Genotype-by-environment interaction and plasticity: Exploring genomic responses of plants to the abiotic environment

Annual Review of Ecology, Evolution, and Systematics

Volumn 44, Issue , 2013, Pages 5-29

  Des Marais, David L ^a   Hernandez, Kyle M ^a   Juenger, Thomas E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Antagonistic pleiotropy; Conditional neutrality; Differential sensitivity; G E; Plasticity; QTL

Indexed keywords

ENVIRONMENTAL FACTOR; GENOME; GENOTYPE; LOCAL ADAPTATION; MAGNITUDE; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; PHYSIOLOGICAL RESPONSE; PLEIOTROPY; SENSITIVITY ANALYSIS;

EID: 84888585514     PISSN: 1543592X     EISSN: 15452069     Source Type: Book Series    
DOI: 10.1146/annurev-ecolsys-110512-135806     Document Type: Review

References (137)

1. Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM. 2005. Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol. 139:1304-12
2. Anderson JT, Lee CR, Rushworth CA, Colautti RI, Mitchell-Olds T. 2013. Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol. Ecol. 22:699-708
3. Auld JR, Agrawal AA, Relyea RL. 2010. Reevaluating the costs and limits of adaptive plasticity. Proc. R. Soc. Lond. Ser. B 277:503-11
4. Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF, et al. 2009. Systems genetics of complex traits in Drosophila melanogaster. Nat. Genet. 41:299-307
5. Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D. 2010. Submergence tolerant rice: SUB1's journey from landrace to modern cultivar. Rice 3:138-47
6. Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, et al. 2006. The PHY-TOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat. Genet. 38:711-15
7. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. 2008. The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 22:699-708
8. Beales J, Turner A, Griffiths S, Snape JW, Laurie DA. 2007. A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor. Appl. Genet. 115:721-33
9. Beavis WD. 1994. The power and deceit of QTL experiments: lessons from comparative QTL studies. In Proc. 49th Annu. Corn Sorghum Ind. Res. Conf., pp. 250-66. Washington, DC: Am. Seed Trade Assoc.
10. Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH. 2010. The role of recently derived FT paralogs in sunflower domestication. Curr. Biol. 20:629-35
11. Bohnert HJ, Nelson DE, Jensen RG. 1995. Adaptations to environmental stresses. Plant Cell 7:1099-111
12. Bowman JC. 1972. Genotype by environment interactions. Ann. Génét. Sél. Anim. 4:117-23
13. Bradshaw AD. 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13:115-55
14. Breitling R, Li Y, Tesson BM, Fu J, Wu C, et al. 2008. Genetical genomics: spotlight on QTL hotspots. PLoS Genet. 4:e1000232
15. Broman KW, Sen S. 2009. A Guide to QTL Mapping with R/qtl. New York: Springer
16. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. 2004. Epistatic interaction between the Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc. Natl. Acad. Sci. USA 101:15670-75
17. Christman MA, Richards JH, McKay JK, Stahl EA, Juenger TE, Donovan LA. 2008. Genetic variation in Arabidopsis thaliana for night-time leaf conductance. Plant Cell Environ. 31:1170-78
18. Colautti RI, Lee CR, Mitchell-Olds T. 2012. Origin, fate, and architecture of ecologically relevant genetic variation. Curr. Opin. Plant Biol. 15:199-204
19. Collins NC, Tardieu F, Tuberosa R. 2008. Quantitative trait loci and crop performance under abiotic stress: Where do we stand? Plant Physiol. 147:469-86
20. Cubillos FA, Yansouni J, Khalili H, Balzergue S, Elftieh S, et al. 2012. Expression variation in connected recombinant populations of Arabidopsis thaliana highlights distinct transcriptome architectures. BMC Genomics 13:117
21. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61:651-79
22. Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA. 2012. PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res. 40:D1194-201
23. deJong G. 1985. Phenotypic plasticity as a product of selection in a variable environment. Am. Nat. 145:493-512
24. Des Marais DL, Juenger TE. 2010. Pleiotropy, plasticity and the evolution of plant abiotic stress tolerance. Ann. N. Y. Acad. Sci. 1206:56-79
25. Des Marais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE. 2012. Physiological genomics of response to soil drying in diverse Arabidopsis accessions. Plant Cell 24:893-914
26. DeWitt TJ, Scheiner SM, eds. 2004. Phenotypic Plasticity: Functional and Conceptual Approaches. Oxford, UK: Oxford Univ. Press
27. DeWitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13:77-81
28. Drew MC, Saker LR. 1978. Nutrient supply and the growth of the seminal root system in barley. J. Exp. Bot. 29:435-51
29. Druka A, Potokina E, Luo Z, Jiang N, Chen X, et al. 2010. Expression quantitative trait loci analysis in plants. Plant Biotechnol. J. 8:10-27
30. Eberhart SA, Russell WA. 1996. Stability parameters for comparing varieties. Crop. Sci. 6:36-40
31. El-Din El-Assal S, Alonso-Blanco C, Peeters AJ, Raz V, Koornneef M. 2001. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat. Genet. 29:435-40
32. Etterson JR, Shaw RG. 2001. Constraint to adaptive evolution in response to global warming. Science 294:151-54
33. Falconer DS. 1952. The problem of environment and selection. Am. Nat. 86:293-98
34. Falconer DS, Mackay TFC. 1996. Introduction to Quantitative Genetics. Essex, UK: Addison Wesley Longman
35. Filiault DL, Wessinger CA, Dinneny JR, Lutes J, Borevitz JO, et al. 2008. Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proc. Natl. Acad. Sci. USA 105:3157-62
36. Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM. 2011. A map of local adaptation in Arabidopsis thaliana. Science 334:86-89
37. Fournier-Level A, Wilczek AM, Cooper MD, Roe JL, Anderson J, et al. 2013. Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana. Mol. Ecol. 22:3552-66
38. Fowler S, Cook D, Thomashow MF. 2007. The CBF cold-response pathway. In Plant Abiotic Stress, ed. MA Jenks, PM Hasegawa, pp. 71-99. Chichester: Blackwell
39. Franklin KA, Whitelam GC. 2005. Phytochromes and shade-avoidance responses in plants. Ann. Bot. 96:169-75
40. Fry JD. 1992. The mixed model analysis of variance applied to quantitative genetics: the biological meaning of the parameters. Evolution 46:540-50
41. Fry JD. 1993. The 'general vigor' problem: Can antagonistic pleiotropy be detected when genetic covariances are positive? Evolution 47:327-33
42. Fry JD. 1996. The evolution of host specialization: Are tradeoffs overrated? Am. Nat. 148:S84-107
43. Fry JD. 2004. Estimation of genetic variances and covariances by restricted maximum likelihood using PROC MIXED. In In Genetic Analysis of Complex Traits Using SAS, ed. AM Saxton, pp. 11-34. Cary, NC: SAS Inst.
44. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, et al. 2005. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470-88
45. Fukao T, Yeung E, Bailey-Serres J. 2011. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23:412-27
46. Gauch HG, Zobel RW. 1996. AMMI analysis of yield trials. In Genotype-by-Environment Interaction, ed. MS Kang, HG Gauch, pp. 85-122. Boca Raton, FL: CRC Press
47. Gazzani S, Gendall AR, Lister C, Dean C. 2003. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132:1107-14
48. Gibson G. 2006. Evolution: the plastic transcriptome. Curr. Biol. 16:R285-87
49. Gibson G, Weir B. 2005. The quantitative genetics of transcription. Trends Genet. 21:616-23
50. Gomulkiewicz R, Kirkpatrick M. 1992. Quantitative genetics and the evolution of reaction norms. Evolution 46:390-411
51. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ergoz ES, et al. 2009. A first generation haplotype map of maize. Science 326:1115-17
52. Gujas B, Alonso-Blanco C, Hardtke CS. 2012. Natural Arabidopsis brx loss-of-function alleles confer root adaptation to acidic soil. Curr. Biol. 22:1962-68
53. Hall MC, Lowry DB, Willis JH. 2010. Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Mol. Ecol. 19:2739-53
54. Hammond JP, Mayes S, Bowen HC, Graham NS, Hayden RM, et al. 2011. Regulatory hotspots are associated with plant gene expression under varying soil phosphorus supply in Brassica rapa. Plant Physiol. 156:1230-41
55. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK. 2006. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol. 142:98-112
56. 13C and response to differential water availability in Arabidopsis thaliana. Evolution 59:81-96
57. Hazen SP, Pathan MS, Sanchez A, Baxter I, Dunn M, et al. 2005. Expression profiling of rice segregating for drought tolerance QTLs using a rice genome array. Funct. Integr. Genomics 5:104-16
58. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76-79
59. Hereford J. 2009. A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173:579-88
60. Hodgins-Davis A, Townsend JP. 2009. Evolving gene expression: from G to E to G×E. Trends Ecol. Evol. 24:649-58
61. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, et al. 2008. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinforma. 2008:420747
62. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344-47
63. Juenger TE. 2013. Natural variation and genetic constraints on drought tolerance. Curr. Opin. Plant Biol. 16:274-81
64. Juenger TE, McKay JK, Hausmann N, Keurentjes J, Sen S, et al. 2005. Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: SC, stomatal conductance and transpiration efficiency. Plant Cell Environ. 28:697-708
65. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, et al. 2001. Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-905
66. Kawecki TJ, Ebert D. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7:1225-41
67. Kesari R, Lasky JR, Villamor JG, Des Marais DL, Chen YJ, et al. 2012. Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation. Proc. Natl. Acad. Sci. USA 109:9197-202
68. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, et al. 2007. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50:347-63
69. Kim D-H, Doyle MR, Sung S, Amasino RM. 2009. Vernalization: winter and the timing of flowering in plants. Annu. Rev. CellDev. Biol. 25:277-99
70. Kliebenstein D. 2009. Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu. Rev. Plant Biol. 60:93-114
71. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, et al. 2002. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43:1096-105
72. Lewontin RC. 1974. The analysis of variance and the analysis of causes. Am. J. Hum. Genet. 26:400-11
73. Li P, Ainsworth EA, Leakey ADB, Ulanov A, Lozovaya V, et al. 2008. Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. Plant Cell Environ. 31:1673-87
74. Li Y, Alvarez OA, Gutteling EW, Tijsterman M, Fu J, et al. 2006. Mapping determinants of gene expression plasticity by genetical genomics in C elegans. PLoS Genet. 2:e222
75. Lin HX, Yamamoto T, Sasaki T, Yano M. 2000. Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor. Appl. Genet. 101:1021-28
76. Littel RC, Milliken GA, Stroup WW, Wolfinger RD. 1996. SAS(R) System for Mixed Models. Cary, NC: SAS Inst.
77. Liu G, Zhu H, Zhang G, Li L, Ye G. 2012. Dynamic analysis of QTLs on tiller number in rice (Oryza sativa L.) with single segment substitution lines. Theor. Appl. Genet. 125:143-53
78. Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, et al. 2007. Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat. Genet. 39:896-900
79. Lovell JT, Juenger TE, Michaels SD, Lasky JR, Platt A, et al. 2013. Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation. Proc. R. Soc. Lond. Ser. B 280:20131042
80. Lowry DB, Hall MC, Salt DE, Willis JH. 2009. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. 183:776-88
81. Lynch M, Walsh B. 1998. Genetics and Analysis of Quantitative Traits. Sunderland, MA: Sinauer
82. Mackay TFC. 2001. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35:303-39
83. Maloof JN, Borevitz JO, Dabi T, Lutes J, Nehring RB, et al. 2001. Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29:441-46
84. McKay JK, Richards JH, Mitchell-Olds T. 2003. Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol. Ecol. 12:1137-51
85. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949-56
86. Mittler R, Blumwald E. 2010. Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 61:443-62
87. Mouchel CF, Briggs GC, Hardtke CS. 2004. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev. 18:700-14
88. Nordborg M, Bergelson J. 1999. The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. Am. J. Bot. 86:470-75
89. Nunez-Farfan J, Schlichting CD. 2001. Evolution in changing environments: the "synthetic" work of Clausen, Keck, and Heisey. Q. Rev. Biol. 76:433-57
90. Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, et al. 1991. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics 127:181-97
91. Peach C, Velten J. 1991. Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol. Biol. 17:49-60
92. Pigliucci M. 2001. Phenotypic Plasticity: Beyond Nature and Nurture. Baltimore, MD: The Johns Hopkins Univ. Press
93. Ren Z, Zheng Z, Chinnusamy V, Zhu J, Cui X, et al. 2010. RAS1, a quantitative trait locus for salt tolerance and ABA sensitivity in Arabidopsis. Proc. Natl. Acad. Sci. USA 107:5669-74
94. Rengel D, Arribat S, Maury P, Martin-Magniette ML, Hourlier T, et al. 2012. A gene-phenotype network based on genetic variability for drought responses reveals key physiological processes in controlled and natural environments. PLoS One 7:e45249
95. Richards CL, Rosas U, Banta J, Bhambhra N, Purugganan MD. 2012. Genome-wide patterns of Arabidopsis gene expression in nature. PLoS Genet. 8:e1002662
96. Robinson MR, Beckerman AP. 2013. Quantifying multivariate plasticity: Genetic variation in resource acquisition drives plasticity in resource allocation to components of life history. Ecol. Lett. 16:281-90
97. Rockman MV. 2012. The QTN program and the alleles that matter for evolution: All that's gold does not glitter. Evolution 66:1-17
98. Sabadin PK, Malosetti M, Boer MP, Tardin FD, Santos FG, et al. 2012. Studying the genetic basis of drought tolerance in sorghum by managed stress trials and adjustments for phenological and plant height differences. Theor. Appl. Genet. 124:1-14
99. Schaefer LR, Jamrozik J. 2008. Random regression models: a longitudinal perspective. J. Anim. Breed. Genet. 125:145-46
100. Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24:35-68
101. Schlichting CD. 1986. The evolution of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst. 17:667-93
102. Schwartz C, Balasubramanian S, Warthmann N, Michael TP, Lempe J, et al. 2009. Cis-regulatory changes at FLOWERING LOCUS T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183:723-32
103. Sheldon CC, Conn AB, Dennis ES, Peacock WJ. 2002. Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527-37
104. Shindo C, Bernasconi G, Hardtke CS. 2008. Intraspecific competition reveals conditional fitness effects of single gene polymorphism at the Arabidopsis root growth regulator BRX. New Phytol. 180:71-80
105. Smith EN, Kruglyak L. 2008. Gene-environment interaction in yeast gene expression. PLoS Biol. 6:e83
106. Smith H. 1990. Signal perception, differential expression within multigene families and the molecular basis of phenotypic plasticity. Plant Cell Environ. 13:585-94
107. Stamatoyannopoulos J. 2004. The genomics of gene expression. Genomics 84:449-57
108. Stinchcombe JR, Function-valued Traits Work. Group, Kirkpatrick M. 2012. Genetics and evolution of function-valued traits: understanding environmentally responsive phenotypes. Trends Ecol. Evol. 27:637-47
109. Street NR, Skogström O, Sjödin A, Tucker J, Rodriguez-Acosta M, et al. 2006. The genetics and genomics of the drought response in Populus. Plant J. 48:312-41
110. Sultan S, Spencer H. 2002. Metapopulation structure favors plasticity over local adaptation. Am. Nat. 160:271-83
111. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R. 2008. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J. Biol. Chem. 283:9269-75
112. Swanson-Wagner RA, DeCook R, Jia Y, Bancroft T, Ji T, et al. 2009. Paternal dominance of trans-eQTL influences gene expression patterns in maize hybrids. Science 326:1118-20
113. Swindell WR, Huebner M, Weber AP. 2007. Plastic and adaptive gene expression patterns associated with temperature stress in Arabidopsis thaliana. Heredity 99:143-50
114. Tomlinson KW, O'Connor TG. 2004. Control of tiller recruitment in bunchgrasses: uniting physiology and ecology. Funct. Ecol. 18:489-96
115. Tonsor SJ, Scott C, Boumaza I, Liss TR, Brodsky JL, Vierling E. 2008. Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Mol. Ecol. 17:1614-26
116. Turner A, Beales J, Faure S, Dunford RP, Laurie DA. 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031-34
117. Ungerer MC, Halldorsdottir SS, Purugganan MD, Mackay TFC. 2003. Genotype-environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics 165:353-65
118. van Eeuwijk FA, Bink MC, Chenu K, Chapman SC. 2010. Detection and use of QTL for complex traits in multiple environments. Curr. Opin. Plant Biol. 13:193-205
119. van Kleunen M, Fischer M. 2005. Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol. 166:49-60
120. van Tienderen PH. 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317-31
121. Via S. 1993. Control of phenotypic plasticity via regulatory genes. Am. Nat. 142:366-70
122. Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10:212-17
123. Via S, Lande R. 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505-23
124. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF. 2005. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 41:195-211
125. Wahlsten D. 1990. Insensitivity of the analysis of variance to heredity-environment interaction. Behav. Brain Sci. 13:109-61
126. Walsh B, Blows MW. 2009. Abundant genetic variation + strong selection = multivariate genetic constraints: A geometric view of adaptation. Annu. Rev. Ecol. Evol. Syst. 40:41-59
127. Wang J, Yu H, Xie W, Xing Y, Yu S, et al. 2010. A global analysis of QTLs for expression variations in rice shoots at the early seedling state. Plant J. 63:1063-74
128. West MA, Kim K, Kliebenstein DJ, van Leeuwen H, Michelmore RW, et al. 2007. Global eQTL mapping reveals the complex genetic architecture of transcript-level variation in Arabidopsis. Genetics 175:1441-50
129. Windig JJ, de Kovel CGF, de Jong G. 2004. Genetics and mechanics of plasticity. See DeWitt & Scheiner 2004, pp. 31-49
130. Xiong H, Goulding EH, Carlson EJ, Tecott LH, McColloch CE, Sen S. 2011. A flexible estimating equations approach for mapping function-valued traits. Genetics 189:305-16
131. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, et al. 2006. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705-8
132. Yan L, Fu D, Li C, Blechl A, Tranquilli G, et al. 2006. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. USA 103:19581-86
133. Yan W, Kang MS. 2003. GGE Biplot Analysis: A Graphical Tool for Breeders, Geneticists, and Agronomists. Boca Raton, FL: CRC Press
134. Yano M, Katayosea Y, Ashikarib M, Yamanouchic U, Monnac L, et al. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene Constans. Plant Cell 12:2473-83
135. Yoshioka K, Shinozaki K, eds. 2009. Signal Cross Talk in Plant Stress Response. Ames, IA: Wiley-Blackwell
136. Zhou S, Campbell TG, Stone EA, Mackay TFC, Anholt RRH. 2012. Phenotypic plasticity of the Drosophila transcriptome. PLoS Genet. 8:e1002593
137. Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, et al. 2011. Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 108:14992-97