Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree

Frontiers in Microbiology

Volumn 5, Issue SEP, 2014, Pages

  Mejía, Luis C ^a,b,f   Herre, Edward A ^a   Sparks, Jed P ^c   Winter, Klaus ^a   García, Milton N ^a   Van Bael, Sunshine A ^a,d   Stitt, Joseph ^e   Shi, Zi ^b   Zhang, Yufan ^b   Guiltinan, Mark J ^b   Maximova, Siela N ^b  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c Cornell University ^*  (United States)

^d Tulane University   (United States)

^e Social Life and Engineering Sciences Imaging Center Materials Research Institute University Park   (United States)

^f INSTITUTO DE INVESTIGACIONES CIENTÍFICAS Y SERVICIOS DE ALTA TECNOLOGÍA   (Panama)

Author keywords

Arabidopsis; Colletotrichum; Fungal endophytes; Gene expression; Plant defense; Populus; Symbiosis; Theobroma

Indexed keywords

CARBON; NITROGEN; TUBULIN;

ARTICLE; CACAO; CACAO GENE; CONFOCAL MICROSCOPY; DOWN REGULATION; ENDOPHYTIC FUNGUS; FUNGAL COLONIZATION; FUNGAL METABOLISM; FUNGUS GROWTH; GENE; GENE EXPRESSION; GENOTYPE PHENOTYPE CORRELATION; HOST RESISTANCE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; NITROGEN METABOLISM; NONHUMAN; PHOTOSYNTHESIS; PHYLOGENY; PLANT FUNGUS INTERACTION; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; UPREGULATION;

ARABIDOPSIS; COLLETOTRICHUM; FUNGI; POPULUS; THEOBROMA;

EID: 84907997853     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00479     Document Type: Article

References (69)

1. Adame-Álvarez, R.-M., Mendiola-Soto, J., and Heil, M. (2014). Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol. Lett. 355, 100-107. doi: 10.1111/1574-6968.12454
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
3. Argout, X., Fouet, O., Wincker, P., Gramacho, K., Legavre, T., Sabau, X., et al. (2008). Towards the understanding of the cocoa transcriptome: production and analysis of an exhaustive dataset of ESTs of Theobroma cacao L. generated from various tissues and under various conditions. BMC Genomics 9:512. doi: 10.1186/1471-2164-9-512
4. Argout, X., Salse, J., Aury, J.-M., Guiltinan, M. J., Droc, G., Gouzy, J., et al. (2011). The genome of Theobroma cacao. Nat. Genet. 43, 101-108. doi: 10.1038/ng.736
5. Arnold, A. E., Mejia, L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N., et al. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. U.S.A. 100, 15649-15654. doi: 10.1073/pnas.2533483100
6. Bae, H., Sicher, R. C., Kim, M. S., Kim, S. H., Strem, M. D., Melnick, R. L., et al. (2009). The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 60, 3279-3295. doi: 10.1093/jxb/erp165
7. Bailey, B. A., Bae, H., Strem, M. D., Roberts, D. P., Thomas, S. E., Crozier, J., et al. (2006). Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224, 1449-1464. doi: 10.1007/s00425-006-0314-0
8. Berardini, T. Z., Mundodi, S., Reiser, L., Huala, E., Garcia-Hernandez, M., Zhang, P., et al. (2004). Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 135, 745-755. doi: 10.1104/pp.104.040071
9. Bradley, D. J., Kjellbom, P., and Lamb, C. J. (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70, 21-30. doi: 10.1016/0092-8674(92)90530-P
10. Bustin, S. A. (2004). A-Z of Quantitative PCR. San Diego, CA: International University Line.
11. Camehl, I., Sherameti, I., Venus, Y., Bethke, G., Varma, A., Lee, J., et al. (2010). Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol. 185, 1062-1073. doi: 10.1111/j.1469-8137.2009.03149.x
12. Campanile, G., Ruscelli, A., and Luisi, N. (2007). Antagonistic activity of endophytic fungi towards Diplodia corticola assessed by in vitro and in planta tests. Eur. J. Plant Pathol. 117, 237-246. doi: 10.1007/s10658-006-9089-1
13. Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr. 53, 209-234. doi: 10.2307/1942495
14. Craine, J. M., Elmore, A. J., Aidar, M. P., Bustamante, M., Dawson, T. E., Hobbie, E. A., et al. (2009). Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980-992. doi: 10.1111/j.1469-8137.2009.02917.x
15. Crozier, J., Thomas, S. E., Aime, M. C., Evans, H. C., and Holmes, K. A. (2006). Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathol. 55, 783-791. doi: 10.1111/j.1365-3059.2006.01446.x
16. Dodds, P. N., and Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548. doi: 10.1038/nrg2812
17. Douglas, A. E. (2014). Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harb Perspect. Biol. 6:a016113. doi: 10.1101/cshperspect.a016113
18. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and Su, Z. (2010). agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70. doi: 10.1093/nar/gkq310
19. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
20. Engel, P., and Moran, N. A. (2013). The gut microbiota of insects - diversity in structure and function. FEMS Microbiol. Rev. 37, 699-735. doi: 10.1111/1574-6976.12025
21. Estrada, C., Wcislo, W. T., and Van Bael, S. A. (2013). Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol. 198, 241-251. doi: 10.1111/nph.12140
22. Evans, H. C., Holmes, K. A., and Thomas, S. E. (2003). Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol. Prog. 2, 149-160. doi: 10.1007/s11557-006-0053-4
23. Evans, R. D. (2001). Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci. 6, 121-126. doi: 10.1016/S1360-1385(01)01889-1
24. Feldhaar, H. (2011). Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36, 533-543. doi: 10.1111/j.1365-2311.2011.01318.x
25. Freeman, S., and Rodriguez, R. J. (1993). Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260, 75-78. doi: 10.1126/science.260.5104.75
26. Friesen, M. L., Porter, S. S., Stark, S. C., Von Wettberg, E. J., Sachs, J. L., and Martinez-Romero, E. (2011). Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42, 23-46. doi: 10.1146/annurev-ecolsys-102710-145039
27. Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi: 10.1186/gb-2004-5-10-r80
28. Gerardo, N. M., and Parker, B. J. (2014). Mechanisms of symbtiont-conferred protection against natural enemies: an ecological and evolutionary framework. Cur. Opin. Insect Sci. (in press). doi: 10.1016/j.cois.2014.08.002
29. Gierlinger, N., and Schwanninger, M. (2006). Chemical imaging of poplar wood cell walls by confocal Raman microscopy. Plant Physiol. 140, 1246-1254. doi: 10.1104/pp.105.066993
30. Gunatilaka, A. A. L. (2006). Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurence. J. Nat. Prod. 69, 509-526. doi: 10.1021/np058128n
31. Hanada, R. E., Pomella, A. W., Costa, H. S., Bezerra, J. L., Loguercio, L. L., and Pereira, J. O. (2010). Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol. 114, 901-910. doi: 10.1016/j.funbio.2010.08.006
32. Herre, E. A., Mejia, L. C., Kyllo, D. A., Rojas, E., Maynard, Z., Butler, A., et al. (2007). Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88, 550-558. doi: 10.1890/05-1606
33. Higginbotham, S. J., Arnold, A. E., Ibañez, A., Spadafora, C., Coley, P. D., and Kursar, T. A. (2013). Bioactivity of fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants. PLoS ONE 8: e73192. doi: 10.1371/journal.pone.0073192
34. Jones, P. G., Allaway, D., Gilmour, D. M., Harris, C., Rankin, D., Retzel, E. R., et al. (2002). Gene discovery and microarray analysis of cacao (Theobroma cacao L.) varieties. Planta 216, 255-264. doi: 10.1007/s00425-002-0882-6
35. Khatabi, B., and Schäfer, P. (2012). Ethylene in mutualistic symbioses. Plant Signal. Behav. 7, 1634-1638. doi: 10.4161/psb.22471
36. Kimbell, J. R., Koropatnick, T. A., and Mcfall-Ngai, M. J. (2006). Evidence for the participation of the proteasome in symbiont-induced tissue morphogenesis. Biol. Bull. 211, 1-6. doi: 10.2307/4134572
37. Kitajima, K., Llorens, A. M., Stefanescu, C., Timchenko, M. V., Lucas, P. W., and Wright, S. J. (2012). How cellulose-based leaf toughness and lamina density contribute to long leaf lifespans of shade-tolerant species. New Phytol. 195, 640-652. doi: 10.1111/j.1469-8137.2012.04203.x
38. Krauss, U., Hidalgo, E., Bateman, R., Adonijah, V., Arroyo, C., Garcãa, J., et al. (2010). Improving the formulation and timing of application of endophytic biocontrol and chemical agents against frosty pod rot (Moniliophthora roreri) in cocoa (Theobroma cacao). Biol. Control 54, 230-240. doi: 10.1016/j.biocontrol.2010.05.011
39. Li, M., Wang, B., Zhang, M., Rantalainen, M., Wang, S., Zhou, H., et al. (2008). Symbiotic gut microbes modulate human metabolic phenotypes. Proc. Natl. Acad. Sci. U.S.A. 105, 2117-2122. doi: 10.1073/pnas.0712038105
40. Lohse, M., Nagel, A., Herter, T., May, P., Schroda, M., Zrenner, R., et al. (2014). Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ. 37, 1250-1258. doi: 10.1111/pce.12231
41. Maximova, S., Marelli, J.-P., Young, A., Pishak, S., Verica, J., and Guiltinan, M. (2006). Over-expression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta 224, 740-749. doi: 10.1007/s00425-005-0188-6
42. Maximova, S., Miller, C., Antunez De Mayolo, G., Pishak, S., Young, A., and Guiltinan, M. J. (2003). Stable transformation of Theobroma cacao L. and influence of matrix attachment regions on GFP expression. Plant Cell Rep. 21, 872-883. doi: 10.1007/s00299-003-0596-7
43. Mejía, L. C., Guiltinan, M. J., Shi, Z., Landherr, L., and Maximova, S., N. (2012). "Expression of designed antimicrobial peptides in Theobroma cacao L. trees reduces leaf necrosis caused by Phytophthora spp," in Small Wonders: Peptides for Disease Control (Washington, DC: American Chemical Society), 379-395.
44. Mejia, L. C., Rojas, E. I., Maynard, Z., Van Bael, S. A., Arnold, E. A., Hebbar, P., et al. (2008). Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46, 4-14. doi: 10.1016/j.biocontrol.2008.01.012
45. Miller, J. D., Mackenzie, S., Foto, M., Adams, G. W., and Findlay, J. A. (2002). Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol. Res. 106, 471-479. doi: 10.1017/S0953756202005671
46. Mitsuhara, I., Ugaki, M., Hirochika, H., Ohshima, M., Murakami, T., Gotoh, Y., et al. (1996). Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 37, 49-59. doi: 10.1093/oxfordjournals.pcp.a028913
47. Motamayor, J., Mockaitis, K., Schmutz, J., Haiminen, N., Livingstone, D., Cornejo, O., et al. (2013). The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol. 14:R53. doi: 10.1186/gb-2013-14-6-r53
48. Oakley, R. V., Wang, Y. S., Ramakrishna, W., Harding, S. A., and Tsai, C. J. (2007). Differential expansion and expression of alpha- and beta-tubulin gene families in Populus. Plant Physiol. 145, 961-973. doi: 10.1104/pp.107.107086
49. Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36. doi: 10.1093/nar/30.9.e36
50. Pieterse, C. M. J., Van Wees, S. C. M., Van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., et al. (1998). A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 1571-1580. doi: 10.1105/tpc.10.9.1571
51. Pugh, T., Fouet, O., Risterucci, A. M., Brottier, P., Abouladze, M., Deletrez, C., et al. (2004). A new cacao linkage map based on codominant markers: development and integration of 201 new microsatellite markers. Theor. Appl. Genet. 108, 1151-1161. doi: 10.1007/s00122-003-1533-4
52. Ritchie, M. E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A., et al. (2007). A comparison of background correction methods for two-colour microarrays. Bioinformatics 23, 2700-2707. doi: 10.1093/bioinformatics/btm412
53. Rodriguez, R. J., White, J. F. Jr., Arnold, A. E., and Redman, R. S. (2009). Fungal endophytes: diversity and functional roles. New Phytol. 182, 314-330. doi: 10.1111/j.1469-8137.2009.02773.x
54. Rojas, E. I., Rehner, S. A., Samuels, G. J., Van Bael, S. A., Herre, E. A., Cannon, P., et al. (2010). Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102, 1318-1338. doi: 10.3852/09-244
55. Rubini, M. R., Silva-Ribeiro, R. T., Pomella, A. W., Maki, C. S., Araújo, W. L., Dos Santos, D. R., et al. (2005). Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches' Broom Disease. Int. J. Biol. Sci. 1, 24-33. doi: 10.7150/ijbs.1.24
56. Shi, Z., Zhang, Y., Maximova, S., and Guiltinan, M. (2013). TcNPR3 from Theobroma cacao functions as a repressor of the pathogen defense response. BMC Plant Biol. 13:204. doi: 10.1186/1471-2229-13-204
57. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:3. doi: 10.2202/1544-6115.1027
58. Smyth, G. K. (2005). "Limma: linear models for microarray data," in Bioinformatics and Computational Biology Solutions using R and Bioconductor, eds R. Gentleman, V. Carey, S. Dudoit, R. Irizarry and W. Huber (New York, NY: Springer), 397-420.
59. Sparks, J. P. (2009). Ecological ramifications of the direct foliar uptake of nitrogen. Oecologia 159, 1-13. doi: 10.1007/s00442-008-1188-6
60. Stat, M., Morris, E., and Gates, R. D. (2008). Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl. Acad. Sci. U.S.A. 105, 9256-9261. doi: 10.1073/pnas.0801328105
61. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. doi: 10.1093/molbev/msm092
62. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., et al. (2004). mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939. doi: 10.1111/j.1365-313X.2004.02016.x
63. Van Bael, S. A., Estrada, C., and Wcislo, W. T. (2011). Fungal-fungal interactions in leaf-cutting ant agriculture. Psyche 2011:617478. doi: 10.1155/2011/617478
64. Van Bael, S. A., Seid, M. A., and Wcislo, W. T. (2012). Endophytic fungi increase the processing rate of leaves by leaf-cutting ants (Atta). Ecol. Entomol. 37, 318-321. doi: 10.1111/j.1365-2311.2012.01364.x
65. Van Bael, S. A., Valencia, M. C., Rojas, E. I., Gómez, N., Windsor, D. M., and Herre, E. A. (2009). Effects of foliar endophytic fungi on the preference and performance of the leaf beetle Chelymorpha alternans in Panama. Biotropica 41, 221-225. doi: 10.1111/j.1744-7429.2008.00476.x
66. Van Rhijn, P., and Vanderleyden, J. (1995). The Rhizobium-plant symbiosis. Microbiol. Rev. 59, 124-142.
67. Verica, J. A., Maximova, S. N., Strem, M. D., Carlson, J. E., Bailey, B. A., and Guiltinan, M. J. (2004). Isolation of ESTs from cacao (Theobroma cacao L.) leaves treated with inducers of the defense response. Plant Cell Rep. 23, 404-413. doi: 10.1007/s00299-004-0852-5
68. Wang, Q., Han, C., Ferreira, A. O., Yu, X., Ye, W., Tripathy, S., et al. (2011). Transcriptional programming and functional interactions within the phytophthora sojae RXLR effector repertoire. Plant Cell 23, 2064-2086. doi: 10.1105/tpc.111.086082
69. Weir, B. S., Johnston, P. R., and Damm, U. (2012). The Colletotrichum gloeosporioides species complex. Stud. Mycol. 73, 115-180. doi: 10.3114/sim0011