The Genetic Architecture of Flowering Time and Photoperiod Sensitivity in Maize as Revealed by QTL Review and Meta Analysis

Journal of Integrative Plant Biology

Volumn 54, Issue 6, 2012, Pages 358-373

  Xu, Jie ^a,b   Liu, Yaxi ^a   Liu, Jian ^a,b   Cao, Moju ^a,b   Wang, Jing ^a,b   Lan, Hai ^a,b   Xu, Yunbi ^c,d   Lu, Yanli ^a,b   Pan, Guangtang ^a,b   Rong, Tingzhao ^a,b  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

Author keywords

Consensus quantitative trait loci (cQTL); Flowering time; Maize; Meta analysis; Molecular breeding; Photoperiod sensitivity

Indexed keywords

ADAPTATION; FLOWERING; GENETIC ANALYSIS; GENOMICS; HOMOLOGY; MAIZE; META-ANALYSIS; MORPHOGENESIS; PHOTOPERIOD;

ARTICLE; FLOWER; GENE EXPRESSION REGULATION; GENETICS; MAIZE; META ANALYSIS; PHOTOPERIODICITY; PHYSIOLOGY; PLANT GENE; QUANTITATIVE TRAIT LOCUS;

FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; PHOTOPERIOD; QUANTITATIVE TRAIT LOCI; ZEA MAYS;

EID: 84862254478     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01128.x     Document Type: Article

References (108)

1. Andersen JR, Schrag T, Melchinger AE, Zein I, Lübberstedt T (2005) Validation of Dwarf8 polymorphisms associated with flowering time in elite European inbred lines of maize (Zea mays L.). Theor. Appl. Genet. 111, 206-217.
2. Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: Integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20, 2324-2326.
3. Aukerman MJ, Lee I, Weigel D, Amasino RM (1999) The Arabidopsis flowering-time gene LUMINIDEPENDENS is expressed primarily in regions of cell proliferation and encodes a nuclear protein that regulates LEAFY expression. Plant J. 18, 195-203.
4. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36, 162-166.
5. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125, 655-664.
6. Balint-Kurti PJ, Johal GS (2009)Maize disease resistance. In: Bennetzen JL, Hake SC, eds. Handbook of Maize: Its Biology. Springer, New York pp. 229-250.
7. Bassiri A, Irish EE, Poethig RS (1992) Heterochronic effects of Teopod 2 on the growth and photosensitivity of the maize shoot. Plant Cell 4, 497-504.
8. Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130, 2385-2395.
9. Bonhomme R, Derieux M, Edmeades GO (1994) Flowering of diverse maize cultivars in relation to temperature and photoperiod in multilocation field strials. Crop Sci. 34, 156-164.
10. Brautigam CA, Smith BS, Ma Z, Palnitkar M, Tomchick DR, Machius M, Deisenhofer J (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101, 12142-12147.
11. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Villeda HS, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325, 714-718.
12. Camus-Kulandaivelu L, Luis-Miguel C, Tollon-Cordet C, Charcosset A, Manicacci D, Tenaillon M (2008) Patterns of molecular evolution associated with two selective sweeps in the Tb1-Dwarf8 region in maize. Genetics 180, 1107-1121.
13. Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423, 881-885.
14. Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A (2004) Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168, 2169-2185.
15. Christie JM (2007) Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21-45.
16. Colasanti J, Muszynski M (2009) The maize floral transition. In: SC Hake, JL Bennetzen, eds. Handbook of Maize: Its Biology. Springer, New York pp. 41-55.
17. Colasanti J, Tremblay R, Wong A, Coneva V, Kozaki A, Mable B (2006) The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 7, 158-175.
18. Colasanti J, Yuan Z, Sundaresan V (1998) The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93, 593-603.
19. Chen MJ, Yuan Z, Huang H (2006) Delayed flowering, an Arabidopsis gene that acts in the autonomous flowering promotion pathway and is required for normal development. J. Integr. Plant Biol. 48, 27-34.
20. Coles N, Zila C, Holland JB (2011) Allelic effect variation at key photoperiod response quantitative trait loci in maize. Crop Sci. 51, 1036-1049.
21. Coles ND, McMullen MD, Balint-Kurti PJ, Pratt RC, Holland JB (2010) Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis. Genetics 184, 799-812.
22. Danilevskaya ON, Meng X, Ananiev EV (2010) Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize. Plant Physiol. 153, 238-251.
23. Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008a) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol. 146, 250-264.
24. Danilevskaya ON, Meng X, Selinger DA, Deschamps S, Hermon P, Vansant G, Gupta R, Ananiev EV, Muszynski MG (2008b) Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize. Plant Physiol. 147, 2054-2069.
25. Deal RB, Kandasamy MK, McKinney EC, Meagher RB (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell 17, 2633-2646.
26. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc. Natl. Acad. Sci. USA 108, 6680-6685.
27. Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 12, 178-184.
28. Doebley J (2004) The genetics of maize evolution. Annu. Rev. Genet. 38, 37-59.
29. Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: Evidence for epistasis and the evolution of dominance. Genetics 141, 333-346.
30. Ducrocq S, Giauffret C, Madur D, Combes V, Dumas F, Jouanne S, Coubriche D, Jamin P, Moreau L, Charcosset A (2009) Fine mapping and haplotype structure analysis of a major flowering time quantitative trait locus on maize chromosome 10. Genetics 183, 1555-1563.
31. Ducrocq S, Madur D, Veyrieras JB, Camus-Kulandaivelu L, Kloiber-Maitz M, Presterl T, Ouzunova M, Manicacci D, Charcosset A (2008) Key impact of Vgt1 on flowering time adaptation in maize: Evidence from association mapping and ecogeographical information. Genetics 178, 2433-2437.
32. Flowers JM, Hanzawa Y, Hall MC, Moore RC, Purugganan MD (2009) Population genomics of the Arabidopsis thaliana flowering time gene network. Mol. Bio. Evol. 26, 2475-2486.
33. Fornara F, Maontaigu AD, Coupland G (2010) Control of flowering time in Arabidopsis. Cell 141, 550-550.e2.
34. Gouesnard B, Rebourg C, Welcker C, Charcosset A (2002) Analysis of photoperiod sensitivity within a collection of tropical maize populations. Genet. Res. Crop Evol. 49, 471-481.
35. Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 103, 1165-1172.
36. Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 131, 1855-1867.
37. Guo B, Sleper D, Lu P, Shannon J, Nguyen H, Arelli P (2006) QTLs associated with resistance to soybean cyst nematode in soybean: Meta-analysis of QTL locations. Crop Sci. 46, 595-602.
38. Hanocq E, Laperche A, Jaminon O, Lainé AL, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor. Appl. Genet. 114, 569-584.
39. Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: A negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351-360.
40. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719-722.
41. He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751-1754.
42. Henderson IR, Dean C (2004) Control of Arabidopsis flowering: The chill before the bloom. Development 131, 3829-3838.
43. Higgins JA, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5, e10065.
44. Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: Time to think about location. Curr. Opin. Plant Biol. 13, 83-89.
45. Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: Not only by coincidence. Trends Plant Sci. 11, 550-558.
46. Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J. 60, 614-625.
47. Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 8, 217-230.
48. 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.
49. Jung C, Müller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci. 14, 563-573.
50. Kebrom TH, Burson BL, Finlayson SA (2006) Phytochrome B represses teosinte branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol. 140, 1109-1117.
51. Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267, 522-525.
52. Kikuchi R, Handa H (2009) Photoperiodic control of flowering in barley. Breed. Sci. 59, 546-552.
53. Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: Winter and the timing of flowering in plants. Ann. Rev. Cell Dev. Biol. 25, 277-299.
54. Koester RP, Sisco PH, Stuber CW (1993) Identification of quantitative trait loci controlling days to flowering and plant height in two near isogenic lines of maize. Crop Sci. 33, 1209-1216.
55. Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J. 16, 345-353.
56. Lazakis CM, Coneva V, Colasanti J (2011) ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J. Exp. Bot. 62, 4833-4842.
57. Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994a) Isolation of LUMINIDEPENDENS: A gene involved in the control of flowering time in Arabidopsis. Plant Cell 6, 75-83.
58. Lee I, Michaels SD, Masshardt AS, Amasino RM (1994b) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903-909.
59. Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Hong CB, Kim HJ, Park CM (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16, 731-740.
60. Liu Z, Bao W, Liang W, Yin J, Zhang D (2010) Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J. Integr. Plant Biol. 52, 670-678.
61. Lu Y, Shah T, Hao Z, Taba S, Zhang S, Gao S, Liu J, Cao M, Wang J, Prakash AB (2011) Comparative SNP and haplotype analysis reveals a higher genetic diversity and rapider LD decay in tropical than temperate germplasm in maize. PLoS ONE 6, e24861.
62. Lu Y, Yan J, Guimaraes CT, Taba S, Hao Z, Gao S, Chen S, Li J, Zhang S, Vivek BS (2009) Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theor. Appl. Genet. 120, 93-115.
63. Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T (2010) Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc. Natl. Acad. Sci. USA 107, 19585-19590.
64. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737-745.
65. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377, 482-485.
66. McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeting induced locallesions in genomes (TILLING) for plant functional genomics. Plant Physiol. 123, 439-442.
67. McSteen P, Malcomber S, Skirpan A, Lunde C, Wu X, Kellogg E, Hake S (2007) Barren inflorescence2 encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiol. 144, 1000-1011.
68. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23, 942.
69. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956.
70. Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc. Natl. Acad. Sci. USA. 101, 3281.
71. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: Interacting pathways as a basis for diversity. Plant Cell 14, S111-S130.
72. Moutiq R, Ribaut J, Edmeades G, Krakowsky M, Lee M (2002) Elements of genotype-environment interaction: Genetic components of the photoperiod response in maize. In: Kang W, ed. Quantitative Genetics, Genomics, and Plant Breeding. CABI, UK pp. 257-267.
73. Mu GQ, Liang Y, Zhang ZM, Wu YQ, Liu SJ, Peng H, Zhang SZ, Pan GT (2009) Mapping quantitative trait loci associated with photoperiod sensitivity in maize (Zea mays L.). Agric. Sci. China 8, 24-30.
74. Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2008) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327-331.
75. Osugi A, Itoh H, Ikeda-Kawakatsu K, Takano M, Izawa T (2011) Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol. 157, 1128-1137.
76. Pepper A, Delaney T, Washburnt T, Poole D, Chory J (1994) DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 78, 109-116.
77. Pepper AE, Chory J (1997) Extragenic suppressors of the Arabidopsis det1 mutant identify elements of flowering-time and light-response regulatory pathways. Genetics 145, 1125-1137.
78. Purugganan MD, Suddith JI (1998) Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function. Proc. Natl. Acad. Sci. USA 95, 8130-8134.
79. Putterill J (2001) Flowering in time: Genes controlling photoperiodic flowering in Arabidopsis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1761-1767.
80. Putterill J, Laurie R, Macknight R (2004) It's time to flower: The genetic control of flowering time. Bioessays 26, 363-373.
81. Quesada V, Dean C, Simpson GG (2005) Regulated RNA processing in the control of Arabidopsis flowering. Int. J. Dev. Biol. 49, 773-780.
82. Reeves PH, Murtas G, Dash S, Coupland G (2002) early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC. Development 129, 5349-5361.
83. Salvi S, Castelletti S, Tuberosa R (2009) An updated consensus map for flowering time QTLs in maize. Maydica 54, 501-512.
84. Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev EV, Svitashev S, Bruggemann E (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc. Natl. Acad. Sci. USA 104, 11376-11381.
85. Salvi S, Tuberosa R, Chiapparino E, Maccaferri M, Veillet S, van Beuningen L, Isaac P, Edwards K, Phillips RL (2002) Toward positional cloning of Vgt1, a QTL controlling the transition from the vegetative to the reproductive phase in maize. Plant Mol. Biol. 48, 601-613.
86. Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13, 1427-1436.
87. Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3, 877-892.
88. Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182, 851-861.
89. Simpson GG (2004) The autonomous pathway: Epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol. 7, 570-574.
90. Simpson GG, Dijkwel PP, 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.
91. Song YH, Ito S, Imaizumi T (2010) Similarities in the circadian clock and photoperiodism in plants. Curr. Opin. Plant Biol. 13, 594-603.
92. Swamy BPM, Vikram P, Dixit S, Ahmed H, Kumar A (2011) Meta-analysis of grain yield QTL identified during agricultural drought in grasses showed consensus. BMC genomics 12, 319-337.
93. Tallury S, Goodman M (1999) Experimental evaluation of the potential of tropical germplasm for temperate maize improvement. Theor. Appl. Genet. 98, 54-61.
94. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28, 286-289.
95. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573-594.
96. Turner NC, Molyneux N, Yang S, Xiong YC, Siddique KHM (2011) Climate change in southwest Australia and northwest China: Challenges and opportunities for crop production. Crop Pasture Sci. 62, 445-456.
97. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006.
98. Wang C, Chen Y, Ku L, Wang T, Sun Z, Cheng F, Wu L (2010) Mapping QTL associated with photoperiod sensitivity and assessing the importance of QTL× environment interaction for flowering time in maize. PLoS ONE 5, e14068.
99. Wang C, Cheng F, Sun Z, Tang J, Wu L, Ku L, Chen Y (2008) Genetic analysis of photoperiod sensitivity in a tropical by temperate maize recombinant inbred population using molecular markers. Theor. Appl. Genet. 117, 1129-1139.
100. Wang Q, Sajja U, Rosloski S, Humphrey T, Kim MC, Bomblies K, Weigel D, Grbic V (2007) HUA2 caused natural variation in shoot morphology of A. thaliana. Curr. Biol. 17, 1513-1519.
101. Wang Y, Yao J, Zhang Z, Zheng Y (2006) The comparative analysis based on maize integrated QTL map and meta-analysis of plant height QTLs. Chin. Sci. Bull. 51, 2219-2230.
102. Weigel D (1995) The genetics of flower development: From floral induction to ovule morphogenesis. Ann. Rev. Genet. 29, 19-39.
103. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843-859.
104. Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14, 87-100.
105. Xu Y, Crouch JH (2008) Marker-assisted selection in plant breeding: From publications to practice. Crop Sci. 48, 391-407.
106. Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T (2001) Genetic control of flowering time in rice, a short-day plant. Plant Physiol. 127, 1425-1429.
107. Zagotta MT, Hicks KA, Jacobs CI, Young JC, Hangarter RP, Meeks-Wagner DR (1996) The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 10, 691-702.
108. Zhang X, Tang B, Liang W, Zheng Y, Qiu F (2011) Quantitative genetic analysis of flowering time, leaf number and photoperiod sensitivity in maize (Zea mays L.). J. Plant Breed. Crop Sci. 3, 168-184.