Tree genotype and genetically based growth traits structure twig endophyte communities

American Journal of Botany

Volumn 101, Issue 3, 2014, Pages 467-478

  Lamit, Louis J ^a   Lau, Matthew K ^a   Sthultz, Christopher M ^b   Wooley, Stuart C ^c   Whitham, Thomas G ^a   Gehring, Catherine A ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Aboveground biomass; Co occurrence analysis; Condensed tannins; Endophyte; Populus angustifolia; Salicaceae; Tree genotype

Indexed keywords

COMMUNITY STRUCTURE; DIAMETER; ENDOPHYTE; FUNGUS; GENETIC ANALYSIS; GENETIC VARIATION; GENOTYPE; HYPOTHESIS TESTING; INTERSPECIFIC VARIATION; POLYMERASE CHAIN REACTION; TANNIN; TERRESTRIAL ECOSYSTEM; WOODY PLANT;

FUNGAL DNA; PROANTHOCYANIDIN;

ABOVEGROUND BIOMASS; ARTICLE; BIOMASS; CHEMISTRY; CO-OCCURRENCE ANALYSIS; CONDENSED TANNINS; DNA SEQUENCE; ENDOPHYTE; FUNGUS; GENETIC VARIABILITY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY; PLANT; POLYMERASE CHAIN REACTION; POPULUS; POPULUS ANGUSTIFOLIA; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SALICACEAE; SPECIES DIFFERENCE; SYMBIOSIS; TREE; TREE GENOTYPE;

ABOVEGROUND BIOMASS; CO-OCCURRENCE ANALYSIS; CONDENSED TANNINS; ENDOPHYTE; POPULUS ANGUSTIFOLIA; SALICACEAE; TREE GENOTYPE;

BASE SEQUENCE; BIOMASS; DNA, FUNGAL; ENDOPHYTES; FUNGI; GENETIC VARIATION; GENOTYPE; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT SHOOTS; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; POPULUS; PROANTHOCYANIDINS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS; TREES;

EID: 84897881627     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1400034     Document Type: Article

References (61)

1. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
2. Anderson, M. J., R. N. Gorley and K. R. Clarke. 2008. PERMANOVA+for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth, UK.
3. Arnold, A. E. 2007. Understanding the diversity of foliar endophytic fungi: Progress, challenges, and frontiers. Fungal Biology Reviews 21: 51 - 66.
4. Arnold, A. E., and E. A. Herre. 2003. Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95: 388-398.
5. Arnold, A. E., Z. Maynard and G. S. Gilbert. 2001. Fungal endophytes in dicotyledonous neotropical trees: Patterns of abundance and diversity. Mycological Research 105: 1502-1507.
6. Arnold, A. E., L. C. Mejia, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins and E. A. Herre. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
7. Arnold, A. E., J. Miadlikowska, K. L. Higgins, S. D. Sarvate, P. Gugger, A. Way, V. Hofstetter et al. 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: Are lichens cradles of symbiotrophic fungal diversification? Systematic Biology 58: 283-297.
8. Bailey J., K. R. Deckert, J. A. Schweitzer, B. J. Rehill, R. L. Lindroth, C. A. Gehring and T. G. W hitham. 2005. Host plant genetics affect hidden ecological players: Links among Populus, condensed tannins, and fungal endophyte infection. Canadian Journal of Botany 83: 356-361.
9. Blackwell, M. 2011. The fungi: 1, 2, 3.5.1 million species? American Journal of Botany 98: 426-438.
10. Carroll, G. 1988. Fungal endophytes in stems and leaves-From latent pathogen to mutualistic symbiont. Ecology 69: 2-9.
11. Carroll, G. C., and F. E. Carroll. 1978. Studies on the incidence of coniferous needle endophytes in the Pacifi c Northwest. Canadian Journal of Botany 56: 3034-3043.
12. Chapela, I. H. 1989. Fungi in healthy stems and branches of American beech and aspen-a comparative study. New Phytologist 113: 65-75.
13. Collado J., G. Platas, I. Gonzalez and F. Pelaez. 1999. Geographical and seasonal infl uences on the distribution of fungal endophytes in Quercus ilex. New Phytologist 144: 525-532.
14. Conner, J. K., and D. L. Hartl. 2004. A primer of ecological genetics. Sinauer, Sunderland, Massachusetts, USA.
15. hristensen, C. M. 1940. Studies on the biology of Valsa sordida and Cytospora chrysosperma. Phytopathology 30: 459-475.
16. Crainiceanu C., and D. Ruppert. 2004. Likelihood ratio tests in linear mixed models with one variance component. Journal of the Royal Statistical Society. Series B. Methodological 66: 165-185.
17. de Gruyter J., and P. Scheer. 1998. Taxonomy and pathogenicity of Phoma exigua var. populi var. nov. causing necrotic bark lesions on poplars. Journal of Phytopathology 146: 411-415.
18. de Souza Sebastianes, F. L., A. S. Romao-Dumaresq, P. T. Lacava, R. H arakava, J. L. Azevedo, I. S. de Melo and A. A. Pizzirani-Kleiner 2013. Species diversity of culturable endophytic fungi from Brazilian mangrove forests. Current Genetics 59: 153-166.
19. Desprez-Loustau, M., L. B. Marcais, L.M. Nageleisen, D. Piou and A. Vannini. 2006. Interactive effects of drought and pathogens in forest trees. Annals of Forest Science 63: 597-612.
20. Elamo, P., M. L. Helander, I. Saloniemi and S. Neuvonen. 1999. Birch family and environmental conditions affect endophytic fungi in leaves. Oecologia 118: 151-156.
21. Faeth, S. H., and K. E. Hammon. 1996. Fungal endophytes and phy-tochemistry of oak foliage: Determinants of oviposition preference of leafminers? Oecologia 108: 728-736.
22. Fischer, D. G., S. C. Hart, B. J. Rehill, R. L. Lindroth, P. Keim and T. G. Whitham. 2006. Do high-tannin leaves require more roots? Oecologia 149: 668-675.
23. Fukami T., I.A. Dickie, J. P. Wilkie, B. C. Paulu, D. Park, A. Roberts, P. K. Buchanan and R. B. Allen. 2010. Assembly history dictates ecosystem functioning: Evidence from wood decomposer communities. Ecology Letters 13: 675-684.
24. Gange, A. C., S. Dey, A. F. Currie and B. C. Sutton. 2007. Site- and species-specifi c differences in endophyte occurrence in two herbaceous plants. Journal of Ecology 95: 614-622.
25. Gardes M and T. D. Bruns. 1993. ITS primers with enhanced specifi city for basidiomycetes-Application to the identifi cation of mycor-rhizae and rusts. Molecular Ecology 2: 113-118.
26. Gotelli, N. J. 2000. Null model analysis of species co-occurrence patterns. Ecology 81: 2606-2621.
27. Gutmann M and W. F. eucht. 1991. A new method for selective localization of flavan-3-ols in plant tissues involving glycolmethacrylate embedding and microwave irradiation. Histochemistry 96: 83-86.
28. Hagerman, A. E., and L. G. Butler. 1994. Assay of condensed tannins or flavonoid oligomers and related flavonoids in plants. Oxygen Radicals in Biological Systems 234: 429-437.
29. Hall, T. A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
30. Hoeksema, J. D., V. B. Chaudhary, C. A. Gehring, N. C. Johnson, J. Karst, R. T. Koide, A. Pringle, et al. 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13: 394-407.
31. Holeski, L. M., A. Vogelzang, G. Stanosz and R. L. Lindroth. 2009. Incidence of Venturia shoot blight in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochemical Systematics and Ecology 37: 139-145.
32. H orner-Devine, M. C., J. M. Silver, M. A. Leibold, B. J. M. Bohannan, R. K. Colwell, J. A. Fuhrman, J. I. Green et al. 2007. A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88: 1345-1353.
33. Huang Y., B. Niu, Y. Gao, L. Fu and W. Li. 2010. CD-HIT Suite: A web server for clustering and comparing biological sequences. Bioinformatics (Oxford, England) 26: 680-682.
34. Hutchison, L. J. 1999. Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Canadian Journal of Botany 77: 898-905.
35. Koide, R. T., B. Xu, J. Sharda, Y. Lekberg and N. Ostiguy. 2005. Evidence of species interactions within an ectomycorrhizal fungal community. New Phytologist 165: 305-316.
36. Korkama-Rajala, T., M. M. Mueller, and T. Pennanen. 2008. Decomposition and fungi of needle litter from slow- and fast-growing Norway spruce (Picea abies) clones. Microbial Ecology 56: 76-89.
37. K raus, T. E. C., R. A. Dahlgren and R. J. Zasoski. 2003. Tannins in nutrient dynamics of forest ecosystems-a review. Plant and Soil 256: 41-66.
38. Lamit, L. J.,T. Wojtowicz, Z. K ovacs, S. C. Wooley, M. Zinkgraf, T. G. Whitham, R. L. Lindroth and C. A. Gehring. 2011. Hybridization among foundation tree species infl uences the structure of associated understory plant communities. Botany 89: 165-174.
39. Lojewski, N. R., D. G. Fischer, J. K. Bailey, J. A. Schweitzer, T. G. W hitham and S. C. Hart. 2009. Genetic basis of aboveground productivity in two native Populus species and their hybrids. Tree Physiology 29: 1133-1142.
40. Martinsen, G. D.,T. G. Whitham, R. J. Turek and P. Keim. 2001. Hybrid populations selectively fi lter gene introgression between species. Evolution 55: 1325-1335.
41. McCune B and J. B. Grace. 2002. Analysis of ecological communities. MjM Software Design, Gleneden Beach, Oregon, USA.
42. Miglia, K. J., E. D. McArthur, R. S. Redman, R. J. Rodriguez, J. C. Zak and D. C. Freeman. 2007. Genotype, soil type, and locale effects on reciprocal transplant vigor, endophyte growth, and microbial functional diversity of a narrow sagebrush hybrid zone in Salt Creek, Canyon, Utah. American Journal of Botany 94: 425-436.
43. Pan, J. J., A. M. Baumgarten and G. May. 2008. Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays). New Phytologist 178: 147-156.
44. Pan J. J., and G. M ay. 2009. Fungal-fungal associations affect the assembly of endophyte communities in maize (Zea mays). Microbial Ecology 58: 668-678.
45. Porter, L. J., L. N. Hrstich and B. G. Chan. 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25: 223-230.
46. Price P. W. 1991. The plant vigor hypothesis and herbivore attack. Oikos 62: 244-261.
47. Rodriguez, R. J., J. F. White J r, A. E. Arnold and R. S. Redman. 2009. Fungal endophytes: Diversity and functional roles. New Phytologist 182: 314-330.
48. Sahashi N., T. Kubono, Y. Miyasawa and S Ito. 1999. Temporal variations in isolation frequency of endophytic fungi of Japanese beech. Canadian Journal of Botany 77: 197-202.
49. Santamaria, O., and J. J. Diez. 2005. Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. Forest Pathology 35: 95-104.
50. Saunders, M., and L. M. Kohn. 2009. Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytologist 182: 229-238.
51. Shaw, R. G. 1987. Maximum-likelihood approaches applied to quantitative genetics of natural populations. Evolution 41: 812-826.
52. Sieber, T. N., F. Sieber-Canavesi and C. E. Dorworth. 1991. Endophytic fungi of red alder (Alnus rubra) leaves and twigs in British Columbia. Canadian Journal of Botany 69: 407-411.
53. Stone, A. C., C. A. Gehring and T G Whitham. 2010. Drought negatively affects communities on a foundation tree: growth rings predict diversity. Oecologia 164: 751-761.
54. Stone L and A Roberts. 1990. The checkerboard score and species distributions. Oecologia 85: 74-79.
55. Swaty, R. L., R. J. Deckert, T.G. Whitham and C. A. Gehring. 2004. Ectomycorrhizal abundance and community composition shifts with drought: Predictions from tree rings. Ecology 85: 1072-1084.
56. Todd, D. 1988. The effects of host genotype, growth-rate and needle age on the distribution of mutualistic, endophytic fungus in Douglas fir plantations. Canadian Journal of Forest Research 18: 601-605.
57. U'Ren J. M., J. W. Dalling, R. E. Gallery, D. R. Maddison, E. C. Davis, C. M. Gibson and A. E. Arnold. 2009. Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: A case study for analyzing fungal environmental samples. Mycological Research 113: 432-449.
58. U'Ren J., M. F. Lutzoni, J. Miadlikowska, A. Laetsch and A. E. Arnold. 2012. Host and geographic structure of endophytic and en-dolichenic fungi at a continental scale. American Journal of Botany 99: 898-914.
59. White, T. J., T. Bruns, S. Lee and J. W. Taylor. 1990. Amplifi cation and direct sequencing of fungal ribosomal RNA genes for phyloge-netics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: A guide to methods and applications, 315-322. Academic Press, San Diego, California, USA.
60. Whitham, T. G., C. A. Gehring, L. J. Lamit, T. W ojtowicz, L. M. Evans, A. R. Keith and D. S. Smith. 2012. Community specifi city: Life and afterlife effects of genes. Trends in Plant Science 1 7: 271-281.
61. Zimmerman, N. B., and P. M. Vitousek. 2012. Fungal endophyte communities refl ect environmental structuring across a Hawaiian landscape. Proceedings of the National Academy of Sciences, USA 109: 13022-13027.