Choristoneura fumiferana is the most economically-important insect pest in eastern North America. Historically, strategies to control epidemics have relied on chemical pesticides that are no longer approved for use. The presence of fungal endophytes in cool area grass species and their role in reducing the impact of herbivorous insects is well understood. Recent work has demonstrated that foliar endophytes of conifers also produce anti-insect toxins. Field and nursery studies testing trees infected with the rugulosin producing endophyte Phialocephala scopiformis reduced the growth and development of C. fumiferana. The study of foliar endophytes from a variety of conifers including: Picea mariana, P. rubens and P. glauca as well as Abies balsamea and Larix laricina for the discovery of other anti-insect toxins are discussed. These endophytes are horizontally transmitted thus they are not present in nursery seedlings. Inoculating seedlings with toxigenic endophyte strains has been demonstrated to be effective in providing the tree with tolerance to herbivorous insects.
PirozynskiKA, MallochDW. (1975) The origin of land plants: a matter of mycotrophism. Bio Systems, 3, 153–164.
2.
PirozynskiKA. (1981) Interactions between fungi and plants through the ages. Canadian Jounal of Botany, 59, 1824–1827.
3.
MillerJD. (1986) Toxins of endophytic and epiphytic fungi of conifer needles. In: FokkemaNJ, Van HuevelJ (eds) Microbiology of the phyllosphere. Cambridge University Press, UK, 223–23l.
4.
WinkM. (2008) Plant secondary metabolism: diversity, function and its evolution. Natural Product Communications, 3, 1205–1216.
5.
Bu'LockJD. (1975) Secondary metabolism. In: The Filamentous Fungi (SmithJE, BerryDR, eds). New York: Academic Press, 33–58.
6.
IwaiY, OmuraS. (1982) Culture conditions for screening of new antibiotics. The Journal of Antibiotics, XXXV, 123–141.
7.
DemainA, VaishnavP. (2006) Involvement of nitrogen-containing compounds in β-lactam biosynthesis and its control. Critical Reviews in Biotechnology, 26, 67–82.
8.
MillerJD, BlackwellBA. (1986) Biosynthesis of 3-acetyldeoxynivalenol and other metabolites by Fusarium culmorum HLX 1503 in a stirred jar fermentor. Canadian Journal of Botany, 64, 1–5.
9.
MillerJD, SavardME, RapiorS. (1994) Production and purification of fumonisins from a stirred jar fermentor. Natural Toxins, 2, 354–359.
10.
MillerJD. (2001) Factors that affect the occurrence of fumonisin. Environ Health Perspective, 109, 321–324.
11.
MillerJD, GreenhalghR. (1988) Metabolites of fungal pathogens and plant resistance. ACS Symposium Series 379 (Biotechnology and Crop Protection), 117–29.
12.
MacLeanDA, BeatonKP, PorterKB, MacKinnonWB, BuddMG. (2002) Potential wood supply losses to spruce budworm in New Brunswick estimated using the spruce budworm decision support system. Forestry Chronicle, 78, 739–750.
13.
RoyamaT, MacKinnonWE, KettelaEG, CarterNE, HartlingLK. (2005) Analysis of spruce budworm outbreak cycles in New Brunswick, Canada, since 1952. Ecology, 86, 1212–1224.
14.
IrlandLC. (1980) Pulpwood, pesticides, and people. Controlling spruce budworm in northeastern North America. Environmental Management, 4, 381–389.
15.
CarrollGC, CarrollFE. (1978) Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Canadian Journal of Botany, 56, 3034–3043.
16.
ClayK, SchardlC. (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. The American Naturalist, 160 Suppl 4, S99–S127.
17.
Sherwood-PikeM, StoneJK, CarrollGC. (1986) Rhabdocline parkeri, a ubiquitous foliar endophyte of Douglas fir. Canadian Journal of Botany, 64, 1849–1855.
18.
ToddD. (1988) The effects of host genotype, growth rate, and needle age on the distribution of a mutalistic, endophytic fungus in Douglas fir plantations. Canadian Journal of Forestry Research, 18, 601–605.
19.
CarrollGC. (1986) The biology of endophytism in plants with particular reference to woody perennials. In Microbiology of the phyllosphere. Edited by FokkemaN.Cambridge University Press, London, 205–222.
20.
RoyamaT. (1984) Population dynamics of the spruce budworm. Ecology Monographs, 54, 429–462.
21.
MillerJD, StrongmanD, WhitneyNJ. (1985) Observations on fungi associated with spruce budworm infested balsam fir needles. Canadian Journal of Forest Research, 15, 896–901.
22.
JohnsonJA, WhitneyNJ. (1989) A study of fungal endophytes of needles of balsam fir (Abies balsamea) and red spruce (Piceae rubens) in New Brunswick, Canada, using cultural and electron microscope techniques. Canadian Journal of Botany, 67, 3513–3516.
23.
JohnsonJA, WhitneyNJ. (1992) Isolation of fungal endophytes from black spruce (Picea mariana) dormant buds and needles from New Brunswick, Canada. Canadian Journal of Botany, 70, 1754–1757.
24.
MillerJD, MackenzieS, FotoM, AdamsGW, FindlayJA. (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycological Research, 106, 471–479.
25.
WilsonR, WheatcroftR, MillerJD, WhitneyNJ. (1994) Genetic diversity among natural populations of endophytic Lophodermium pinastri from Pinus resinosa. Mycological Research, 98, 740–744.
26.
MillerJD, CheridH, SumarahMW, AdamsGW. (2009) Horizontal transmission of the Picea glauca foliar endophyte Phialocephala scopiformis CBS 120377. Fungal Ecology, 2, 98–101.
27.
SumarahMW, AdamsGW, BerghoutJ, SlackG, WilsonA, MillerJD. (2008) Spread and persistence of a rugulosin-producing endophyte in white spruce seedlings. Mycological Research, 112, 731–736.
28.
CalhounLA, FindlayJA, MillerJD, WhitneyNJ. (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycological Research, 96, 281–286.
29.
MillerJD, SumarahMW, AdamsGW. (2008) Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. Journal of Chemical Ecology, 34, 362–368.
30.
FindlayJA, LiG, PennerPE, MillerJD. (1995) Novel diterpenoid insect toxins from a conifer endophyte. Journal of Natural Products, 58, 197–200.
31.
FindlayJA, ButheleziS, LavoieR, Pern-RodriguezL, MillerJD. (1995) Bioactive isocoumarins and related metabolites from conifer endophytes. Journal of Natural Products, 58, 1759–1766.
32.
CrousPW, SummerellBA, CarnegieAJ, MohammedC, HimamanW, GroenewaldJZ. (2007) Foliicolous Mycosphaerella spp. and their anamorphs on Corymbia and Eucalyptus. Fungal Divers, 26, 143–185.
33.
FindlayJA, LiG, JohnsonJA. (1997) Bioactive compounds from an endophytic fungus from eastern larch (Larix laricina) needles. Canadian Journal of Chemistry, 75, 716–719.
34.
FindlayJA. (1996) Natural insect toxins from endophytic fungi. Revista Latinoamericana de Quimica, 24, 214–222.
35.
FindlayJA, LiG, MillerJD, WomiloujuTO. (2003) Insect toxins from spruce endophytes. Canadian Journal of Chemistry, 81, 284–292.
36.
HorakovaK, KernacovaB, NemecP, FuskaJ. (1976) Characterization of the cytotoxic activity of vermiculine. Journal of Antibiotics, 29, 1109–1111.
37.
KoshinoH, TeradaSI, YoshiharaT, SakamuraS, ShimanukiT, SatoT, TajimiA. (1988) Three phenolic acid derivatives from stromata of Epichloë typhina on Phleum pretense. Phytochemisry, 27, 1333–1338.
38.
MaoS, LeeSJ, HwangboH, KimYW, ParkKH, ChaGS, ParkRD, KimKY. (2006) Isolation and characterization of antifungal substances from Burkholderia sp. culture broth. Current Microbiology, 53, 358–364.
39.
MiyazawaM, AnzaiJ, FujiokaJ, IsikawaY. (2003) Insecticidal compounds against Drosophila melanogaster from Cornus officinalis Sieb. Et Zucc. Natural Product Research, 17, 337–339.
40.
SumarahMW, PunianiE, BlackwellBA, MillerJD. (2008) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. Journal of Natural Products, 71, 1393–1398.
41.
BrewerD, ArsenaultGP, WrightJLC, ViningLC. (1973) Production of bikaverin by Fusarium oxysporum and its identity with lycopersin. Journal of Antibiotics, 26, 778–781.
42.
GiordanoW, AvalosJ, Cerda-OlmedoE, DomenechCE. (1999) Nitrogen availability and production of bikaverin and gibberellins in Gibberella fujikuroi. FEMS Microbiology Letters, 173, 389–393.
43.
HidyPH, BaldwinRS, GreashamRL, KeithCL, McMullenJR. (1977) Zearalenone and some derivatives: production and biological activities. Advanced and Applied Microbiology, 22, 59–82.
44.
MillerJD, YoungJC, TrenholmHL. (1983) Fusarium toxins in field corn. I: time course of fungal growth and production of deoxynivalenol and other mycotoxins. Canadian Journal of Botany, 61, 3080–3087.
45.
RokemJS, LantzAE, NielsenJ. (2007) Systems biology of antibiotic production by microorganisms. Natural Product Reports, 24, 1262–1287.
46.
WiemannP, WillmannA, StraetenM, KleigreweK, BeyerM, HumpfHU, TudzynskiB. (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Molecular Microbiology, 72, 931–946.
47.
BrownDW, DyerRB, McCormickSP, KendraDF, PlattnerRD. (2004). Functional demarcation of the fusarium core trichothecene gene cluster. Fungal Genetics and Biology, 41, 454–462.
48.
TeichertS, WottawaM, SchönigB, TudzynskiB. (2006) Role of the Fusarium fujikuroi TOR kinase in nitrogen regulation and secondary metabolism. Eukaryotic cell, 5, 1807–1819.
49.
TudzynskiB. (2005) Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology. Applied Microbiology and Biotechnology, 66, 597–611.
50.
CastilloIN, FierroF, GutiérrezS, MartínJF. (2006) Genome-wide analysis of differentially expressed genes from Penicillium chrysogenum grown with a repressing or a non-repressing carbon source. Current Genetics, 49, 85–96.
51.
KosalkováK, Rodríguez-SáizM, BarredoJL, MartínJL. (2007) Binding of the PTA1 transcriptional activator to the divergent promoter region of the Wrst two genes of the penicillin pathway in different Penicillium species. Current Genetics, 52, 229–237.
52.
LirasP, MartínJF. (2006) Gene clusters for β-lactam antibiotics and control of their expression: why have clusters evolved, and from where did they originate?International Microbiology, 9, 9–19.
53.
MartínJF. (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. Journal of Bacteriology, 186, 5197–5201.
54.
GaffoorI, TrailF. (2006) Characterization of two polyketide synthase genes involved in zearalenone biosynthesis in Gibberella zeae. Applied and Environmental Microbiology, 72, 1793–1799.
55.
GaryHL. (1971) Seasonal and diurnal changes in moisture contents and water deficits of Engelmann spruce needles. Botanical Gazette, 132, 327–332.
56.
ReinaJJ, DomingguezE, HerediaA. (2001) Water sorption–desorption in conifer cuticles: The role of lignin. Physiologia Plantarum, 112, 372–378.
57.
ZwiazekJJ. (1991) Cell wall changes in white spruce (Picea glauca) needles subjected to repeated drought stress. Physiologia Plantarum, 82, 513–518.
58.
SumarahMW, MillerJD, AdamsGW. (2005) Measurement of a rugulosin-producing endophyte in white spruce seedlings. Mycologia, 97, 770–776.
