A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana

New Phytologist

Volumn 187, Issue 4, 2010, Pages 1102-1111

  Paul Victor, Cloé ^a   Züst, Tobias ^a   Rees, Mark ^b   Kliebenstein, Daniel J ^c   Turnbull, Lindsay A ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arabidopsis thaliana; Defence; Glucosinolate; Herbivore; Relative growth rate; Trade off

Indexed keywords

GLUCOSINOLATE;

DICOTYLEDON; GROWTH RATE; HERBIVORE; INSECT; PHYSIOLOGICAL RESPONSE; REPRODUCTIVE COST; STANDARDIZATION; TRADE-OFF;

ANIMAL; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LEPIDOPTERA; PLANT DISEASE; PLANT SEED;

ANIMALS; ARABIDOPSIS; GLUCOSINOLATES; LEPIDOPTERA; MODELS, BIOLOGICAL; PLANT DISEASES; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HEXAPODA;

EID: 77955762975     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03325.x     Document Type: Article

References (59)

1. Agrawal AA, Conner JK, Stinchcombe JR. Evolution of plant resistance and tolerance to frost damage. Ecology Letters 2004, 7:1199-1208.
2. Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control 1974, C19:716-723.
3. Almeida-Cortez JS, Shipley W. No significant relationship exists between seedling relative growth rate under nutrient limitation and potential tissue toxicity. Functional Ecology 2002, 16:122-127.
4. Almeida-Cortez JS, Shipley B, Arnason JT. Do plant species with high relative growth rates have poorer chemical defences? Functional Ecology 1999, 13:819-827.
5. Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Koornneef M. Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 1999, 96:4710-4717.
6. Alonso-Blanco C, Peeters AJ, Koornneef M, Lister C, Dean C, van den Bosch N, Pot J, Kuiper MT. Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant Journal 1998, 14:259-271.
7. Arendt JD. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 1997, 72:149-177.
8. Arendt JD. Allocation of cells to proliferation vs. differentiation and its consequences for growth and development. Journal of Experimental Zoology 2000, 288:219-234.
9. Barth C, Jander G. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant Journal 2006, 46:549-562.
10. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF. Allocating resources to reproduction and defense. Bioscience 1987, 37:58-67.
11. Beekwilder J, van Leeuwen W, van Dam NM, Bertossi M, Grandi V, Mizzi L, Soloviev M, Szabados L, Molthoff JW, Schipper B. The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS ONE 2008, 3:e2068.
12. Bergelson J, Purrington CB. Surveying patterns in the cost of resistance in plants. American Naturalist 1996, 148:536-558.
13. Bernacchi CJ, Coleman JS, Bazzaz FA, McConnaughay KDM. Biomass allocation in old-field annual species grown in elevated CO2 environments: no evidence for optimal partitioning. Global Change Biology 2000, 6:855-863.
14. Bidart-Bouzat MG, Kliebenstein DJ. Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana. Journal of Chemical Ecology 2008, 34:1026-1037.
15. Bones AM, Rossiter JT. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiologia Plantarum 1996, 97:194-208.
16. Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 2003, 62:471-481.
17. Coleman JS, McConnaughay KDM. A non-functional interpretation of a classical optimal-partitioning example. Functional Ecology 1995, 9:951-954.
18. Coley PD, Bryant JP, Chapin FS. Resource availability and plant antiherbivore defense. Science 1985, 230:895-899.
19. Durham Brooks TL, Miller ND, Spalding EP. Plasticity of Arabidopsis root gravitropism throughout a multi-dimensional condition space quantified by automated image analysis. Plant Physiology 2010, 152:206-216.
20. Enquist BJ, West GB, Charnov EL, Brown JH. Allometric scaling of production and life-history variation in vascular plants. Nature 1999, 401:907-911.
21. Fu J, Keurentjes JJB, Bouwmeester H, America T, Verstappen FWA, Ward JL, Beale MH, de Vos RCH, Dijkstra M, Scheltema RA. System-wide molecular evidence for phenotypic buffering in Arabidopsis. Nature Genetics 2009, 41:166-167.
22. Grime JP. Plant strategies, vegetation processes, and ecosystem properties 2002, Chichester, UK, John Wiley & Sons Ltd
23. Halkier BA, Gershenzon J. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 2006, 57:303-333.
24. Hansen BG, Kerwin RE, Ober JA, Lambrix VM, Mitchell-Olds T, Gershenzon J, Halkier BA, Kliebenstein DJ. A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiology 2008, 148:2096-2108.
25. Herms DA, Mattson WJ. The dilemma of plants - to grow or defend. Quarterly Review of Biology 1992, 67:283-335.
26. Hunt R. Plant growth curves: a functional approach to plant growth analysis 1982, London, UK, Edward Arnold
27. Hunt R, Cornelissen JHC. Physiology, allocation, and growth rate: a reexamination of the Tilman model. American Naturalist 1997, 150:122-130.
28. Iwasa Y. Dynamic optimization of plant growth. Evolutionary Ecology Research 2000, 2:437-455.
29. Jander G, Cui JP, Nhan B, Pierce NE, Ausubel FM. The TASTY locus on chromosome 1 of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni. Plant Physiology 2001, 126:890-898.
30. Keurentjes JJB, Fu JY, Terpstra IR, Garcia JM, van den Ackerveken G, Snoek LB, Peeters AJM, Vreugdenhil D, Koornneef M, Jansen RC. Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proceedings of the National Academy of Sciences, USA 2007, 104:1708-1713.
31. Keurentjes JJB, Sulpice R, Gibon Y, Steinhauser MC, Fu JY, Koornneef M, Stitt M, Vreugdenhil D. Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biology 2008, 9:20.
32. Kim JH, Jander G. Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant Journal 2007, 49:1008-1019.
33. Kliebenstein DJ. Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant, Cell & Environment 2004, 27:675-684.
34. Kliebenstein DJ, D'Auria JC, Behere AS, Kim JH, Gunderson KL, Breen JN, Lee G, Gershenzon J, Last RL, Jander G. Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant Journal 2007, 51:1062-1076.
35. Kliebenstein DJ, Gershenzon J, Mitchell-Olds T. Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 2001a, 159:359-370.
36. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J, Mitchell-Olds T. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiology 2001b, 126:811-825.
37. Kliebenstein DJ, Pedersen D, Barker B, Mitchell-Olds T. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 2002, 161:325-332.
38. Koricheva J. Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 1999, 119:467-473.
39. Koricheva J. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 2002, 83:176-190.
40. Mauricio R. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. American Naturalist 1998, 151:20-28.
41. McConnaughay KDM, Coleman JS. Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 1999, 80:2581-2593.
42. Nour-Eldin HH, Halkier BA. Piecing together the transport pathway of aliphatic glucosinolates. Phytochemistry Reviews 2009, 8:53-67.
43. Paul-Victor C, Turnbull LA. The effect of growth conditions on the seed size/number trade-off. PLoS ONE 2009, 4:e6917. http://dx.doi.org/10.1371/journal.pone.0006917, doi: 10.1371/journal.pone.0006917
44. Perrin N, Sibly RM. Dynamic-models of energy allocation and investment. Annual Review of Ecology and Systematics 1993, 24:379-410.
45. Pinheiro JC, Bates DM. Mixed-effects models in S and S-plus 2000, London, UK, Springer
46. Poorter L, Kitajima K. Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 2007, 88:1000-1011.
47. Poorter H, Remkes C. Leaf-area ratio and net assimilation rate of 24 wild-species differing in relative growth-rate. Oecologia 1990, 83:553-559.
48. Purrington CB, Bergelson J. Fitness consequences of genetically engineered herbicide and antibiotic resistance in Arabidopsis thaliana. Genetics 1997, 145:807-814.
49. R: a language and environment for statistical computing 2008, R Development Core Team, Vienna, Austria, R Foundation for Statistical Computing
50. Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Bushena C. Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology 1998, 12:327-338.
51. Reichelt M, Brown PD, Schneider B, Oldham NJ, Stauber E, Tokuhisa J, Kliebenstein DJ, Mitchell-Olds T, Gershenzon J. Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 2002, 59:663-671.
52. Rose KE, Atkinson RL, Turnbull LA, Rees M. The costs and benefits of fast living. Ecology Letters 2009, 12:1379-1384.
53. Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM. Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 2002, 83:505-517.
54. Sønderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA, Kliebenstein DJ. A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2007, 2:16.
55. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC. Starch as a major integrator in the regulation of plant growth. Proceedings of the National Academy of Sciences, USA 2009, 106:10348-10353.
56. Turnbull LA, Paul-Victor C, Schmid B, Purves DW. Growth rates, seed size, and physiology: do small-seeded species really grow faster? Ecology 2008, 89:1352-1363.
57. Wentzell AM, Rowe HC, Hansen BG, Ticconi C, Halkier BA, Kliebenstein DJ. Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. Plos Genetics 2007, 3:1687-1701.
58. West GB, Brown JH, Enquist BJ. A general model for ontogenetic growth. Nature 2001, 413:628-631.
59. West MAL, van Leeuwen H, Kozik A, Kliebenstein DJ, Doerge RW, St Clair DA, Michelmore RW. High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genome Research 2006, 16:787-795.