Abstract
The genus Fusarium consists of 100 or more valid species, although it is anticipated that additional cryptic species will be defined. We are concerned with one species F. verticillioides (Saccardo) Nirenberg, the sexual stage of which is Gibberella moniliformis Wineland. Historically, this fungus was based on the broad concept of Fusarium nomenclature, and the common synonyms F. moniliforme or Gibberella fujikuroi, mating population A, were used. In this review, both synonyms will be used depending upon the author’s earlier citations. F. verticillioides under its various synonyms is associated with well over 32 plant families and is known to be seed-borne on at least 10 of these, where it causes seedling blights, root rots, stem rots, and pre- and post-harvest kernel rots. Thus, this species and other Fusarium species are nonhost-specific or host generalists. F. verticillioides, however, is a noted parasite of maize and is found throughout the world wherever maize is grown. Of considerable importance is that this fungus infects maize as a symptomless endophyte, where it produces several homologues of the fumonisin mycotoxins, primarily fumonisin B1 and B2. The fumonisins produce toxicity syndromes in livestock, poultry, and is implicated in several human diseases. Surveys indicate that approximately 95% of the world’s isolates are capable of producing this group of mycotoxins apparently resulting from the endophytic infection. In addition to the fumonisins, F. verticillioides produces several other metabolites of varying toxicities to plants and animals. Fusaric acid is one such toxin although it is produced by this and all other fusaria examined. The role of fusaric acid within the association now includes activity as a quorum sensing inhibitor. Quorum sensing is crucial to the proper performance and ecological fitness of most microbial populations, including fungi. Inhibiting this mechanism dooms most organisms to low competitive interspecific and intraspecific competition, while allowing the fusaria to dominate the intercellular spaces of maize. Thus, importance of quorum sensing is briefly reviewed along with the emphasis that it might play in maintaining dominant interactions among other F. verticillioides as a means of control or regulating competing organisms.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abe CAL, Faria CB, Castro FF, de Souza SR, Santos FC, da Silva CN, Tessmann DJ, Barbosa-Tessmann IP (2015) Fungi isolated from maize (Zea mays L.) grains and production of associated enzyme activities. Int J Mol Sci 16:15328–15346
Andreote FD, de Araujo WI, de Azevedo JL, van Elas JD, da Rocha UN et al (2009) Endophytic colonization of potato (Solanum tuberosum L) by a novel competent bacterial endophyte, Pseudomonas putida strain P9, and its effect on associated bacterial communities. Appl Environ Microbiol 75:3396–3406
Bacon CW, Hinton DM (1996) Symptomless endophytic colonization of maize by Fusarium moniliforme. Can J Bot 74:1195–1202
Bacon CW, Nelson PE (1994) Fumonisin production in maize by toxigenic strains of Fusarium moniliforme and Fusarium proliferatum. J Food Protect 57:514–521
Bacon CW, Bennett RM, Hinton DM, Voss KA (1992) Scanning electron microscopy of Fusarium moniliforme within asymptomatic maize kernels and kernels associated with equine leukoencephalomalacia. Plant Dis 76:144–148
Bacon CW, Porter JK, Norred WP, Leslie JF (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62:4039–4043
Bacon CW, Hinton DM, Glenn AE, Macias FA, Marin D (2007) Interaction of Bacillus mojavensis and Fusarium verticillioides with a benzoxazolinone (BOA) and its transformation product, APO. J Chem Ecol 33:1885–1897
Blacutt AA, Mitchell TR, Bacon CW, Gold SE (2016) Bacillus mojavensis RRC101 lipopeptides provoke physiological and metabolic changes during antagonism against Fusarium verticillioides. Mol Plant Micro Inter 29(9):713–723
Broomhead JN, Ledoux DR, Bermudez AJ, Rottinghaus GE (2002) Chronic effects of fumonisin B1 in broilers and turkeys fed dietary treatments to market age poultry. Science 81:56–611
Cambrier V, Hance T, de-Hoffmann E (1999) Non-injured maize contains several 1,4-benzoxazin-3-one related compounds but only as glucoconjugates. Phytochem Anal 10:119–126
Cambrier V, Hance T, de-Hoffmann E (2000) Variation of DIMBOA and related compounds content in relation to the age and plant origin in maize. Phytochemistry 53:223–229
Defoirdt T, Brackman G, Coenye T (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol 21:619–624
Desjardins AE, Plattner RD, Gordon TR (2000) Gibberella fujikuroi mating population A and Fusarium subglutinans from teosinte species and maize corn from Mexico and Central America. Mycol Res 104:865–872
Faure D, Vereecke D, Leveau JYH (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303
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
Fuqua WC, Winans SC, Greenburg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-dependent transcriptional regulators. J Bacteriol 176:269–275
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
Guo B, Zhang Y, li S, Lai T, Chen J, Ding W (2016) Extract from maize (Zea mays L.): antibacterial activity of DIMBOA and its derivatives against Ralstonia solanacearum. Molecules 21:1396–1419
Hardoim PR, Hardoim CP, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7(2):e30438. https://doi.org/10.1371/journal-pone.0030438
Hartman A, Schikora A (2012) Quorum sensing of bacteria and tans-kingdom interaction of N-acyl homoserine lactone with eukaryotes. J Chem Ecol 38:740–713
Helman Y, Chernin L (2014) Silencing the mod: disrupting quorum sensing as a means to fight plant disease. Mol Plant Pathol 16(3):316–329. https://doi.org/10.1111/mpp.12180
Hyun-Soo C, Park S-Y, Ryu C-M, Kim JF, Kim J-G, Park S-H (2007) Interference of quorum sensing and virulence of the rice pathogen Bukholderia glumae by an engineered endophytic bacterium. FEMS Microbiol Ecol 60:14–23
Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography, and ecology. PLoS One 6:1–22
Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization, and distribution within plant. Microorganisms 5:77–103
Krings M, Hass H, Kerp H, Taylor TN, Agerer R, Dotzler N (2005) Endophytic cyanobacteria in a 400-million -yr.-old plant: a scenario for the origin of a symbiosis? Rev Palaeobot Palyno 153:62–69
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermen EJ (2007a) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution and host responses. New Phytol 174:648–657
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007b) An alternative mode of early land plant colonization by putative endomycorrhizal fungi. Plant Sig Behavior 2:125–126
LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Evol 77:73–111
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell, Iowa
Leslie JF, Plattner RD, Desjardins AE, Llitich CJR (1992) Fumonisin B1 production and vegetative compatibility of strains from Gibberella fujikuroi mating population “A” (Fusarium moniliforme). Mycopathologia 117:37–45
Lewis DH (1974) Micro-organisms and plants: the evolution of parasitism and mutualism. Symp Soc Gen Microbiol 24:374–392
Liu Y, Zuo S, Zou Y, Wand J, Song W (2013) Study on diversity of endophytic bacterial communities in seed of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012
Lopez D, Vlamakis H, Losick R, Kolter R (2009) Paracrine signaling in a bacterium. Genes Dev 23:1631–1638
Margulis L (1976) Genetic and evolutionary consequences of symbiosis. Exp Parasitol 39:277–349
Martin-Rodriguez AJ, Reyer F, Martin J, Perez-Yepez J, Leon-Barrios M, Couttolene A, Espinoza C, Trigos A, Martin VS, Norte M, Pernandez JJ (2014) Inhibition of bacterial quorum sensing by extracts from aquatic fungi: first reports from marine endophytes. Mar Drugs 12:5503–5526
Matsuoka Y, Vigouroux Y, Dermastia M, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084
McLean RJC, Pierson LS, Fuqua C (2004) A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 58:351–360
Mookherjee A, Singh S, Maiti MK (2017) Quorum sensing inhibitors: can endophytes be prospective sources? Arch Microbiol 200(2):355–369. https://doi.org/10.1007/s00203-017-1437-3
Mousa WK, Shearer CR, Limay-Rios V, Zhou T, Raizada MN (2015) Bacterial endophytes from maize suppress Fusarium graminearum in modern maize and inhabit mycotoxin accumulation. Front Plant Sci 6:805–824
Mukhopadhyay K, Gassison NK, Hinton DM, Bacon CW, Khush GS, Peck HD Data N (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134:151–159
Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32:694–698
Nelson EK (2017) The seed microbiome: origins, interactions, and impacts. Plant Soil 422:7–34
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248
Niemeyer HM (1988) Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones), defense chemical in the Gramineae. Phytochemistry 27:3349–3358
Niemeyer HM (2009) Hydroxamic acids derived from 2-hydrox-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J Agric Chem 57:1677–1696
O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematic and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493
Ongena M, Jourdan E, Adam A, Paquot M, Brana A, Joris B, Arpignyy J-L, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090
Park WJ, Hochholdinger F, Giel A (2004) Release of the benzoxazinoids defense molecules during lateral and crown rot emergency in Zea mays. J Plant Physiol 161:981–985
Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R (2009) Starch grain and phytolith evidence for early ninth millennium B.P. maize from the central Balsas River Valley, Mexico. Proc Natl Acad Sci USA 106:5019–5024
Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Kote M, Nielsen J, Eberl L, Givskov M (2005a) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814
Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK, Christensen KB, Jensen PO, Andersen JB, Koch B, Larsen TO, Hentzer M, Eberl L, Hoib N, Givskov M (2005b) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340
Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716
Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802–808
Riley RT, Voss KA, Yoo H-S, Gelderblom WCA, Merrill AH (1994) Mechanisms of fumonisins toxicity and carcinogenesis. J Food Protec 57:638–645
Rodrigues AC, de Oliveria BD, de Silva ER, Sacramento NTB, Bertoldi MC, Pinto UM (2015) Food Sci Technol Campinas 36:337–343
Rodriguez RJ, White Jr JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Saikkonen K, Wali P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280
Schikora A, Schenk ST, Hartmann A (2016) Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl homoserine lactone group. Plant Mol Biol 90:605–612
Shahzad R, Khan AL, Bilal S, Lee I-J (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant. Growth Front Plant Sci 9:24. https://doi.org/10.3389/fpls.2018.00024
Sheiner EK, Rumbaugh KP, Williams SC (2005) Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29:935–947
Shephard GS, Thiel PG, Stockenström S, Sydenham EW (1996) Worldwide survey of fumonisin contamination of corn and corn-based products. J Assoc Off Anal Chem Int 79:671–687
Snook ME, Mitchell T, Hinton DM, Bacon CW (2009) Isolation and characterization of Leu-7 surfactin from the endophytic bacterium Bacillus mojavensis RRC 101, a biocontrol agent for Fusarium verticillioides. J Agric Food Chem 57:4287–4292
Subramoni S, Nathoo N, Klimov E, Vuan A-C (2014) Agrobacterium tumefaciens responses to plant-derived signaling molecules. Front Plant Sci 5:1–12
Summerell BA, Laurence EB, Liew ECY, Leslie JF (2010) Biogeography and phylogeography of Fusarium: a review. Fungal Divers 44:3–13
Tan SY, Chua SL, Chen Y, Rice SA, Kjelleberg S, Nielsen TE, Yang L, Gibskov M (2013) Identification of five structurally unrelated quorum-sensing inhibitors of Pseudomonas aeruginosa from a natural-derived database. Antimicro Agents Chemother 57:5629–5641
Taylor JW, Berbee MI (2006) Dating divergence in the fungal tree of life: review and new analyses. Mycology 98:838–849
Taylor TN, Krings M (2005) Fossil microorganisms and land plants: associations and interactions. Symbiosis 40:119–135
Thiel PG, Gelderblom WCA, Marasas WFO, Nelson PE, Wilson TM (1986) Survey of fumonisin production by Fusarium species. Appl Environ Microbiol 57:1098–1093
Tung TT, Jakobsen TH, Dao TT, Fuglsang AT, Givskov M, Christensen SB, Nielsen J (2017) Fusaric acid and analogues as gram-negative bacterial quorum sensing inhibitors. Eur J Med Chem 126:1011–1020
Verbeke F, Craemer SD, Debuune N, Janssens Y, Wynendaele E, Van de Wiele C, Spiegleer BD (2017) Peptides as quorum sensing molecules: measurement techniques and obtained levels in vitro and in vivo. Front Neuro Sci 11:183–201
Voss KA, Norred WP, Plattner RD, Bacon CW (1989) Hepatotoxicity and renal toxicity in rats of corn samples associated with field cases of equine leukoencephalomalacia. Food Chem Toxicol 27:89–96
Yang L, Zuo S, Zou Y, Wang J, Song W (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L, Nogda 108) at different growth stages. Ann Microbiol 63:71–79
Yates IE, Jaworski AJ (2000) Differential growth of Fusarium moniliforme relative to tissues from ‘Silver queen’, a sweet maize. Can J Bot 78:472–480
Yates IE, Hiett KL, Kapczynski DR, Smart W, Glenn AE, Hinton DM, Bacon CW, Meinersmann R, Liu S, Jaworski AJ (1999) Gus transformation of the maize fungal endophyte Fusarium moniliforme. Mycol Res 103:129–136
Yue Q, Bacon CW, Richardson MD (1998) Biotransformation of BOA and 6-methoxy-benzoxazolinone by Fusarium moniliforme. Phytochemistry 48:451–454
Zhang J, Boone L, Kocz R, Zhang C, Binns AN, Lynn DG (2000) At the maize/Agrobacterium interfaces natural factors limiting host transformation. Chem Biol 7:611–621
Zuniga A, Poupin MJ, Donso R, Ledger T, Guiliani N, Gutierrez RA, Gonzalez B (2013) Quorum sensing and indol-3-acitic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant Microbe Interact 26:546–553
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bacon, C.W., Hinton, D.M. (2019). Fungal and Bacterial Maize Kernel Interactions with the Vertically Transmitted Endophytic State of Fusarium verticillioides. In: Verma, S., White, Jr, J. (eds) Seed Endophytes. Springer, Cham. https://doi.org/10.1007/978-3-030-10504-4_10
Download citation
DOI: https://doi.org/10.1007/978-3-030-10504-4_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-10503-7
Online ISBN: 978-3-030-10504-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)