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Decreased Root-Knot Nematode Gall Formation in Roots of the Morning Glory Ipomoea tricolor Symbiotic with Ergot Alkaloid-Producing Fungal Periglandula Sp.

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Abstract

Many species of morning glories (Convolvulaceae) form symbioses with seed-transmitted Periglandula fungal endosymbionts, which produce ergot alkaloids and may contribute to defensive mutualism. Allocation of seed-borne ergot alkaloids to various tissues of several Ipomoea species has been demonstrated, including roots of I. tricolor. The goal of this study was to determine if infection of I. tricolor by the Periglandula sp. endosymbiont affects Southern root-knot nematode (Meloidogyne incognita) gall formation and host plant biomass. We hypothesized that I. tricolor plants infected by Periglandula (E+) would develop fewer nematode-induced galls compared to non-symbiotic plants (E-). E+ or E- status of plant lines was confirmed by testing methanol extracts from individual seeds for endosymbiont-produced ergot alkaloids. To test the effects of Periglandula on nematode colonization, E+ and E- I. tricolor seedlings were grown in soil infested with high densities of M. incognita nematodes (N+) or no nematodes (N-) for four weeks in the greenhouse before harvesting. After harvest, nematode colonization of roots was visualized microscopically, and total gall number and plant biomass were quantified. Four ergot alkaloids were detected in roots of E+ plants, but no alkaloids were found in E- plants. Gall formation was reduced by 50% in E+ plants compared to E- plants, independent of root biomass. Both N+ plants and E+ plants had significantly reduced biomass compared to N- and E- plants, respectively. These results demonstrate Periglandula’s defensive role against biotic enemies, albeit with a potential trade-off with host plant growth.

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References

  • Afkhami ME, Rudgers JA (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am Nat 172:405–416

    Article  PubMed  Google Scholar 

  • Ahimsa-Muller MA, Markert A, Hellwig S, Knoop V, Steiner U, Drewke C, Leistner E (2007) Clavicipitaceous fungi associated with ergoline alkaloid-containing Convolvulaceae. J Nat Prod 70:1955–1960

    Article  PubMed  CAS  Google Scholar 

  • Amor-Prats D, Harborne JB (1993) Allelochemical effects of ergoline alkaloids from Ipomoea parasitica on Heliothis virescens. Chemoecology 4:55–61

    Article  CAS  Google Scholar 

  • Anaya AL, Calera MR, Mata R, Pereda-Miranda R (1990) Allelopathic potential of compounds isolated from Ipomoea tricolor Cav. (Convolvulaceae). J Chem Ecol 16:2145–2152

    Article  CAS  PubMed  Google Scholar 

  • Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacetty AA, Snook ME, Glenn AE, Noe JP, Hill N, Culbreath A, Timper P, Nagabhyru P, Bacon CW (2009a) Toxicity of endophyte-infected tall fescue alkaloids and grass metabolites on Pratylenchus scribneri. Phytopathology 99:1336–1345

    Article  CAS  PubMed  Google Scholar 

  • Bacetty AA, Snook ME, Glenn AE, Noe JP, Nagabhyru P, Bacon CW (2009b) Chemotaxis disruption in Pratylenchus scribneri by tall fescue root extracts and alkaloids. J Chem Ecol 35:844–850

    Article  CAS  PubMed  Google Scholar 

  • Barbosa RC, Riet-Correa F, Medeiros RM, Lima EF, Barros SS, Gimeno EJ, Molyneux RJ, Gardner DR (2006) Intoxication by Ipomoea sericophylla and Ipomoea riedelii in goats in the state of Paraíba, northeastern Brazil. Toxicon 47:371–379

    Article  CAS  PubMed  Google Scholar 

  • Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Ann Rev Ecol Evol Syst 40:1–20

    Article  Google Scholar 

  • Beaulieu WT, Panaccione DG, Hazekamp CS, Mckee MC, Ryan KL, Clay K (2013) Differential allocation of seed-borne ergot alkaloids during early ontogeny of morning glories (Convolvulaceae). J Chem Ecol 39:919–930

    Article  CAS  PubMed  Google Scholar 

  • Beaulieu WT, Panaccione DG, Ryan KL, Kaonongbua W, Clay K (2015) Phylogenetic and chemotypic diversity of Periglandula species in eight new morning glory hosts (Convolvulaceae). Mycologia 107:667–678

    Article  CAS  PubMed  Google Scholar 

  • Bridge J, Plowright RA, Peng D (1990) Nematode parasites of rice. In: Luc M (ed) Plant parasitic nematodes in subtropical and tropical agriculture. CABI Publishing, Wallingford, UK, pp 69–108

    Google Scholar 

  • Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrd DW Jr, Ferris HO, Nusbaum CJ (1972) A method for estimating numbers of eggs of Meloidogyne spp. in soil. J Nematology 4:266–269

    CAS  Google Scholar 

  • Cervantes-Flores JC, Yencho GC (2002) Host reactions of sweetpotato genotypes to root-knot nematodes and variation in virulence of Meloidogyne incognita populations. HortScience. 37:1112–1116

    Article  Google Scholar 

  • Cheplick GP, Clay K, Wray S (1989) Interactions between fungal endophyte infection and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97

    Article  Google Scholar 

  • Christian N, Herre EA, Mejia LC, Clay K (2017) Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc R Soc B284:20170641

    Article  CAS  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Clay K (2014) Defensive symbiosis: a microbial perspective. Funct Ecol 28:293–298

    Article  Google Scholar 

  • Clay K, Cheplick GP (1989) Effect of ergot alkaloids from fungal endophyte-infected grasses on the fall armyworm (Spodoptera frugiperda). J Chem Ecol 15:169–182

    Article  CAS  PubMed  Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    Article  PubMed  Google Scholar 

  • Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci U S A 102:12465–12470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701

    Article  CAS  Google Scholar 

  • Eich E (2008) Solanaceae and Convolvulaceae: secondary metabolites. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Elmi AA, West CP, Robbins RT, Kirkpatrick TL (2000) Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci 55:166–172

    Article  Google Scholar 

  • Escobar C, Barcala M, Cabrera J, Fenoll C (2015) Overview of root-knot nematodes and giant cells. Adv Bot Res 73:1–32

    Article  Google Scholar 

  • Eserman LA, Tiley GP, Jarret RL, Leebens-Mack JH, Miller RE (2014) Phylogenetics and diversification of morning glories (tribe Ipomoeeae, Convolvulaceae) based on whole plastome sequences. Am J Bot 101:92–103

    Article  PubMed  Google Scholar 

  • Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Annals NY Acad Sci 503:295–306

    Article  CAS  Google Scholar 

  • Florea S, Panaccione DG, Schardl CL (2017) Ergot alkaloids of the family Clavicipitaceae. Phytopathology 107:504–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franck G (1983) Companion planting: successful gardening the organic way. Thorsons Publishing, London

    Google Scholar 

  • Gardiner MR, Royce R, Oldroyd B (1965) Ipomoea muelleri intoxication of sheep in Western Australia. Brit Vet J 121:272–277

    Article  Google Scholar 

  • Grum DS, Cook D, Baucom D, Mott IW, Gardner DR, Creamer R, Allen JG (2013) Production of the alkaloid swainsonine by a fungal endophyte in the host Swainsona canescens. J Nat Prod 76:1984–1988

    Article  CAS  PubMed  Google Scholar 

  • Haine ER (2008) Symbiont-mediated protection. Proc Roy Soc B 275:353–361

    Article  Google Scholar 

  • Janzen DH (1985) The natural history of mutualisms. In: Boucher D (ed) The biology of mutualism: ecology and evolution. Oxford University Press, Oxford, pp 40–99

    Google Scholar 

  • Jia C, Ruan WB, Zhu MJ, Ren AZ, Gao YB (2013) Potential antagonism of cultivated and wild grass–endophyte associations towards Meloidogyne incognita. Biol Control 64:225–230

    Article  Google Scholar 

  • Karuri HW, Olago D, Neilson R, Mararo E, Villinger J (2017) A survey of root knot nematodes and resistance to Meloidogyne incognita in sweet potato varieties from Kenyan fields. Crop Prot 92:114–121

    Article  Google Scholar 

  • Kaur N, Cooper WR, Duringer JM, Badillo-Vargas IE, Esparza-Diaz G, Rashed A, Horton DR (2018) Survival and development of potato psyllid (Hemiptera: Triozidae) on Convolvulaceae: effects of a plant-fungus symbiosis (Periglandula). PLoS One 13:e0201506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kellner RL (2001) Suppression of pederin biosynthesis through antibiotic elimination of endosymbionts in Paederus sabaeus. J Insect Physiol 47:475–483

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick TL, Oosterhuis DM, Wullschleger SD (1991) Interaction of Meloidogyne incognita and water stress in two cotton cultivars. J Nematol 23:462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kucht S, Groß J, Hussein Y, Grothe T, Keller U, Basar S, König WA, Steiner U, Leistner E (2004) Elimination of ergoline alkaloids following treatment of Ipomoea asarifolia (Convolvulaceae) with fungicides. Planta 219:619–625

    Article  CAS  PubMed  Google Scholar 

  • Lee ST, Gardner DR, Cook D (2017) Identification of indole diterpenes in Ipomoea asarifolia and Ipomoea muelleri, plants tremorgenic to livestock. J Ag Food Chem 65:5266–5277

    Article  CAS  Google Scholar 

  • Leistner E, Steiner U (2018) The genus Periglandula and its symbiotum with morning glory plants (Convolvulaceae). In: Anke T, Schuffler A (eds) The Mycota XV. Springer, Berlin, pp 131–147

    Google Scholar 

  • Lopanik N, Lindquist N, Targett N (2004) Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 139:131–139

    Article  PubMed  Google Scholar 

  • Malinowski DP, Belesky DP, Fedders JM (1999) Endophyte infection may affect the competitive ability of tall fescue grown with red clover. J Agron Crop Sci 183:91–101

    Article  Google Scholar 

  • McBride RG, Mikkelsen RL, Barker KR (1999) A comparison of three methods for determining root-knot nematode infection of cotton roots. Nematropica 29:147–151

    Google Scholar 

  • Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, Stitt J, Shi Z, Zhang Y, Guiltinan MJ, Maximova SN (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 12:479

    Google Scholar 

  • Nowak J, Woźniakiewicz M, Klepacki P, Sowa A, Kościelniak P (2016) Identification and determination of ergot alkaloids in morning glory cultivars. Anal Bioanal Chem 408:3093–3102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyczepir AP, Meyer SL (2010) Host status of endophyte-infected and noninfected tall fescue grass to Meloidogyne spp. J Nematol 42:151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panaccione DG (2005) Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiol Lett 251:9–17

    Article  CAS  PubMed  Google Scholar 

  • Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB (2006) Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass. Nematology 8:583–590

    Article  CAS  Google Scholar 

  • Panaccione DG, Ryan KL, Schardl CL, Florea S (2012) Analysis and modification of ergot alkaloid profiles in fungi. Meth Enzymol 515:267–290

    Article  CAS  Google Scholar 

  • Panaccione DG, Beaulieu WT, Cook D (2014) Bioactive alkaloids in vertically transmitted fungal endophytes. Funct Ecol 28:299–314

    Article  Google Scholar 

  • Patchett B, Gooneratne R, Chapman B, Fletcher L (2011) Effects of loline-producing endophyte-infected meadow fescue ecotypes on New Zealand grass grub (Costelytra zealandica). NZ J Agric Res 54:303–313

    Article  CAS  Google Scholar 

  • Potter DA, Patterson CG, Redmond CT (1992) Influence of turfgrass species and tall fescue endophyte on feeding ecology of Japanese beetle and southern masked chafer grubs (Coleoptera: Scarabaeidae). J Econ Entomol 85:900–909

    Article  Google Scholar 

  • Ralmi NH, Khandaker MM, Mat N (2016) Occurrence and control of root knot nematode in crops: a review. Aust J Crop Sci 11:1649

    Article  Google Scholar 

  • Ryan KL, Moore CT, Panaccione DG (2013) Partial reconstruction of the ergot alkaloid pathway by heterologous gene expression in Aspergillus nidulans. Toxins 5:445–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND, Nagabhyru P (2013a) Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins 5:1064–1088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri K, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnon RD, Khan AK, Leistner E, Li C, Liu JG, Liu J, Liu M, Mace W, Machado C, Nagabhyru P, Pan J, Schmid J, Sugawara K, Steiner U, Takach JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z (2013b) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 28:e1003323

    Article  CAS  Google Scholar 

  • Schouten A (2016) Mechanisms involved in nematode control by endophytic fungi. Annu Rev Phytopathol 54:121–142

    Article  CAS  PubMed  Google Scholar 

  • Starr JL, Jeger MJ (1985) Dynamics of winter survival of eggs and juveniles of Meloidogyne incognita and M. arenaria. J Nematol 17:252

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steiner U, Leibner S, Schardl CL, Leuchtmann A, Leistner E (2011) Periglandula, a new fungal genus within the Clavicipitaceae and its association with Convolvulaceae. Mycologia 103:1133–1114

    Article  PubMed  Google Scholar 

  • Timper P, Gates RN, Bouton JH (2005) Response of Pratylenchus spp. in tall fescue infected with different strains of the fungal endophyte Neotyphodium coenophialum. Nematology 7:105–110

    Article  Google Scholar 

  • Tranier MS, Pognant-Gros J, Quiroz RD, González CN, Mateille T, Roussos S (2014) Commercial biological control agents targeted against plant-parasitic root-knot nematodes. Braz Arch Biol Tech 57:831–841

    Article  Google Scholar 

  • van der Putten WH, Van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53

    Article  Google Scholar 

  • Vandermeer JH (1989) The ecology of intercropping. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • West CP, Izekor E, Oosterhuis DM, Robbins RT (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112:3–6

    Article  Google Scholar 

  • Yeates GW (1999) Effects of plants on nematode community structure. Annu Rev Phytopathol 37:127–149

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Wheeler TA, Starr JL, Valencia CU, Sword GA (2018) A fungal endophyte defensive symbiosis affects plant-nematode interactions in cotton. Plant Soil 422:251–266

    Article  CAS  Google Scholar 

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Acknowledgements

Authors are grateful to Yuan-Zheng Zhao, Chuwen Li, Michael Frisby, Clay lab members, Indiana University (IU) Greenhouse staff, IU Light Microscopy Imaging Center, Dr. Erik Ragsdale and lab members (IU) and Dr. Antoon Ploeg (University of California-Riverside) for all contributions and technical support for the success of this research. L.D. was supported by a National Science Foundation Graduate Research Fellowship. D.G.P. was supported by National Institutes of Health grant 2R15GM114774-2 and Hatch funds. This research was financially supported in part by grant 429440 from the Simons Foundation to the Smithsonian Tropical Research Institute (W. Wcislo, P.I.).

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Durden, L., Wang, D., Panaccione, D. et al. Decreased Root-Knot Nematode Gall Formation in Roots of the Morning Glory Ipomoea tricolor Symbiotic with Ergot Alkaloid-Producing Fungal Periglandula Sp.. J Chem Ecol 45, 879–887 (2019). https://doi.org/10.1007/s10886-019-01109-w

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