Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana

Nature

Volumn 465, Issue 7298, 2010, Pages 632-636

  Todesco, Marco ^a   Balasubramanian, Sureshkumar ^a,m   Hu, Tina T ^b,n   Traw, M Brian ^c   Horton, Matthew ^d   Epple, Petra ^e   Kuhns, Christine ^f,g   Sureshkumar, Sridevi ^a   Schwartz, Christopher ^h,i   Lanz, Christa ^a   Laitinen, Roosa A E ^a   Huang, Yu ^b   Chory, Joanne ^h,j   Lipka, Volker ^f,g   Borevitz, Justin O ^d   Dangl, Jeffery L ^e,k   Bergelson, Joy ^d   Nordborg, Magnus ^b,l   Weigel, Detlef ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

^f SAINSBURY LABORATORY   (United Kingdom)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

^h SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

ⁱ UNIVERSITY OF WISCONSIN MADISON   (United States)

^j HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^k UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^l GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^m UNIVERSITY OF QUEENSLAND   (Australia)

ⁿ PRINCETON UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ANTIHERBIVORE DEFENSE; DICOTYLEDON; DISEASE RESISTANCE; EVOLUTIONARY BIOLOGY; FITNESS; GENETIC VARIATION; GENOMICS; HERBIVORY; TRADE-OFF;

ACCELERATED CELL DEATH 6 GENE; ARABIDOPSIS; ARTICLE; BIOMASS; CONTROLLED STUDY; GENE LOCUS; GENETIC VARIABILITY; HERBIVORY; INFECTION SENSITIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEFENSE; PLANT DISEASE; PLANT GENE; PLANT GENOME; PLANT LEAF; PLANT PATHOGEN INTERACTION; PLEIOTROPY; PRIORITY JOURNAL; VEGETATIVE GROWTH;

ALLELES; ANKYRINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC FITNESS; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; QUANTITATIVE TRAIT LOCI;

EID: 77953198418     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09083     Document Type: Article

References (53)

1. Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227 (2005).
2. Holub, E. B. The arms race is ancient history in Arabidopsis, the wildflower. Nature Rev. Genet. 2, 516-527 (2001).
3. Holub, E. B. Natural variation in innate immunity of a pioneer species. Curr. Opin. Plant Biol. 10, 415-424 (2007).
4. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).
5. Bent, A. F. & Mackey, D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436 (2007).
6. Heil, M. & Baldwin, I. T. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67 (2002).
7. Mauricio, R. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am. Nat. 151, 20-28 (1998).
8. Heil, M., Hilpert, A., Kaiser, W. & Linsenmair, K. E. Reduced growth and seed set following chemical induction of pathogen defence: Does Systemic Acquired Resistance (SAR) incur allocation costs? J. Ecol. 88, 645-654 (2000).
9. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M. & Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77 (2003).
10. Zavala, J. A. & Baldwin, I. T. Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecol. 4, 11 (2004).
11. Korves, T. A novel cost of R gene resistance in the presence of disease. Am. Nat. 163, 489-504 (2004).
12. Lu, H., Rate, D. N., Song, J. T. & Greenberg, J. T. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15, 2408-2420 (2003).
13. Lu, H., Liu, Y. & Greenberg, J. T. Structure-function analysis of the plasma membrane-localized Arabidopsis defense component ACD6. Plant J. 44, 798-809 (2005).
14. Balasubramanian, S. et al. QTL mapping in new Arabidopsis thaliana advanced intercross-recombinant inbred lines. PLoS ONE 4, e4318 (2009).
15. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121-1133 (2006).
16. Rate, D. N., Cuenca, J. V., Bowman, G. R., Guttman, D. S. & Greenberg, J. T. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11, 1695-1708 (1999).
17. Lorrain, S., Vailleau, F., Balague, C. & Roby, D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263-271 (2003).
18. Greenberg, J. T. & Yao, N. The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6, 201-211 (2004).
19. Yu, I. C., Parker, J. & Bent, A. F. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl Acad. Sci. USA 95, 7819-7824 (1998).
20. Gaffney, T. et al. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754-756 (1993).
21. Lu, H. et al. Genetic analysis of acd6-1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis. Plant J. 58, 401-412 (2009).
22. Abreu, M. E. & Munné-Bosch, S. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J. Exp. Bot. 60, 1261-1271 (2009).
23. Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).
24. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature. doi:10.1038/nature08800 (24 March 2010).
25. Bomblies, K. et al. Local-scale patterns of genetic variability, outcrossing and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet. 6, e1000890 (2010).
26. Traw, M. B., Kniskern, J. M. & Bergelson, J. SAR increases fitness of Arabidopsis thaliana in the presence of natural bacterial pathogens. Evolution 61, 2444-2449 (2007).
27. Van der Hoorn, R. A., De Wit, P. J. & Joosten, M. H. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7, 67-71 (2002).
28. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657 (2003).
29. Broman, K. W., Wu, H., Sen, S. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889-890 (2003).
30. Tuinstra, M., Ejeta, G. & Goldsbrough, P. Heterogenous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theor. Appl. Genet. 95, 1005-1011 (1997).
31. Warthmann, N., Fitz, J. & Weigel, D. MSQT for choosing SNP assays from multiple DNA alignments. Bioinformatics 23, 2784-2787 (2007).
32. Koch, E. & Slusarenko, A. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2, 437-445 (1990).
33. Ossowski, S., Schwab, R. & Weigel, D. Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53, 674-690 (2008).
34. Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S. & Mullineaux, P. M. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832 (2000).
35. Weigel, D. & Glazebrook, J. Arabidopsis: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 2002).
36. Lempe, J. et al. Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet. 1, e6 (2005).
37. Platt, A. et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet. 6, e1000843 (2010).
38. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
39. Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609-W612 (2006).
40. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
41. Thornton, K. libsequence: a C11 class library for evolutionary genetic analysis. Bioinformatics 19, 2325-2327 (2003).
42. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
43. Paradis, E., Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290 (2004).
44. Hirata, T. & Takamatsu, S. Nucleotide sequence diversity of rDNA internal transcribed spacers extracted from conidia and cleistothecia of several powdery mildew fungi. Mycoscience 37, 283-288 (1996).
45. Adam, L. & Somerville, S. C. Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341-356 (1996).
46. Vogel, J. & Somerville, S. Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl Acad. Sci. USA 97, 1897-1902 (2000).
47. Holt, B. F. III et al. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev. Cell 2, 807-817 (2002).
48. Kaminaka, H. et al. bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 25, 4400-4411 (2006).
49. King, E. O., Ward, M. K. & Raney, D. E. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44, 301-307 (1954).
50. Jakob, K. et al. Pseudomonas viridiflava and P. syringae-natural pathogens of Arabidopsis thaliana. Mol. Plant Microbe Interact. 15, 1195-1203 (2002).
51. Segarra, G., Jauregui, O., Casanova, E. & Trillas, I. Simultaneous quantitative LC-ESI-MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress. Phytochemistry 67, 395-401 (2006).
52. Dewdney, J. et al. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24, 205-218 (2000).
53. Konieczny, A. & Ausubel, F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 4, 403-410 (1993).