Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Flowering time control: gene network modelling and the link to quantitative genetics

Stephen M. Welch A E , Zhanshan Dong A B , Judith L. Roe C and Sanjoy Das D
+ Author Affiliations
- Author Affiliations

A Department of Agronomy, Kansas State University, Manhattan, KS 66506, USA.

B Current address: Pioneer Hi-Bred International, Inc., 7300 NW 62nd Ave, Johnston, IA 50131, USA.

C Division of Biology, Kansas State University, Manhattan, KS 66506, USA.

D Department of Electrical and Computer Engineering, Kansas State University, Manhattan, KS 66506, USA.

E Corresponding author. Email: welchsm@ksu.edu

Australian Journal of Agricultural Research 56(9) 919-936 https://doi.org/10.1071/AR05155
Submitted: 9 May 2005  Accepted: 20 June 2005   Published: 28 September 2005

Abstract

Flowering is a key stage in plant development that initiates grain production and is vulnerable to stress. The genes controlling flowering time in the model plant Arabidopsis thaliana are reviewed. Interactions between these genes have been described previously by qualitative network diagrams. We mathematically relate environmentally dependent transcription, RNA processing, translation, and protein–protein interaction rates to resultant phenotypes. We have developed models (reported elsewhere) based on these concepts that simulate flowering times for novel A. thaliana genotype–environment combinations. Here we draw 12 contrasts between genetic network (GN) models of this type and quantitative genetics (QG), showing that both have equal contributions to make to an ideal theory. Physiological dominance and additivity are examined as emergent properties in the context of feed-forwards networks, an instance of which is the signal-integration portion of the A. thaliana flowering time network. Additivity is seen to be a complex, multi-gene property with contributions from mass balance in transcript production, the feed-forwards structure itself, and downstream promoter reaction thermodynamics. Higher level emergent properties are exemplified by critical short daylength (CSDL), which we relate to gene expression dynamics in rice (Oryza sativa). Next to be discussed are synergies between QG and GN relating to the quantitative trait locus (QTL) mapping of model coefficients. This suggests a new verification test useful in GN model development and in identifying needed updates to existing crop models. Finally, the utility of simple models is evinced by 80 years of QG theory and mathematical ecology.

Additional keywords: regulation, differential equations, photothermal, pathways.


Acknowledgments

An earlier version of this work is in the published Proceedings of the 4th International Crop Science Congress (26 September–4 October 2004, Brisbane, Australia). The Congress organisers kindly gave their permission to publish this updated version, for which we are grateful. We also benefited from the inputs of Mark Cooper and Graeme Hammer; open discussions with other authors in this Special Issue, especially Francois Tardieu; and comments from anonymous reviewers. This work was supported in part by NSF Projects 32115 and 0425759, USDA Project 2003–35304–13217, and Hatch Project KAES 0507, all at Kansas State University. This is Contribution No. 05-191-J from the Kansas Agricultural Experiment Station.


References


Akutsu T, Miyano S, Kuhara S (1999) Identification of genetic networks from a small number of gene expression patterns under the boolean network model. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Akutsu T, Miyano S, Kuhara S (2000) Inferring qualitative relations in genetic networks and metabolic pathways. Bioinformatics 16, 727–734.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Alabadi D, Oyama T, Yanovsky M, Harmon F, Mas P, Kay S (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880–883.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Auckerman M, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell 15, 2730–2741.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nature Genetics 36, 162–166.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bagnall D, King R, Whitelam G, Boylan M, Wagner D, Quail P (1995) Flowering responses to altered expression of phytochrome in mutants and transgenic lines of Arabidopsis thaliana (L.) Heynh. Plant Physiology 108, 1495–1503.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baldi, P ,  and  Hatfield, G (2002). ‘DNA microarrays and gene expression.’ (Cambridge University Press: Cambridge, UK)

Barash Y, Friedman N (2001) Context specific bayesian clustering for gene expression data. ‘Proceedings of the 5th Annual International Conference on Computational Molecular Biology RECOMB-2001’. 2–11..


Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blazquez M (2000) Flower development pathways. Journal of Cell Science 113, 3547–3548.
PubMed |
open url image1

Blazquez MA, Ahn J, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana.  Nature Genetics 33, 168–171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blazquez M, Green T, Nilsson O, Sussman M, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. The Plant Cell 10, 791–800.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blazquez M, Koornneef M, Putterill J (2001) Flowering on time: genes that regulate the floral transition. EMBO Reports 2, 1078–1082.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blazquez M, Trenor M, Weigel D (2002) Independent control of gibberellin biosynthesis and flowering time by the circadian clock in Arabidopsis.  Plant Physiology 130, 1770–1775.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blazquez M, Weigel D (1999) Independent regulation of flowering by phytochrome B and gibberellins in Arabidopsis.  Plant Physiology 120, 1025–1032.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bolouri H, Davidson EH (2003) Transcriptional regulatory cascades in development: initial rates, not steady state, determine network kinetics. Proceedings of the National Academy of Sciences of the United States of America 100, 9371–9376.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boote K, Jones J, Batchelor W, Nafziger E, Myers O (2003) Genetic coefficients in the CROPGRO-Soybean model: links to field performance and genomics. Agronomy Journal 95, 32–51. open url image1

Boss PK, Bastow RM, Mylned JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. The Plant Cell 16, S18–S31.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bowman J, Alvarez J, Weigel D, Meyerowitz E, Smyth D (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721–743. open url image1

Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis.  Science 275, 80–83.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bunning E (1936) Die endonome tagesrhythmik als grundlage der photoperiodischen reaktion. Berichte der Deutschen Botanischen Gesellschaft 54, 590–607. open url image1

Burd C, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615–621.
PubMed |
open url image1

Campos H, Cooper M, Habben JE, Edmeades GO, Schussler JR (2004) Improving drought tolerance in maize: a view from industry. Field Crops Research 90, 19–34.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carre I (2001) Daylength perception and the photoperiodic regulation of flowering in Arabidopsis.  Journal of Biological Rhythms 16, 415–423.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Carrington J, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301, 336–338.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chandler J, Wilson A, Dean C (1996) Arabidopsis mutants showing an altered response to vernalization. The Plant Journal 10, 637–644.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen T, He H, Church G (1999) Modeling gene expressions with differential equations. ‘Proceedings of Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Cheverud JM, Routman EJ (1995) Epistasis and its contribution to genetic variance components. Genetics 139, 1455–1461.
PubMed |
open url image1

Chou M, Haung M, Yang C (2001) EMF genes interact with late-flowering genes in regulating floral initiation genes during shoot development in Arabidopsis thaliana.  Plant and Cell Physiology 42, 499–507.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Comai L, Harada JJ (1990) Transcriptional activities in dry seed nuclei indicate the timing of the transition from embryogeny to germination. Proceedings of the National Academy of Sciences of the United States of America 87, 2671–2674.
PubMed |
open url image1

Cooper M, Chapman S, Podlich DW, Hammer GL (2002) The GP problem: quantifying gene-to-phenotype relationships. In Silico Biology 2, 151–164.
PubMed |
open url image1

Cooper M, Podlich DW, Smith OS (2005) Gene-to-phenotype models and complex trait genetics. Australian Journal of Agricultural Research 56, 895–918. open url image1

CRC (1996). ‘Standard mathematical tables and formula.’ (CRC Press: Boca Raton, FL)

D’Haesseleer P, Wen X, Fuhrman S, Somogyi R (1999) Linear modeling of mRNA expression levels during CNS development and injury. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C , et al . (2002) A genomic regulatory network for development. Science 295, 1669–1678.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Davis S (2002) Photoperiodism: the coincidental perception of the season. Current Biology 12, R841–R843.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Devlin P (2002) Signs of the time: environmental input to the circadian clock. Journal of Experimental Botany 53, 1535–1550.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dong Z (2003) Incorporation of genomic information into the simulation of flowering time in Arabidopsis thaliana. PhD dissertation, Kansas State University, USA. ( : )

Dubnau J, Struhl G (1996) RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694–699.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eriksson M, Millar A (2003) The circadian clock. A plant’s best friend in a spinning world. Plant Physiology 132, 732–738.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER (2004) A gene regulatory network for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. The Plant Cell 16, 2923–2939.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER.  Development 127, 725–734.
PubMed |
open url image1

Fisher R (1918) The correlation between relatives on the supposition of Mendelian inheritance. Transactions of the Royal Society Edinburgh 52, 399–433. open url image1

Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulated photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. The EMBO Journal 18, 4679–4688.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Frank S (1999) Population and quantitative genetics of regulatory networks. Journal of Theoretical Biology 197, 281–294.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Friedman N, Linial M, Nachman I, Pe’er D (2000) Using Bayesian networks to analyze expression data. Journal of Computational Biology 7, 601–620.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gendall A, Levy Y, Wilson A, Dean C (2001) The VERNALIZATION2 gene mediates the epigenetic regulation of vernalization in Arabidopsis.  Cell 107, 525–535.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Goff SA, Ricke D, Lan T, Presting G, Wang R , et al . (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Goss P, Peccoud J (1999) Analysis of the stabilizing effect of Rom on the genetic network controlling ColE1 plasmid replication. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Goto N, Kumagai T, Koornneef M (1991) Flowering responses to lightbreaks in photomorphogenic mutants of Arabidopsis thaliana, a long-day plant. Physiologia Plantarum 83, 209–215.
Crossref | GoogleScholarGoogle Scholar | open url image1

Guo H, Yang H, Mocker T, Lin C (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science 279, 1360–1363.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Halliday K, Salter M, Thingnaes E, Whitelam G (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT.  The Plant Journal 33, 875–885.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hammer GL, Chapman S, van Oosterom E, Podlich DW (2005) Trait physiology and crop modelling as a framework to link phenotypic complexity to underlying genetic systems. Australian Journal of Agricultural Research 56, 947–960. open url image1

Hammes, GG (2000). ‘Thermodynamics and kinetics for the biological sciences.’ (Wiley-Interscience: New York)

Hanks, J ,  and  Ritchie, J (Eds) (1991). ‘Modeling plant and soil systems.’ (ASA, CSSA, and SSSA: Madison, WI)

Hartemink A, Gifford D, Jaakkola T, Young R (2001) Using graphical models and genomic expression data to statistically validate models of genetic regulatory networks. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Haughn G, Schultz E, Martinez-Zapater T (1995) The regulation of flowering in Arabidopsis thaliana: meristems, morphogenesis, and mutants. Canadian Journal of Botany 73, 959–981. open url image1

Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Current Opinion in Plant Biology 6, 13–19.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis.  Science 302, 1751–1754.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hempel F, Weigel D, Mandel M, Ditta G, Zambryski P, Feldman L, Yanofsky M (1997) Floral determination and expression of floral regulatory genes in Arabidopsis.  Development 124, 3845–3853.
PubMed |
open url image1

Hepworth S, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. The EMBO Journal 21, 4327–4337.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hudson M (2000) The genetics of phytochrome signaling in Arabidopsis.  Seminars in Cell and Developmental Biology 11, 475–483.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huq E, Tepperman J, Quail P (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis.  Proceedings of the National Academy of Sciences of the United States of America 97, 9789–9794.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ideker T, Thorsson V, Karp R (2000) Discovery of regulatory interactions through perturbation: inference and experimental design. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Irmak A, Jones J, Mavromatis T, Welch S, Boote K, Wilkerson G (2000) Evaluating methods for simulating soybean cultivar responses using cross validation. Agronomy Journal 92, 1140–1149. open url image1

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, 344–347.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Johnson C (2001) Endogenous timekeepers in photosynthetic organisms. Annual Review of Physiology 63, 695–728.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis.  Plant Physiology 105, 141–149.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kardailsky I, Shakla V, Ahn J, Dagenais N, Christensen S, Nguyen J, Chory J, Harrison M, Weigel D (1999) Activation tagging of the floral inducer FT.  Science 286, 1962–1965.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kauffman, S (1993). ‘The origins of order: self-organization and selection in evolution.’ (Oxford University Press: Oxford, UK)

Kauffman S, Peterson C, Samuelsson B, Troein C (2003) Random Boolean network models and the yeast transcriptional network. Proceedings of the National Academy of Sciences of the United States of America 100, 14796–14799.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kauffman S, Peterson C, Samuelsson B, Troein C (2004) Genetic networks with canalyzing Boolean rules are always stable. Proceedings of the National Academy of Sciences of the United States of America 101, 17102–17107.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kenzior AL, Folk WR (1998) AtMSI4 and RbAp48 WD-40 repeat proteins bind metal ions. FEBS Letters 440, 425–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kingston R, Narlikar G (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes and Development 13, 2339–2352.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araaki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant and Cell Physiology 43, 1096–1105.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koornneef M, Hanhart C, van der Veen J (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana.  Molecular and General Genetics 229, 57–66.
PubMed |
open url image1

Kot, M (2001). ‘Elements of mathematical ecology.’ (Cambridge University Press: Cambridge, UK)

Kurata H, Taira K (2000) Two-phase partition method for simulating a biological system at extremely high speed. General Bioinformatics 11, 185–195. open url image1

Lamb R, Hill T, Tan Q, Irish V (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129, 2079–2086.
PubMed |
open url image1

Lee I, Aukerman M, Gore S, Lohman K, Michaels S, Weaver L, John M, Feldmann K, Amasino R (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis.  The Plant Cell 6, 75–83.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee S, Cheng H, King K, Wang W, He Y, Hussain A, Lo J, Harberd N, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes and Development 16, 646–658.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Levy Y, Dean C (1998) The transition to flowering. The Plant Cell 10, 1973–1989.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Levy Y, Mesnage S, Mylne J, Gendall R, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–247.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liang S, Fuhrman S, Somogyi R (1998) REVEAL: A general reverse engineering algorithm for inference of genetic network architecture. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing CO.: Singapore)


Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta G, Yanofsky M (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. The Plant Cell 11, 1007–1018.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lin C (2000) Photoreceptors and regulation of flowering time. Plant Physiology 123, 39–50.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lotka, A (1925). ‘Elements of physical biology.’ (Williams and Wilkins Co.: Baltimore, MD)

Lynch, M ,  and  Walsh, B (1998). ‘Genetics and analysis of quantitative traits.’ (Sinauer Associates, Inc.: Sunderland, MA)

Ma CX, Casella G, Wu RL (2002) Functional mapping of quantitative trait loci underlying the character process: a theoretical framework. Genetics 161, 1751–1762.
PubMed |
open url image1

Ma CX, Wu R, Casella G (2004) FunMap: functional mapping of complex traits. Bioinformatics 20, 1808–1811.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Macknight R, Bancroft I, Page T, Lister C, Schmidt R , et al . (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737–745.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002) Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA.  The Plant Cell 14, 877–888.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Maki Y, Tominaga D, Okamoto M, Watanabe S, Eguchi Y (2001) Development of a system for the inference of large-scale genetic networks. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing CO.: Singapore)


Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T (2000) Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana.  Plant and Cell Physiology 41, 791–803.
PubMed |
open url image1

Makino S, Matsushika A, Kojima M, Oda Y, Mizuno T (2001) Light response of the circadian waves of the APRR1/TOC1 quintet: When does the quintet start singing rhythmically in Arabidopsis?  Plant and Cell Physiology 42, 334–339.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Makino S, Matsushika A, Kojima M, Yamashino T, Mizuno T (2002) The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. characterization with APRR1-overexpressing plants. Plant and Cell Physiology 43, 58–69.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Alejandra Mandel M, Gustafson-Brown C, Savidge B, Yanofsky M (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1.  Nature 360, 273–277.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Marnellos G, Deblandre G, Mjolsness E, Kintner C (2000) Delta-notch lateral inhibitory patterning in the emergence of ciliated cells in Xenopus: experimental observations and a gene network model. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Martínez-Zapater JM, Coupland G, Dean C, Koornneef M (1994) The transition to flowering in Arabidopsis. ‘’. (Eds E Meyerowitz, C Somerville) pp. 403–433. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY)

Martínez-Zapater JM, Jarillo J, Cruz-Alvarez M, Roldán M, Salinas J (1995) Arabidopsis late-flowering fve mutants are affected in both vegetative and reproductive development. The Plant Journal 7, 543–551.
Crossref | GoogleScholarGoogle Scholar | open url image1

Martínez-Zapater JM, Somerville C (1990) Effect of light quality and vernalization on late-flowering mutants of Arabidopsis thaliana.  Plant Physiology 92, 770–776. open url image1

Matsuno H, Doi A, Nagasaki M, Miyano S (2000) Hybrid Petri net representation of gene regulatory network. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Matsushika A, Imamura A, Yamashino T, Mizuno T (2002a) Aberrant expression of the light-inducible and circadian-regulated APRR9 gene belonging to the circadian-associated APRR1/TOC1 quintet results in the phenotype of early flowering in Arabidopsis thaliana.  Plant and Cell Physiology 43, 833–843.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Matsushika A, Makino S, Kojima M, Mizuno T (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis.  Plant and Cell Physiology 41, 1002–1012.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Matsushika A, Makino S, Kojima M, Yamashino T, Mizuno T (2002b) The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: II. Characterization with CCA1-overexpressing plants. Plant and Cell Physiology 43, 118–122.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McClung C (2001) Circadian rhythms in plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 139–162.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McCown RL, Hochman Z, Carberry P (2002) Probing the enigma of decision support systems for farmers: learning from experience and from theory. Agricultural Systems 74, 1–10.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mendoza L, Alvarez-Buylla E (1998) Dynamics of the genetic regulatory network for Arabidopsis thaliana flower morphogenesis. Journal of Theoretical Biology 193, 307–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mendoza L, Alvarez-Buylla E (2000) Genetic regulation of root hair development in Arabidopsis thaliana: a network model. Journal of Theoretical Biology 204, 311–326.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Michaels S, Amasino R (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts a repressor of flowering. The Plant Cell 11, 949–956.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Michaels S, He Y, Scortecci K, Amasino R (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 of the United States of America 100, 10102–10107.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Millar A (1999) Biological clocks in Arabidopsis thaliana.  New Phytologist 141, 175–197.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mockler T, Guo H, Yang H, Duong H, Lin C (1999) Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 126, 2073–2082.
PubMed |
open url image1

Moon J, Suh SS, Lee H, Choi KR, Hong C, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis.  The Plant Journal 35, 613–623.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: integrating pathways as a basis for diversity. The Plant Cell 14, S111–S130.
PubMed |
open url image1

Murakami-Kojima M, Nakamichi N, Yamashino T, Mizuno T (2002) The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana.  Plant and Cell Physiology 43, 675–683.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ng M, Yanofsky M (2001) Activation of the Arabidopsis B class homeotic genes by APETALA1.  The Plant Cell 13, 739–753.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Omholt SW, Plahte E, Oyehaug L, Xiang K (2000) Gene regulatory networks generating the phenomena of additivity, dominance and epistasis. Genetics 155, 969–980.
PubMed |
open url image1

Parcy F, Bomblies K, Weigel D (2002) Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral mersitem identity in Arabidopsis. Development 129, 2519–2527.
PubMed |
open url image1

Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395, 561–566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Park D, Somers D, Kim Y, Choy Y, Lim H, Soh M, Kim H, Kay S, Nam H (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579–1582.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana.  Current Biology 12, 1484–1495.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peng J, Carol P, Richards D, King K, Cowling R, Murphy G, Harberd N (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes and Development 113, 194–207. open url image1

Pittendrigh C (1972) Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proceedings of the National Academy of Sciences of the United States of America 69, 2734–2737.
PubMed |
open url image1

Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847–857.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quesada V, Macknight R, Dean C, Simpson G (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. The EMBO Journal 22, 3142–3152.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis.  Development 126, 1109–1120.
PubMed |
open url image1

Reed J, Nagpal P, Poo1e D, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. The Plant Cell 5, 147–157.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reeves P, Coupland G (2000) Response of plant development to environment: control of flowering by daylength and temperature. Current Opinion in Plant Biology 3, 37–42.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reeves P, Coupland G (2001) Analysis of flowering time control in Arabidopsis by comparison of double and triple mutants. Plant Physiology 126, 1085–1091.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reinitz J, Sharp D (1995) Mechanism of eve stripe formation. Mechanisms of Development 49, 133–158.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reymond M, Muller B, Leonardi A, Charcosset A, Tardieu F (2003) Combining quantitative trait loci analysis and an ecophysiological model to analyze the genetic variability of the responses of maize leaf growth to temperature and water deficit. Plant Physiology 131, 664–675.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Richards FJ (1959) A flexible growth function for empirical use. Journal of Experimental Botany 10, 290–300. open url image1

Roden L, Song H, Jackson S, Morris K, Carre I (2002) Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis.  Proceedings of the National Academy of Sciences of the United States of America 99, 13313–13318.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rosenzweig C, Philips J, Goldberg R, Carroll J, Hodges T (1996) Potential impacts of climate change on citrus and potato production in the US. Agricultural Systems 52, 455–479.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rouse DT, Sheldon C, Bagnall D, Peacock W, Dennis E (2002) FLC, a repressor of flowering, is regulated by genes in different inductive pathways. The Plant Journal 29, 183–191.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruiz-Garcia L, Madueno F, Wilkinson M, Haughn G, Salinas J, Martinez-Zapater J (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis.  The Plant Cell 9, 1921–1934.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Salk Institute (2000) Functional genomics and the virtual plant: a blueprint for understanding how plants are built and how to improve them. NSF Workshop Report, The Arabidopsis Information Resource (TAIR).

Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. BioEssays 22, 38–47.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Samach A, Gover A (2001) Photoperiodism: the consistent use of CONSTANS.  Current Biology 11, R651–R654.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Samach A, Onouchi H, Gold S, Ditta S, Schwarz-Sommer Z, Yanofsky F, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis.  Science 288, 1613–1616.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Samsonova M, Serov V (1999) NetWork: An interactive interface to the tools for analysis of genetic network structure and dynamics. ‘Proceedings of Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Schmid M, Uhlenhaut N, Godard F, Demar M, Bressan R, Weigel D, Lohmann J (2003) Dissection of floral induction pathways using global expression analysis. Development 130, 6001–6012.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schomburg F, Patton D, Meinke D, Amasino R (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. The Plant Cell 13, 1427–1436.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sheldon C, Burn J, Perez P, Metzger J, Edwards J, Peacock J, Dennis E (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. The Plant Cell 11, 445–458.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sheldon C, Rouse D, Finnegan E, Peacock W, Dennis E (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC).  Proceedings of the National Academy of Sciences of the United States of America 97, 3753–3758.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shimamoto K, Kyozuka J (2002) Rice as a model for comparative genomics of plants. Annual Review of Plant Biology 53, 399–419.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Silverstone A, Ciampaglio C, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. The Plant Cell 10, 155–169.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Silverstone A, Mak P, Martinez E, Sun T (1997) The RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana.  Genetics 146, 1087–1099.
PubMed |
open url image1

Simon R, Igeno MI, Coupland G (1996) Activation of floral meristem identity genes in Arabidopsis.  Nature 384, 59–62.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time? Science 296, 285–289.
Crossref | PubMed |
open url image1

Simpson G, Dijkwel P, Quesada V, Henderson I, Dean C (2003) FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113, 777–787.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Simpson G, Gendall A, Dean C (1999) When to switch to flowering. Annual Review of Cell and Developmental Biology 15, 519–550.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith H (2000) Phytochromes and light signal perception by plants — an emerging synthesis. Nature 407, 585–591.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Somers D (1999) The physiology and molecular bases of the plant circadian clock. Plant Physiology 121, 9–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stewart D, Cober E, Bernard R (2003) Modeling genetic effects on the photothermal response of soybean phenological development. Agronomy Journal 95, 65–70. open url image1

Stormo GD, Fields DS (1998) Specificity, free energy, and information content in protein-DNA interactions. Trends in Biochemical Sciences 23, 109–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.  Nature 410, 1116–1120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sung Z, Chen L, Moon YH, Lertpiriyapong K (2003) Mechanisms of floral repression in Arabidopsis.  Current Opinion in Plant Biology 6, 29–35.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Szallasi Z, Liang S (1998) Modeling the normal and neoplastic cell cycle with realistic boolean genetic networks: their application for understanding carcinogenesis and assessing therapeutic strategies. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Tardieu F (2003) Virtual plants: modeling as a tool for the genomics of tolerance to water deficit. Trends in Plant Science 8, 9–14.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tardieu F, Reymond M, Muller B, Granier C, Simonneau T, Sadok W, Welcker C (2005) Linking physiological and genetic analyses of the control of leaf growth under changing environmental conditions. Australian Journal of Agricultural Research 56, 937–946. open url image1

Tominaga D, Okamoto M, Maki Y, Watanabe S, Eguchi Y (1999) Nonlinear numerical optimization technique based on genetic algorithm for inverse problem: towards the inference of genetic networks. ‘Proceedings of the German Conference on Bioinformatics. GCB ’99’. 4–6 October 1999, Vol 4.. (Ed.  R Giegerich , R Hofestädt , T Lengauer , W Mewes , D Schomburg , M Vingron , E Wingender ) pp. 127–140. (GBF-Braunschweig and University of Bielefeld: Hanover, Germany)


Tsuji, G , Uehara, G ,  and  Balas, S (Eds) (1994). ‘DSSAT version 3: A decision support system for agrotechnology transfer (3 volumes).’ (University of Hawaii: Honolulu, HI)

Tubiello F, Rosenzweig C, Kimball B, Pinter P, Wall G, Hunsaker D, LaMorte R, Garcia R (1999) Testing CERES-wheat with free-air carbon dioxide enrichment (FACE) experiment data: CO2 and water interactions. Agronomy Journal 91, 247–255. open url image1

van Eeuwijk FA, Malosetti M, Yin X, Struik PC, Stam P (2005) Statistical models for genotype by environment data: From conventional ANOVA to eco-physiological QTL models. Australian Journal of Agricultural Research 56, 883–894. open url image1

von Bertalanffy L (1957) Quantitative laws for metabolism and growth. The Quarterly Review of Biology 32, 217–231.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wagner D, Sablowski R, Meyerowitz E (1999) Transcriptional activation of APETALA1 by LEAFY.  Science 285, 582–584.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Walsh B (2001) Quantitative genetics, genomics, and the future of plant breeding. ‘Quantitative genetics, genomics, and plant breeding’. (Ed. M Kang) pp. 23–32. (CAB International)

Walsh B (2005) The struggle to exploit non-additive variation. Australian Journal of Agricultural Research 56, 873–881. open url image1

Wang H, Elston T, Mogliner A, Oster G (1998) Force generation in RNA polymerase. Biophysical Journal 74, 1186–1202.
PubMed |
open url image1

Weaver D, Workman C, Stormo G (1999) Modeling regulatory network with weight matrices. ‘Proceedings of the Pacific Symposium on Biocomputing’. (World Publishing Co.: Singapore)


Weigel D, Alvarez J, Smyth D, Yanofsky M, Meyerowitz E (1992) LEAFY controls floral meristem identity in Arabidopsis.  Cell 69, 843–859.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377, 495–500.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weigel D, Meyerowitz EM (1993) Activation of floral homeotic genes in Arabidopsis. Science 261, 1723–1726. open url image1

Welch S, Roe J, Das S, Dong Z, He R, Kirkham M (2005) Merging genomic control networks and soil-plant-atmosphere-continuum (SPAC) models. Agricultural Systems , open url image1

Welch SM, Roe J, Dong Z (2003) A genetic neural network model of flowering time control in Arabidopsis thaliana. Agronomy Journal 95, 71–81. open url image1

Welch SM, Wilkerson G, Whiting K, Sun N, Vagts T, Buol G, Mavromatis T (2002) Estimating soybean model genetic coefficients from private-sector variety performance trial data. Transactions of the American Society of Agricultural Engineers 45, 1163–1175. open url image1

Welch SM, Zhang J, Sun N, Mak TY (2000) Efficient estimation of genetic coefficients for crop models. ‘Proceedings of the Third International Symposium Systems Approaches for Agricultural Development’. CD-ROM computer file.. (Ed. W Bowen ) (International Potato Center (CIP: Lima, Peru)


White J, Hoogenboom G (1996) Simulating effects of genes for physiological traits in a process-oriented crop model. Agronomy Journal 88, 416–422. open url image1

White JW, McMaster GS, Edmeades GO (2004) Linking functional genomics and physiology for global change research. Field Crops Research 90, 1–170.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wolf D, Eeckman F (1998) On the relationship between genomic regulatory element organization and gene regulatory dynamics. Journal of Theoretical Biology 195, 167–186.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wright S (1921a) Correlation and causation. Journal of Agricultural Research 20, 557–585. open url image1

Wright S (1921b) Systems of mating. I. The biometric relations between parents and offspring. Genetics 6, 111–123. open url image1

Wright S (1921c) Systems of mating. II. The effects of inbreeding on the genetic composition of a population. Genetics 6, 124–143. open url image1

Wright S (1921d) Systems of mating. III. The biometric relations between parents and offspring. Genetics 6, 144–161. open url image1

Wu W, Zhou Y, Li W, Mao D, Chen Q (2002) Mapping of quantitative trait loci based on growth models. Theoretical and Applied Genetics 105, 1043–1049.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T (2001) Genetic control of flowering time in rice, a short-day plant. Plant Physiology 127, 1425–1429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yanovsky M, Kay S (2002) Molecular basis of seasonal time measurement in Arabidopsis.  Nature 419, 308–312.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yin X, Chasalow S, Dourleijn C, Stam P, Kropff M (2000) Coupling estimated effects of QTLs for physiological traits to a crop growth model: predicting yield variation among recombinant inbred lines in barley. Heredity 85, 539–549.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yin X, Kropff M, McLaren G, Visperas R (1995) A nonlinear model for crop development as a function of temperature. Agricultural and Forest Meteorology 77, 1–16.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yin X, Kropff M, Nakagawa H, Horie T, Goudriaan J (1997) A model for photothermal responses of flowering in rice I. Model evaluation. Field Crops Research 51, 201–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yin X, Kropff M, Stam P (1999a) The role of ecophysiological models in QTL analysis: the example of specific leaf area in barley. Heredity 82, 415–421.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yin X, Stam P, Dourleijn C, Kropff M (1999b) AFLP mapping of quantitative trait loci for yield determining physiological characters in spring barley. Theoretical and Applied Genetics 99, 244–253.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yu H, Xu Y, Tan E, Kumar P (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proceedings of the National Academy of Sciences of the United States of America 99, 16336–16341.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao W, Wu R, Ma C, Casella G (2004a) A fast algorithm for functional mapping of complex traits. Genetics 167, 2133–2137.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao W, Zhu J, Gallo-Meagher M, Wu R (2004b) A unified statistical model for functional mapping of environment-dependent genetic expression and genotype×Environment interactions for ontogenetic development. Genetics 168, 1751–1762.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1