) Eukaryotic genome complexity. Nature. Education 1:96

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443

    Article  PubMed  Google Scholar 

  • Riggs PJ, Chelius MK, Iniguez AL et al (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:829–836

    Google Scholar 

  • Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802–808

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Roos IMM, Hattingh MJ (1983) Scanning electron microscopy of Pseudomonas syringae pv, morsprunorum on sweet cherry leaves. J Phytopathol 108:18–25

    Article  Google Scholar 

  • Rosenblueth M, Martinez-Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181:337–344

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Saunders M, Kohn LM (2009) Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytol 182:229–238

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol 33:69–82

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shehata H (2016) Molecular and physiological mechanisms underlying the antifungal and nutrient acquisition activities of beneficial microbes

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel MR, Johnson MC, Varney DR et al (1984) A fungal endophyte in tall fescue: incidence and dissemination. Phytopathology 74:932–937

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Takenaka M, Zehrmann A, Verbitskiy D et al (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  CAS  PubMed  Google Scholar 

  • Venter JC, Adams MD, Myers EW et al (2001) The sequence of the human genome. Science 291:1304–1351

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wagner BL, Lewis LC (2000) Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 66:3468–3473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wicklow DT, Poling SM (2009) Antimicrobial activity of pyrrocidines from Acremonium zeae against endophytes and pathogens of maize. Phytopathology 99:109–115

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jason G. Wallace .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

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

Publish with us

Policies and ethics