Quantitative trait loci × environment interactions for plant morphology vary over ontogeny in Brassica rapa

New Phytologist

Volumn 201, Issue 2, 2014, Pages 657-669

  Dechaine, Jennifer M ^a   Brock, Marcus T ^b   Iniguez Luy, Federico L ^c   Weinig, Cynthia ^b  

^a CENTRAL WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c INSTITUTO DE INVESTIGACIONES AGROPECUARIAS   (Chile)

Author keywords

Brassica rapa; Evolutionary development; Modularity; Ontogeny; Phenotypic plasticity; QTL environment interactions; Quantitative trait loci (QTLs); Trade offs

Indexed keywords

BREEDING SEASON; DICOTYLEDON; EVOLUTIONARY BIOLOGY; GENETIC ENGINEERING; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; MORPHOLOGY; ONTOGENY; PHENOTYPIC PLASTICITY; QUANTITATIVE ANALYSIS; SEEDLING; TRADE-OFF;

ANATOMY AND HISTOLOGY; BRASSICA RAPA; ENVIRONMENT; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INBREEDING; PLANT GENE; PLANT STEM; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; TIME;

BRASSICA RAPA; ENVIRONMENT; GENES, PLANT; INBREEDING; PLANT STEMS; QUANTITATIVE TRAIT LOCI; RECOMBINATION, GENETIC; REPRODUCTION; TIME FACTORS;

EID: 84890604099     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12520     Document Type: Article

References (97)

1. Adler LS, Wikler K, Wyndham FS, Linder CR, Schmitt J. 1993. Potential for persistence of genes escaped from canola: germination cues in crop, wild, and crop-wild hybrid Brassica rapa. Functional Ecology 7: 736-745.
2. Axelsson T, Shavorskaya O, Lagercrantz U. 2001. Multiple flowering time QTLs within several Brassica species could be the result of duplicated copies of one ancestral gene. Genome 44: 856-864.
3. Barthelemy D. 1991. Levels of organisation and repetition phenomena in seed plants. Acta Biotheoretica 39: 309-323.
4. Box GEP, Cox DR. 1964. An analysis of transformations. Journal of the Royal Statistical Society, Series B 26: 211-243.
5. Bradshaw AD. 1965. Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115-155.
6. Brakefield PM, Gates J, Keys Z, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB. 1996. Development, plasticity and evolution of butterfly eyespot patterns. Nature 384: 236-242.
7. Brakefield PM, Kesbeke F, Koch PB. 1998. The regulation of phenotypic plasticity of eyespots in the butterfly Bicyclus anynana. The American Naturalist 152: 853-860.
8. Brock MT, Dechaine JM, Iniguez-Luy FL, Maloof JN, Stinchcombe JR, Weinig C. 2010. Floral genetic architecture: an examination of QTL architecture underlying floral (co)variation across environments. Genetics 186: 1451-1465.
9. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. 2004. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences, USA 101: 15670-15675.
10. Cao G, Zhu J, He C, Gao Y, Yan J, Wu P. 2001. Impact of epistasis and QTL × environment interaction on the developmental behavior of plant height in rice (Oryza sativa L.). Theoretical and Applied Genetics 103: 153-160.
11. Casal JJ, Ballare CL, Tourn M, Sanchez RA. 1994. Anatomy, growth and survival of a long-hypocotyl mutant of Cucumis sativus deficient in phytochrome B. Annals of Botany 73: 569-575.
12. Casal JJ, Smith H. 1989. The function, action, and adaptive significance of phytochrome in light-grown plants. Plant, Cell & Environment 12: 855-862.
13. Causin HF, Wulff RD. 2003. Changes in the responses to light quality during ontogeny in Chenopodium album. Canadian Journal of Botany 81: 152-163.
14. Cheng Y, Wang Q, Ban Q, Geng J, Zhang XW, Yi Y, Hou X. 2009. Unconditional and conditional quantitative trait loci mapping for plant height in nonheading chinese cabbage. HortScience 44: 268-273.
15. Churchill GA, Doerge RW. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
16. Dechaine JM, Johnston JA, Brock MT, Weinig C. 2007. Constraints on the evolution of adaptive plasticity: costs of plasticity to density are expressed in segregating progenies. New Phytologist 176: 874-882.
17. Diggle PK. 1994. The expression of andromonoecy in Solanum hirtum (Solanaceae): phenotypic plasticity and ontogenetic contingency. American Journal of Botany 81: 1354-1365.
18. Dmitriew C, Blows CMW, Rowe L. 2010. Ontogenetic change in genetic variance in size depends on growth environment. The American Naturalist 175: 640-649.
19. Donohue K. 2003. Setting the stage: phenotypic plasticity as habitat selection. International Journal of Plant Sciences 164: S79-S92.
20. Donohue K, Messiqua D, Pyle EH, Heschel MS, Schmitt J. 2000. Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54: 1956-1968.
21. Donohue K, Schmitt J. 1999. The genetic architecture of plasticity to density in Impatiens capensis. Evolution 53: 1377-1386.
22. Dorn LA, Mitchell-Olds T. 1991. Genetics of Brassica campestris. 1. Genetic constraints on evolution of life-history characters. Evolution 45: 371-379.
23. Dudley SA, Schmitt J. 1995. Genetic differentiation in morphological responses to simulated foliar shade between populations of Impatiens capensis from open and woodland sites. Functional Ecology 9: 655-666.
24. Dudley SA, Schmitt J. 1996. Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. The American Naturalist 147: 445-465.
25. Edwards CE, Weinig C. 2011. The quantitative-genetic and QTL architecture of trait integration and modularity in Brassica rapa across simulated seasonal settings. Heredity 106: 661-677.
26. Erickson DL, Fenster CB, Stenoien HK, Price D. 2004. Quantitative trait locus analysis and the study of evolutionary processes. Molecular Ecology 13: 2505-2522.
27. Flury B. 1998. Common principal components and related multivariate models. New York, NY, USA: John Wiley & Sons.
28. Givnish TJ. 1982. On the adaptive significance of leaf height in forest herbs. The American Naturalist 120: 353-381.
29. Gomulkievicz R, Kirkpatrick M. 1992. Quantitative genetics and the evolution of reaction norms. Evolution 46: 390-411.
30. Gurganus MC, Fry JD, Nuzhdin SV, Pasyukova EG, Lyman RF, Mackay TFC. 1998. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. Genetics 149: 1883-1898.
31. Gutteling EW, Doroszuk A, Riksen JAG, Prokop Z, Reszka J, Kammenga JE. 2007. Environmental influence on the genetic correlations between life-history traits in Caenorhabditis elegans. Heredity 98: 206-213.
32. Hadfield JD, Wilson AJ, Garant D, Sheldon BC, Kruuk LEB. 2010. The misuse of BLUP in ecology and evolution. The American Naturalist 174: 116-125.
33. Haselhorst MSH, Edwards CE, Rubin MJ, Weinig C. 2011. Genetic architecture of life history traits and environment-specific trade-offs. Molecular Ecology 20: 4042-4058.
34. Hausmann NJ, Juenger TE, Sen S, Stow KA, Dawson TE, Simms EL. 2005. Quantitative trait loci affecting d13C and response to differential water availability in Arabidopsis thaliana. Evolution 59: 81-96.
35. He Q, Berg A, Li Y, Vallejos E, Wu R. 2009. Mapping genes for plant structure, development and evolution: functional mapping meets ontology. Trends in Genetics 26: 39-46.
36. Heuret P, Meredieu C, Coudurier T, Coudurier F, Barthelemy D. 2006. Ontogenetic trends in the morphological features of main stem annual shoots of Pinus pinaster (Pinaceae). American Journal of Botany 93: 1577-1587.
37. Hinata K, Prakash S. 1984. Ethnobotany and evolutionary origin of Indian oleiferous Brassicae. Indian Journal of Genetics and Plant Breeding 44: 102-112.
38. Iniguez-Luy FL, Lukens L, Farnham MW, Amasino RM, Osborn TC. 2009. Development of public immortal mapping populations, molecular markers and linkage maps for rapid cycling Brassica rapa and B. oleracea. Theoretical and Applied Genetics 120: 31-43.
39. Johanson U, West J, Lister C, Miichaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
40. Juenger T, Perez-Perez JM, Bernal S, Micol JL. 2005. Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture. Evolution & Development 7: 259-271.
41. Kassen R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15: 173-190.
42. Kim SY, Park BS, Kwon SJ, Kim J, Lim MH, Park YD, Kim DY, Suh SC, Jin YM, Ahn JH et al. 2007. Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Cell Reports 26: 327-336.
43. Koornneef M. 1991. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular and General Genetics 229: 57-66.
44. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Annual Reviews of Plant Physiology and Plant Molecular Biology 49: 345-370.
45. Koornneef M, Blankestijn-de Vries H, Hanhart C, Soppe W, Peeters T. 1994. The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant Journal 6: 911-919.
46. de Kroon H, Huber H, Stuefer JF, van Groenendael JM. 2005. A modular concept of phenotypic plasticity in plants. New Phytologist 166: 73-82.
47. Lechowicz MJ, Blais PA. 1988. Assessing the contribution of multiple interacting traits to plant reproductive success: environmental dependence. Journal of Evolutionary Biology 1: 255-273.
48. Lee I, Michaels SD, Masshardt AS, Amasino RM. 1994. The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant Journal 6: 903-909.
49. Levins R. 1968. Evolution in changing environments: some theoretical explorations. Princeton, NJ, USA: Princeton University Press.
50. Levy YY, Dean C. 1993. The transition to flowering. The Plant Cell 10: 1973-1989.
51. Lloyd DG. 1984. Variation strategies of plants in heterogeneous environments. Biological Journal of the Linnean Society 21: 357-385.
52. Lou P, Zhao J, Kim JS, Shen S, Del Carpio DP, Song X, Jin M, Vreugdenhil D, Wang X, Koornneef M et al. 2007. Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. Journal of Experimental Botany 58: 4005-4016.
53. Lynch M, Walsh JB. 1998. Genetics and analysis of quantitative traits. Sunderland, MA, USA: Sinauer Associates Inc.
54. Mackay TFC, Stone EA, Ayroles JF. 2009. The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics 10: 565-577.
55. Mezey JG, Houle D. 2003. Comparing G matrices: are common principal components informative? Genetics 165: 411-425.
56. Michaels SD, Amasino RM. 2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell 13: 935-941.
57. Michaels SD, He Y, Scortecci KC, Amasino RM. 2003. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences, USA 100: 10102-10107.
58. Mitchell-Olds T. 1996. Pleiotropy causes long-term genetic contraints on life-history evolution in Brassica rapa. Evolution 50: 1849-1858.
59. Nishioka M, Tamura K, Hayashi M, Fujimori Y, Ohkawa Y, Kuginuki Y, Harada K. 2005. Mapping of QTLs for bolting time in Brassica rapa (syn. campestris) under different environmental conditions. Breeding Science 55: 127-133.
60. Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, Lydiate DJ, Trick M. 1997. Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146: 1123-1129.
61. Parrish JAD, Bazzaz FA. 1985. Nutrient content of Abutilon theophrasti seeds and the competitive ability of the resulting plants. Oecologia 65: 247-251.
62. Perez-Perez JM, Serrano-Cartagena J, Micol JL. 2002. Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162: 893-915.
63. Phillips PC, Arnold SJ. 1999. Hierarchical comparison of genetic variance-covariance matrices. I. Using the flury hierarchy. Evolution 53: 1506-1515.
64. Pigliucci M. 1997. Ontogenic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae). American Journal of Botany 84: 887-895.
65. Pigliucci M, Schlichting CD. 1995. Ontogenetic reaction norms in Lobelia siphilitica (Lobeliaceae): response to shading. Ecology 76: 2134-2144.
66. Prakash S, Hinata K. 1980. Taxonomy, cytogenetics and origin of crop Brassicas, a review. Opera Botanica 55: 1-57.
67. R Development Core Team. 2007 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
68. Roach DA. 1986. Life history variation in Geranium carolinianum. 1. Covariation between characters at different stages of the life cycle. The American Naturalist 128: 47-57.
69. Robertson A. 1959. The sampling variance of genetic correlations. Biometrics 15: 469-485.
70. Room PM, Maillette L, Hanan JS. 1994. Module and metamer dynamics and virtual plants. Advances in Ecological Research 25: 105-157.
71. SAS 2001. SAS software version 8 for Windows. Cary, NC, USA: SAS Institute Inc.
72. Schlichting C, Pigliucci M. 1998. Phenotypic evolution: a reaction norm perspective. Sunderland, MA, USA: Sinauer Associates, Inc.
73. Schlichting CD. 1989. Plasticity in Phlox. II. Plasticity of character correlations. Oecologia 78: 496-501.
74. Schmalhausen II. 1949. Factors of evolution. Philadelphia, PA, USA: Blakiston.
75. Schmitt J, McCormac AC, Smith H. 1995. A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. The American Naturalist 146: 937-953.
76. Schranz ME, Quijada P, Sung SB, Lukens L, Amasino RM, Osborn TC. 2002. Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162: 1457-1468.
77. Simpson GG, Dean C. 2002. Arabidopsis, the rosetta stone of flowering time? Science 296: 285-289.
78. Smith H. 2000. Phytochromes and light signal perception by plants - an emerging synthesis. Nature 407: 585-591.
79. Teutonico RA, Osborn TC. 1995. Mapping loci controlling vernalization requirement in Brassica rapa. Theoretical and Applied Genetics 91: 1279-1283.
80. Ungerer MC, Halldorsdottir SS, Modliszewski JL, Mackay TFC, Purugganan MD. 2002. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics 160: 1133-1151.
81. Ungerer MC, Halldorsdottir SS, Purugganan MD, Mackay TFC. 2003. Genotype-environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics 165: 353-365.
82. Via S, Gomulkievicz R, De Jong G, Scheiner S, Schlichting CD, Van Tienderen P. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10: 212-217.
83. Vieira C, Pasyukova EG, Zeng ZB, Hackett JB, Lyman RF, Mackay TFC. 2000. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics 154: 213-227.
84. Wang S, Basten CJ, Zeng ZB. 2007. Windows QTL Cartographer version 2.5. Raleigh, NC, USA: NCSU Statistical Genetics.
85. Weinig C. 2000a. Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54: 124-136.
86. Weinig C. 2000b. Plasticity versus canalization: population differences in the timing of shade-avoidance responses. Evolution 54: 441-451.
87. Weinig C, Delph LF. 2001. Phenotypic plasticity early in life contrains developmental responses later. Evolution 55: 930-936.
88. Weinig C, Ungerer MC, Dorn LA, Kane NC, Toyonaga Y, Halldorsdottir SS, Mackay TFC, Purugganan MD, Schmitt J. 2002. Novel loci control variation in reproductive timing in Arabidosis thaliana in natural environments. Genetics 162: 1875-1884.
89. White J. 1979. The plant as a metapopulation. Annual Review of Ecology and Systematics 10: 109-145.
90. Williams PH, Hill CB. 1986. Rapid-cycling populations of Brassica. Science 232: 1385-1389.
91. Willmann MR, Roethig RS. 2011. The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis. Development 138: 677-685.
92. Winn AA. 1996a. Adaptation to fine-grained environmental variation: an analysis of within-individual leaf variation in an annual plant. Evolution 50: 1111-1118.
93. Winn AA. 1996b. The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutionary Biology 9: 737-752.
94. Wu R. 1998. The detection of plasticity genes in heterogenous environments. Evolution 52: 967-977.
95. Wu X, Wang Z, Chang X, Jing R. 2010. Genetic dissection of developmental behaviors of plant height in wheat under diverse water regimes. Journal of Experimental Botany 61: 2923-2937.
96. Yang X, Yu YJ, Zhang FL, Zou ZR, Zhao XY, Zhang DS, Xu JB. 2007. Linkage map construction and quantitative trait loci analysis for bolting based on a double haploid population of Brassica rapa. Journal of Integrative Plant Biology 49: 664-671.
97. Yuan YX, Wu J, Zhang XW, Xu DH, Bonnema G, Wang XW. 2009. A naturally occurring splicing site mutation in the Brasscia rapa FLC1 gene is associated with variation in flowering time. Journal of Experimental Botany 60: 1299-1308.