A unified approach to the estimation and interpretation of resistance costs in plants

Heredity

Volumn 107, Issue 5, 2011, Pages 386-394

  Vila Aiub, M M ^a   Neve, P ^b   Roux, F ^c  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIV LILLE   (France)

Author keywords

defence traits; fitness; genetic background; resistance costs

Indexed keywords

ALLELE; COST-BENEFIT ANALYSIS; EXPERIMENTAL STUDY; FITNESS; FUTURE PROSPECT; GENETIC VARIATION; LIFE HISTORY TRAIT; PLANT;

ADAPTATION; BIOLOGICAL MODEL; DISEASE RESISTANCE; GENE FREQUENCY; GENETIC SELECTION; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; PLANT; PLANT GENE; REPRODUCTIVE FITNESS; REVIEW;

ADAPTATION, BIOLOGICAL; DISEASE RESISTANCE; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENES, PLANT; GENETIC FITNESS; GENOTYPE; MODELS, GENETIC; PLANTS; SELECTION, GENETIC;

EID: 80054808932     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2011.29     Document Type: Review

References (79)

1. Al-Ahmad H, Dwyer J, Moloney M, Gressel J (2006). Mitigation of establishment of Brassica napus transgenes in volunteers using a tandem construct containing a selectively unfit gene. Plant Biotechnol J 4: 7-21.
2. Al-Ahmad H, Galili S, Gressel J (2005). Poor competitive fitness of transgenically mitigated tobacco in competition with the wild type in a replacement series. Planta 222: 372-385. (Pubitemid 41429394)
3. Al-Ahmad H, Gressel J (2006). Mitigation using a tandem construct containing a selectively unfit gene precludes establishment of Brassica napus transgenes in hybrids and backcrosses with weedy Brassica rapa. Plant Biotechnol J 4: 23-33.
4. Bahri B, Kaltz O, Leconte M, De Vallavieille-Pope C, Enjalbert J (2009). Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f.sp.tritici. BMC Evol Biol 9: 26.
5. Barrett LG, Kniskern JM, Bodenhausen N, Zhang W, Bergelson J (2009). Continua of specificity and virulence in plant hostpathogen interactions: causes and consequences. New Phytol 183: 513-529.
6. Baucom RS, Mauricio R (2004). Fitness costs and benefits of novel herbicide tolerance in a noxious weed. Proc Natl Acad Sci USA 101: 13386-13390. (Pubitemid 39209675)
7. Bayley CC, Morgan M, Dale EC, Ow DW (1992). Exchange of gene activity in transgenic plants catalyzed by the Cre-lox site-specific recombination system. Plant Mol Biol 18: 353-361.
8. Bergelson J (1994). The effects of genotype and the environment on costs of resistance in lettuce. Am Nat 143: 349-359.
9. Bergelson J, Purrington CB (1996). Surveying patterns in the cost of resistance in plants. Am Nat 148: 536-558.
10. Bergelson J, Purrington CB, Palm CJ, Lopez-Gutierrez JC (1996). Costs of resistance: a test using transgenic Arabidopsis thaliana. Proc R Soc Lond Ser B-Biol Sci 263: 1659-1663. (Pubitemid 27055558)
11. Boege K, Dirzo R, Siemens D, Brown P (2007). Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10: 177-187.
12. Brown JKM (2002). Yield penalties of disease resistance in crops. Curr Opin Plant Biol 5: 339-344.
13. Burdon JJ, Thrall PH (2003). The fitness costs to plants of resistance to pathogens. Genome Biol 4: 227.
14. Burke JM, Rieseberg LH (2003). Fitness effects of transgenic disease resistance in sunflowers. Science 300: 1250. (Pubitemid 36618230)
15. Carrière Y, Ellers-Kirk C, Liu YB, Sims MA, Patin AL, Dennehy TJ et al. (2001). Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 94: 1571-1576. (Pubitemid 33750171)
16. Cochran DG (1993). Decline of pyrethroid resistance in the absence of selection pressure in a population of German cockroaches (Dictyoptera: Blattellidae). J Econ Entomol 86: 1639-1644. (Pubitemid 2072920)
17. Cohan FM, King EC, Zawadzki P (1994). Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution 48: 81-95. (Pubitemid 2113192)
18. Cousens RD, Gill GS, Speijers EJ (1997). Comment: number of sample populations required to determine the effects of herbicide resistance on plant growth and fitness. Weed Res 37: 1-4. (Pubitemid 27210738)
19. Coustau C, Chevillon C, ffrench-Constant R (2000). Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15: 378-383. (Pubitemid 30646792)
20. Délye C, Matejicek A, Gasquez J (2002). PCR-based detection of resistance to acetyl-CoA carboxylase-inhibiting herbicides in black-grass (Alopecurus myosuroides Huds) and ryegrass (Lolium rigidum Gaud). Pest Manag Sci 58: 474-478. (Pubitemid 34453471)
21. Ducrocq S, Madur D, Veyrieras JB, Camus-Kulandaivelu L, Kloiber-Maitz M, Presterl T et al. (2008). Key impact of Vgt1 on flowering time adaptation in maize: evidence from association mapping and ecogeographical information. Genetics 178: 2433-2437.
22. Ellstrand NC, Prentice HC, Hancock JF (1999). Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30: 539-563. (Pubitemid 30065637)
23. Falconer DS, Mackay TFS (1996). Introduction to Quantitative Genetics, 4th edn. Longman: Essex.
24. Fritz RS, Simms EL (1992). Plant Resistance to Herbivores and Pathogens. University of Chicago Press: Chicago, USA.
25. Gassmann AJ (2005). Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off. Oecologia 145: 575-585. (Pubitemid 41437693)
26. Giancola S, McKhann HI, Bérard A, Camilleri C, Durand S, Libeau P et al. (2006). Utilization of the three high-throughput SNP genotyping methods, the GOOD assay, Amplifluor and TaqMan, in diploid and polyploid plants. Theor Appl Genet 112: 1115-1124.
27. Goss EM, Bergelson J (2007). Fitness consequences of infection of Arabidopsis thaliana with its natural bacterial pathogen Pseudomonas viridiflava. Oecologia 152: 71-81. (Pubitemid 46639999)
28. Green JM (2009). Evolution of glyphosate-resistant crop technology. Weed Sci 57: 108-117.
29. Guillemaud T, Lenormand T, Bourguet D, Chevillon C, Pasteur N, Raymond M (1998). Evolution of resistance in Culex pipiens: allele replacement and changing environment. Evolution 52: 443-453. (Pubitemid 28222720)
30. Heidel AJ, Clarke JD, Antonovics J, Dong X (2004). Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168: 2197-2206. (Pubitemid 40066354)
31. Herms DA, Mattson WJ (1992). The dilemma of plants-to grow or defend. Q Rev Biol 67: 283-335.
32. Holt JS, Thill DC (1994). Growth and productivity of resistant plants. In: Powles SB and Holtum JAM (eds). Herbicide Resistance in Plants. Biology and Biochemistry. Lewis Publishers: Boca Raton, pp 299-316.
33. Jackson MW, Stinchcombe JR, Korves TM, Schmitt J (2004). Costs and benefits of cold tolerance in transgenic Arabidopsis thaliana. Mol Ecol 13: 3609-3615. (Pubitemid 39415690)
34. Jordan N (1996). Effects of the triazine-resistance mutation on fitness in Amaranthus hybridus (Smooth Pigweed). J Appl Ecol 33: 141-150.
35. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ et al. (2008). Efficient control of population structure in model organism association mapping. Genetics 178: 1709-1723.
36. Keller LF, Waller DM (2002). Inbreeding effects in wild populations. Trends Ecol Evol 17: 230-241. (Pubitemid 34270584)
37. Korves T, Bergelson J (2004). A novel cost of R gene resistance in the presence of disease. Am Nat 163: 489-504. (Pubitemid 38630543)
38. Labbé P, Sidos N, Raymond M, Lenormand T (2009). Resistance gene replacement in the mosquito Culex pipiens: fitness estimation from long-term cline series. Genetics 182: 303-312.
39. Lander ES, Schork NJ (1994). Genetic dissection of complex traits. Science 265: 2037.
40. Laughlin KD, Power AG, Snow AA, Spencer LJ (2009). Risk assessment of genetically engineered crops: fitness effects of virus-resistance transgenes in wild Cucurbita pepo. Ecol Appl 19: 1091-1101.
41. Lenormand T, Bourguet D, Guillemaud T, Raymond M (1999). Tracking the evolution of insecticide resistance in the mosquito Culex pipiens. Nature 400: 861-864. (Pubitemid 29406719)
42. Lenormand T, Raymond M (2000). Analysis of clines with variable selection and variable migration. Am Nat 155: 70-82. (Pubitemid 30132336)
43. Li A, Lohmeyer KH, Miller JA (2009). Dynamics and mechanisms of permethrin resistance in a field population of the horn fly, Haematobia irritans irritans. Insect Sci 16: 175-184.
44. Maisnier-Patin S, Andersson DI (2004). Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res Microbiol 155: 360-369. (Pubitemid 38781179)
45. Marshall DL, Ellstrand NC (1986). Sexual selection in Raphanus sativus: experimental data on nonrandom fertilization, maternal choice, and consequences of multiple paternity. Am Nat 127: 446.
46. Mauricio R (1998). Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am Nat 151: 20-28. (Pubitemid 28131911)
47. McCloskey WB, Holt JS (1990). Triazine resistance in Senecio vulgaris parental and nearly isonuclear backcrossed biotypes is correlated with reduced productivity. Plant Physiol 92: 954-962. (Pubitemid 120029784)
48. McCloskey WB, Holt JS (1991). Effect of growth temperature on biomass production of nearly isonuclear triazine-resistant and-susceptible common groundsel (Senecio vulgaris L). Plant Cell Environ 14: 699-705.
49. Menchari Y, Chauvel B, Darmency H, Delye C (2008). Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in blackgrass Alopecurus myosuroides. J Appl Ecol 45: 939-947. (Pubitemid 351614871)
50. Nagylaki T (1975). Conditions for the existence of clines. Genetics 80: 595-615.
51. Neve P (2007). Challenges for herbicide resistance evolution and management: 50 Years after Harper. Weed Res 47: 365-369. (Pubitemid 47346680)
52. Neve P, Powles S (2005). High survival frequencies at low herbicide use rates in populations of Lolium rigidum result in rapid evolution of herbicide resistance. Heredity 95: 485-492. (Pubitemid 41720001)
53. Nordborg M, Weigel D (2008). Next-generation genetics in plants. Nature 456: 720-723.
54. Núñez-Farfán J, Fornoni J, Valverde PL (2007). The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Syst 38: 541-566.
55. Osborne BI, Wirtz U, Baker B (1995). A system for insertional mutagenesis and chromosomal rearrangement using the Ds transposon and Cre-lox. Plant J 7: 687-701.
56. Paris M, Roux F, Berard A, Reboud X (2008). The effects of the genetic background on herbicide resistance fitness cost and its associated dominance in Arabidopsis thaliana. Heredity 101: 499-506.
57. Pedersen BP, Neve P, Andreasen C, Powles SB (2007). Ecological fitness of a glyphosate-resistant Lolium rigidum population: growth and seed production along a competition gradient. Basic Appl Ecol 8: 258-268. (Pubitemid 46528381)
58. Preston C, Powles SB (2002). Evolution of herbicide resistance in weeds: initial frequency of target site-based resistance to acetolactate synthase-inhibiting herbicides in Lolium rigidum. Heredity 88: 8-13. (Pubitemid 34171971)
59. Preston C, Wakelin AM, Dolman FC, Bostamam Y, Boutsalis P (2009). A decade of glyphosate-resistant Lolium around the world: mechanisms, genes, fitness, and agronomic management. Weed Sci 57: 435-441.
60. Purrington CB (2000). Costs of resistance. Curr Opin Plant Biol 3: 305-308. (Pubitemid 30437869)
61. Purrington CB, Bergelson J (1997). Fitness consequences of genetically engineered herbicide and antibiotic resistance in Arabidopsis thaliana. Genetics 145: 807-814. (Pubitemid 27108034)
62. Purrington CB, Bergelson J (1999). Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana. Am Nat 154: S82-S91.
63. Restif O, Koella J (2004). Concurrent evolution of resistance and tolerance to pathogens. Am Nat 164: E90-E102.
64. Roux F, Camilleri C, Bérard A, Reboud X (2005). Multigenerational versus single generation studies to estimate herbicide resistance fitness cost in Arabidopsis thaliana. Evolution 59: 2264-2269. (Pubitemid 41552998)
65. Roux F, Gasquez J, Reboud X (2004). The dominance of the herbicide resistance cost in several Arabidopsis thaliana mutant lines. Genetics 166: 449-460. (Pubitemid 38364731)
66. Roux F, Giancola S, Durand S, Reboud X (2006). Building of an experimental cline with Arabidopsis thaliana to estimate herbicide fitness cost. Genetics 173: 1023-1031. (Pubitemid 43945916)
67. Roux F, Reboud X (2005). Is the cost of herbicide resistance expressed in the breakdown of the relationships between characters? A case study using synthetic-auxin-resistant Arabidopsis thaliana mutants. Genet Res 85: 101-110. (Pubitemid 40975756)
68. Salzmann D, Handley RJ, Mueller-Scharer H (2008). Functional significance of triazine-herbicide resistance in defence of Senecio vulgaris against a rust fungus. Basic Appl Ecol 9: 577-587.
69. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002). Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17: 278-285. (Pubitemid 34518297)
70. Tardif FJ, Rajcan I, Costea M (2006). A mutation in the herbicide target site acetohydroxyacid synthase produces morphological and structural alterations and reduces fitness in Amaranthus powellii. New Phytol 169: 251-264.
71. Thrall PH, Burdon JJ (2003). Evolution of virulence in a plant host-pathogen metapopulation. Science 299: 1735-1737. (Pubitemid 36337200)
72. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003). Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77. (Pubitemid 36569584)
73. Vacher C, Bourguet D, Rousset F, Chevillon C, Hochberg ME (2003). Modelling the spatial configuration of refuges for a sustainable control of pests: a case study of Bt cotton. J Evol Biol 16: 378-387. (Pubitemid 36567969)
74. Vila-Aiub MM, Neve P, Powles SB (2009a). Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184: 751-767.
75. Vila-Aiub MM, Neve P, Powles SB (2005a). Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167: 787-796. (Pubitemid 43923814)
76. Vila-Aiub MM, Neve P, Powles SB (2009b). Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum. J Ecol 97: 772-780.
77. Vila-Aiub MM, Neve P, Steadman KJ, Powles SB (2005b). Ecological fitness of a multiple herbicide-resistant Lolium rigidum population: dynamics of seed germination and seedling emergence of resistant and susceptible phenotypes. J Appl Ecol 42: 288-298. (Pubitemid 40641083)
78. Wang T, Picard JC, Tian X, Darmency H (2010). A herbicideresistant ACCase 1781 Setaria mutant shows higher fitness than wild type. Heredity 105: 394-400.
79. Yu Q, Collavo A, Zheng MQ, Owen M, Sattin M, Powles SB (2007). Diversity of acetyl-coenzyme a carboxylase mutations in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145: 547-558. (Pubitemid 47575137)