Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity

New Phytologist

Volumn 209, Issue 4, 2016, Pages 1681-1692

  Busby, Posy E ^a,b   Peay, Kabir G ^c   Newcombe, George ^b  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Cladosporium; Epicoccum; Trichoderma; Alternaria; Endophyte; Genetic resistance; Phyllosphere; Plant defense

Indexed keywords

ABUNDANCE; DECIDUOUS TREE; DISEASE RESISTANCE; DISEASE SEVERITY; ENDOPHYTE; EPIPHYTE; EXPERIMENTAL STUDY; FOLIAGE; MOLECULAR ANALYSIS; NATIVE SPECIES; PLANT DEFENSE; RUST DISEASE; SPATIAL DISTRIBUTION; TAXONOMY; WILD POPULATION;

PACIFIC NORTHWEST;

ALTERNARIA; CLADOSPORIUM; EPICOCCUM; FUNGI; MELAMPSORA; POPULUS TRICHOCARPA; TRICHODERMA;

BASIDIOMYCETES; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; POPULUS; STATISTICAL MODEL; TREE;

BASIDIOMYCOTA; LIKELIHOOD FUNCTIONS; LINEAR MODELS; PLANT DISEASES; PLANT LEAVES; POPULUS; TREES;

EID: 84969406047     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13742     Document Type: Article

References (62)

1. Adame-Álvarez R-M, Mendiola-Soto J, Heil M. 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiology Letters 355: 100-107.
2. Adams RI, Miletto M, Taylor JW, Bruns TD. 2013. Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. The ISME Journal 7: 1262-1273.
3. Agrios G. 2005. Plant pathology. San Diego, CA, USA: Elsevier Academic Press.
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
5. Arnold A, Mejia L, Kyllo D, Rojas E, Maynard Z, Robbins N, Herre E. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
6. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA. 2002. Are tropical fungal endophytes hyperdiverse? Ecology Letters 3: 267-274.
7. Bronstein J. 2009. The evolution of facilitation and mutualism. Journal of Ecology 97: 1160-1170.
8. Busby PE, Zimmerman N, Weston DJ, Jawdy SS, Houbraken J, Newcombe G. 2013. Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen, Drepanopeziza populi. Ecosphere 4: 125.
9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
10. Clay K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69: 10-16.
11. Clay K. 2014. Defensive symbiosis: a microbial perspective (C. Fox, ed.). Functional Ecology 28: 293-298.
12. Davidson DW, McKey D. 1993. Evolutionary ecology of symbiotic ant-plant relationships. Journal of Hymenoptera Research 2: 13-83.
13. Dunlap J, Stettler R. 1996. Genetic variation and productivity of Populus trichocarpa and its hybrids. IX. Phenology and Melampsora rust incidence of native black cottonwood clones from four river valleys in Washington. Forest Ecology and Management 87: 233-256.
14. Dunlap J, Stettler R. 2001. Variation in leaf epidermal and stomatal traits of Populus trichocarpa from two transects across the Washington Cascades. Canadian Journal of Botany 79: 528-536.
15. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10: 996-998.
16. Ellis B. 1972. Dematiaceous hyphomycetes. State College, PA, USA: Commonwealth Mycological Institute.
17. Funk A, Centre PFR. 1985. Foliar fungi of western trees. Victoria, BC, USA: Pacific Forest Research Centre.
18. Ganley R, Newcombe G. 2006. Fungal endophytes in seeds and needles of Pinus monticola. Mycological Research 110: 318-327.
19. Ganley R, Sniezko R, Newcombe G. 2008. Endophyte-mediated resistance against white pine blister rust in Pinus monticola. Forest Ecology and Management 255: 2751-2760.
20. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for Basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
21. Goffe WL, Ferrier GD, Rogers J. 1994. Global optimization of statistical functions with simulated annealing. Journal of Econometrics 60: 65-99.
22. Jones N. 2013. Food fuelled with fungi. Nature 504: 199.
23. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
24. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22: 5271-5277.
25. Kurose D, Furuya N, Tsuchiya K, Tsushima S. 2012. Endophytic fungi associated with Fallopia japonica (Polygonaceae) in Japan and their interactions with Puccinia polygoni-amphibii var. tovariae, a candidate for classical biological control. Fungal Biology 116: 785-791.
26. Larkin RP, Fravel DR. 1998. Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Disease 82: 1022-1028.
27. Ledford H. 2015. Plant dwellers take the limelight. Nature 523: 137-138.
28. Lee K, Pan JJ, May G. 2009. Endophytic Fusarium verticillioides reduces disease severity caused by Ustilago maydis on maize. FEMS Microbiology Letters 299: 31-37.
29. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B. 2012. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research 40: W622-W627.
30. Martin JA, Macaya-Sanz D, Witzell J, Blumenstein K, Gil L. 2015. Strong in vitro antagonism by elm xylem endophytes in not accompanied by temporally stable in planta protection against a vascular pathogen under field conditions. European Journal of Plant Pathology 142: 185-196.
31. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17: 10-12.
32. McNew GL. 1960. The nature, origin, and evolution of parasitism. Plant Pathology: An Advanced Treatise 2: 19-69.
33. Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, Stitt J, Shi Z, Zhang Y, Guiltinan MJ et al. 2014. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology 5: 479.
34. Morin L, Auld BA, Brown JF. 1993. Interaction between Puccinia xanthii and facultative parasitic fungi on Xanthium occidentale. Biological Control 3: 288-295.
35. Müller MM, Valjakka R, Suokko A, Hantula J. 2001. Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Molecular Ecology 10: 1801-1810.
36. 2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4: 133-142.
37. Newcombe G. 1996. The specificity of fungal pathogens of Populus. Stettler R, Bradshaw H, Heilman P, Hinckley T, eds. Biology of Populus. Ottawa, ON, Canada: NRC Research Press, 223-246.
38. Newcombe G. 1998. Association of Mmd1, a major gene for resistance to Melampsora medusae f. sp. deltoidae, with quantitative traits in poplar rust. Phytopathology 88: 114-121.
39. Newcombe G, Stirling B, Bradshaw HD. 2001. Abundant pathogenic variation in the new hybrid rust Melampsora × columbiana on hybrid poplar. Phytopathology 91: 981-985.
40. R Core Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL http://www.R-project.org/ [accessed December 2013].
41. Raghavendra AKH, Newcombe G. 2013. The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytologist 197: 909-918.
42. Ridout M, Newcombe G. 2015. The frequency of modification of Dothistroma pine needle blight severity by fungi within the native range. Forest Ecology and Management 337: 153-160.
43. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS. 2008. Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal 2: 404-416.
44. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182: 314-330.
45. Rubin EM. 2008. Genomics of cellulosic biofuels. Nature 454: 841-845.
46. Saunders M, Kohn LM. 2008. Host-synthesized secondary compounds influence the in vitro interactions between fungal endophytes of maize. Applied and Environmental Microbiology 74: 136-142.
47. Saville DJ. 1990. Multiple comparison procedures - the practical solution. American Statistician 44: 174-180.
48. Schulz B, Rommert A-K, Dammann U, Aust H-J, Strack D. 1999. The endophyte-host interaction: a balanced antagonism? Mycological Research 103: 1275-1283.
49. Schulz B, Wanke U, Draeger S, Aust H-J. 1993. Endophytes from herbaceous plants and schrubs: effectiveness of surface sterilization methods. Mycological Research 12: 1447-1450.
50. Sharma IK, Heather WA. 1983. Sensitivity to Cladosporium species of the reactions of cultivars of Populus × euramericana to races of Melampsora larici-populina. Forest Ecology and Management 7: 49-56.
51. Smith DP, Peay KG. 2014. Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS ONE 9: e90234.
52. Stokstad E. 2007. Deadly wheat fungus threatens world's breadbaskets. Science 315: 1786-1787.
53. Stone J, Bacon C, White J. 2000. An overview of endopytic microbes: endophytism defined. Bacon C, White J, eds. Microbial endophytes. New York, NY, USA: Marcel Dekker, 3-29.
54. Thrall PH, Hochberg ME, Burdon JJ, Bever JD. 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology and Evolution 22: 120-126.
55. U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE. 2012. Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99: 898-914.
56. US Geological Survey. 1999. Digital representation of "Atlas of United States Trees" by Elbert L. Little, Jr. US Geological Survey Professional Paper 1650.
57. Vázquez de Aldana BR, Bills G, Zabalgogeazcoa I. 2013. Are endophytes an important link between airborne spores and allergen exposure? Fungal Diversity 60: 33-42.
58. Vorholt JA. 2012. Microbial life in the phyllosphere. Nature Reviews Microbiology 10: 828-840.
59. Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T. 2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecology Letters 17: 717-726.
60. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego, CA, USA: Academic Press, 315-322.
61. Woo SL, Scala F, Ruocco M, Lorito M. 2006. The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96: 181-185.
62. Zimmerman NB, Vitousek PM. 2012. Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proceedings of the National Academy of Sciences, USA 109: 13022-13027.