Key flowering genes including FT-like genes are upregulated in the vasculature of apple dwarfing rootstocks

Tree Genetics and Genomes

Volumn 10, Issue 1, 2014, Pages 189-202

  Foster, Toshi M ^a   Watson, Amy E ^a   van Hooijdonk, Ben M ^a   Schaffer, Robert J ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

Dwarfing rootstocks; Floral induction; Flowering Locus T (FT); Gene expression; Malus

Indexed keywords

MALUS; MALUS X DOMESTICA;

EID: 84892488245     PISSN: 16142942     EISSN: 16142950     Source Type: Journal    
DOI: 10.1007/s11295-013-0675-z     Document Type: Article

References (87)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056. doi: 10. 1126/science. 1115983.
2. Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25: 605-614. DOI http://www. nature. com/emboj/journal/v25/n3/suppinfo/7600950a_S1. html.
3. An HL, Roussot C, Suarez-Lopez P, Corbesler L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615-3626. doi: 10. 1242/dev. 01231.
4. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043. doi: 10. 1126/science. 1126038.
5. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275: 80-83. doi: 10. 1126/science. 275. 5296. 80.
6. Carrière EA (1897) Un nouveau sujet pour greffer les pommes. Revue Horticole: 436-437.
7. Celton JM (2007) Dissection of the dwarfing effect of the apple rootstock 'M. 9'. Massey University, New Zealand.
8. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033. doi: 10. 1126/science. 1141752.
9. Cummins J, Aldwinkle H (1983) Apple rootstock breeding. Cornell University, Geneva.
10. Davies RT, Goetz DH, Lasswell J, Anderson MN, Bartel B (1999) IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. The Plant Cell 11: 365-376. doi: 10. 1105/tpc. 11. 3. 365.
11. Eckardt NA (2007) Phloem-borne FT signals flowering in cucurbits. The Plant Cell Online 19: 1435-1438. doi: 10. 1105/tpc. 107. 053447.
12. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14: 703-712. doi: 10. 1007/s11248-005-6752-3.
13. Ferree DC, Carlson RF (1987) Apple rootstocks. In: Rom RC, Carlson RF (eds) Rootstocks for fruit crops. Wiley, New York, NY, pp 107-143.
14. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. The Plant Cell 12: 599-609. doi: 10. 1105/tpc. 12. 4. 599.
15. Fischer C (1994) Shortening of the juvenile period in apple breeding. In: Schmidt H, Kellerhals M (eds) Progress in temperate fruit breeding. Kluwer, Dordrecht, pp 161-164.
16. Flachowsky H, Peil A, Sopanen T, Elo A, Hanke V (2007) Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early-flowering in apple (Malus × domestica Borkh.). Plant Breed 126: 137-145. doi: 10. 1111/j. 1439-0523. 2007. 01344. x.
17. Foster T, Johnston R, Seleznyova A (2003) A morphological and quantitative characterization of early floral development in apple (Malus × domestica Borkh.). Ann Bot 92: 199-206.
18. Fulford RM (1966) The morphogenesis of apple buds: II. The development of the Bud. Ann Bot 30: 25-38.
19. Gregory PJ, George TS (2011) Feeding nine billion: the challenge to sustainable crop production. J Exp Bot 62: 5233-5239. doi: 10. 1093/jxb/err232.
20. Gyllenstrand N, Clapham D, Källman T, Lagercrantz U (2007) A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol 144: 248-257. doi: 10. 1104/pp. 107. 095802.
21. Hackett WP (1985) Juvenility, maturation and rejuvenation in woody plants. Hortic Rev 7: 109-155.
22. Halle F, Oldeman RAA, Tomlinson PB (1978) Tropical trees and forests: an architectural analysis. In: Tropical trees and forests: an architectural analysis., pp 441 pp.
23. Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci U S A 102: 7748-7753. doi: 10. 1073/pnas. 0500932102.
24. Hartmann U, Hohmann 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. doi: 10. 1046/j. 1365-313x. 2000. 00682. x.
25. Hättasch C, Flachowsky H, Kapturska D, Hanke M-V (2008) Isolation of flowering genes and seasonal changes in their transcript levels related to flower induction and initiation in apple (Malus domestica). Tree Physiol 28: 1459-1466. doi: 10. 1093/treephys/28. 10. 1459.
26. Hättasch C, Flachowsky H, Hanke M-V, Lehmann S, Gau A, Kapturska D (2009) The switch to flowering: genes involved in floral induction of the apple 'Pinova' and the role of the flowering gene MdFT. Acta Horticult 839: 701.
27. Hsu C-Y, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. The Plant Cell 18: 1846-1861. doi: 10. 1105/tpc. 106. 041038.
28. Hsu CY, Adams JP, Kim HJ, No K, Ma CP, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, dePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci U S A 108: 10756-10761. doi: 10. 1073/pnas. 1104713108.
29. Hsu C-Y, Adams JP, No K, Liang H, Meilan R, Pechanova O, Barakat A, Carlson JE, Page GP, Yuceer C (2012) Overexpression of constans homologs CO1 and CO2 fails to alter normal reproductive onset and fall Bud Set in woody perennial poplar. PLoS One 7: 45448. doi: 10. 1371/journal. pone. 0045448.
30. Imamura T, Nakatsuka T, Higuchi A, Nishihara M, Takahashi H (2011) The gentian orthologs of the FT/TFL1 gene family control floral initiation in Gentiana. Plant Cell Physiol 52: 1031-1041. doi: 10. 1093/pcp/pcr055.
31. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17: 1050-1054. doi: 10. 1016/j. cub. 2007. 05. 008.
32. Janssen B, Thodey K, Schaffer R, Alba R, Balakrishnan L, Bishop R, Bowen J, Crowhurst R, Gleave A, Ledger S, McArtney S, Pichler F, Snowden K, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biology 8: 16.
33. Jensen P, Rytter J, Detwiler E, Travis J, McNellis T (2003) Rootstock effects on gene expression patterns in apple tree scions. Plant Mol Biol 53: 493-511. doi: 10. 1023/B: PLAN. 0000019122. 90956. 3b.
34. Jensen P, Makalowska I, Altman N, Fazio G, Praul C, Maximova S, Crassweller R, Travis J, McNellis T (2010) Rootstock-regulated gene expression patterns in apple tree scions. Tree Genet Genomes 6: 57-72. doi: 10. 1007/s11295-009-0228-7.
35. Kamboj JS, Browning G, Blake PS, Quinlan JD, Baker DA (1999) GC-MS-SIM analysis of abscisic acid and indole-3-acetic acid in shoot bark of apple rootstocks. Plant Growth Regul 28: 21-27. doi: 10. 1023/a: 1006299414481.
36. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286: 1962-1965. doi: 10. 1126/science. 286. 5446. 1962.
37. 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. doi: 10. 1126/science. 286. 5446. 1960.
38. Kotoda N, Wada M (2005) MdTFL1, A TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis. Plant Sci 168: 95-104. doi: 10. 1016/j. plantsci. 2004. 07. 024.
39. Kotoda N, Wada M, Komori S, Kidou S, Abe K, Masuda T, Soejima J (2000) Expression pattern of homologues of floral meristem identity genes LFY and AP1 during flower development in apple. J Amer Soc Hortic Sci 125: 398-403.
40. Kotoda N, Wada M, Kusaba S, Kano-Murakami Y, Masuda T, Soejima J (2002) Overexpression of MdMADS5, an APETALA1-like gene of apple, causes early flowering in transgenic Arabidopsis. Plant Sci 162: 679-687. doi: 10. 1016/s0168-9452(02)00024-9.
41. Kotoda N, Hayashi H, Suzuki M, Igarashi M, Hatsuyama Y, S-i K, Igasaki T, Nishiguchi M, Yano K, Shimizu T, Takahashi S, Iwanami H, Moriya S, Abe K (2010) Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus × domestica Borkh.). Plant Cell Physiol 51: 561-575. doi: 10. 1093/pcp/pcq021.
42. Krogan NT, Long JA (2009) Why so repressed? Turning off transcription during plant growth and development. Curr Opin Plant Biol 12: 628-636. doi: 10. 1016/j. pbi. 2009. 07. 011.
43. Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T, Seo M, Kanno Y, Häkkinen ST, van Montagu MCE, Thevelein JM, Maaheimo H, Oksman-Caldentey K-M, Rodriguez PL, Rischer H, Goossens A (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci. doi: 10. 1073/pnas. 1103010108.
44. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357-359. http://www. nature. com/nmeth/journal/v9/n4/abs/nmeth. 1923. html#supplementary-information.
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079. doi: 10. 1093/bioinformatics/btp352.
46. Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci 103: 6398-6403. doi: 10. 1073/pnas. 0601620103.
47. Lin M-K, Belanger H, Lee Y-J, Varkonyi-Gasic E, Taoka K-I, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. The Plant Cell Online 19: 1488-1506. doi: 10. 1105/tpc. 107. 051920.
48. Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17: 1055-1060. doi: 10. 1016/j. cub. 2007. 05. 009.
49. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137: 149-156. doi: 10. 1104/pp. 104. 052811.
50. Mimida N, Kotoda N, Ueda T, Igarashi M, Hatsuyama Y, Iwanami H, Moriya S, Abe K (2009) Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus × domestica Borkh.). Plant Cell Physiol 50: 394-412. doi: 10. 1093/pcp/pcp001.
51. Mimida N, Komori S, Suzuki A, Wada M (2013) Functions of the apple TFL1/FT orthologs in phase transition. Sci Hortic 156: 106-112. doi: 10. 1016/j. scienta. 2013. 04. 001.
52. Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk Y-K (2006) Analyses of expressed sequence tags from apple. Plant Physiol 141: 147-166. doi: 10. 1104/pp. 105. 076208.
53. Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, Omura M, Ikoma Y (2007) Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu marc.). J Exp Bot 58: 3915-3927. doi: 10. 1093/jxb/erm246.
54. Notaguchi M, Abe M, Kimura T, Daimon Y, Kobayashi T, Yamaguchi A, Tomita Y, Dohi K, Mori M, Araki T (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol 49: 1645-1658. doi: 10. 1093/pcp/pcn154.
55. Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S (2007) Characterization of phloem-sap transcription profile in melon plants. J Exp Bot 58: 3645-3656. doi: 10. 1093/jxb/erm214.
56. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. The Plant Cell 23: 3089-3100. doi: 10. 1105/tpc. 111. 089300.
57. Pilcher RLR, Celton J-M, Gardiner SE, Tustin DS (2008) Genetic markers linked to the dwarfing trait of apple rootstock 'malling 9'. J Am Soc Hortic Sci 133: 100-106.
58. Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35: 1742-1755. doi: 10. 1111/j. 1365-3040. 2012. 02558. x.
59. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330: 1397-1400. doi: 10. 1126/science. 1197004.
60. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842. doi: 10. 1093/bioinformatics/btq033.
61. Roberts R (1934) Ring grafting and stock effect. Proc Am Soc Hortic Sci 32: 328-329.
62. Santiago J, Dupeux F, Round A, Antoni R, Park S-Y, Jamin M, Cutler SR, Rodriguez PL, Marquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462: 665-668. DOI http://www. nature. com/nature/journal/v462/n7273/suppinfo/nature08591_S1. html.
63. Sawa M, Kay SA (2011) GIGANTEA directly activates flowering locus T in Arabidopsis thaliana. Proc Natl Acad Sci U S A 108: 11698-11703. doi: 10. 1073/pnas. 1106771108.
64. Seleznyova A, Tustin DS (2008) From the patterns of axillary flowering to the hypotheses at a meristem level: Simulation modelling of rootstock-induced effects in young apple trees. Annals of Botany.
65. Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Lifschitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci 106: 8392-8397. doi: 10. 1073/pnas. 0810810106.
66. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey SD V, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, NY, pp 397-420.
67. Soejima J, Yoshida Y, Haniuda T, Bessho H, Tsuchiya S, Masuda T, Komori S, Sanada T, Ito Y, Sadamori S, Kashimura Y (2010) New dwarfing apple rootstocks 'JM1', 'JM7', and 'JM8'. Bull Natl Inst Fruit Tree Sci 11: 1-16.
68. Soumelidou K, Battey NH, John P, Barnett JR (1994) The anatomy of the developing Bud union and its relationship to dwarfing in apple. Ann Bot 74: 605-611. doi: 10. 1006/anbo. 1994. 1161.
69. Tiwari SB, Shen Y, Chang HC, Hou YL, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, Belachew A, Repetti PP, Reuber TL, Ratcliffe OJ (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187: 57-66. doi: 10. 1111/j. 1469-8137. 2010. 03251. x.
70. Tränkner C, Lehmann S, Hoenicka H, Hanke M-V, Fladung M, Lenhardt D, Dunemann F, Gau A, Schlangen K, Malnoy M, Flachowsky H (2010) Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta 232: 1309-1324. doi: 10. 1007/s00425-010-1254-2.
71. Tränkner C, Lehmann S, Hoenicka H, Hanke M-V, Fladung M, Lenhardt D, Dunemann F, Gau A, Schlangen K, Malnoy M, Flachowsky H (2011) Note added in proof to: over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta 233: 217-218. doi: 10. 1007/s00425-010-1317-4.
72. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech 28: 511-515. http://www. nature. com/nbt/journal/v28/n5/abs/nbt. 1621. html#supplementary-information.
73. Tukey H, Brase K (1944) The dwarfing effect of an intermediate stem-piece of malling IX apple. Proc Am Soc Hortic Sci 42: 357-364.
74. Turnbull C (2011) Long-distance regulation of flowering time. J Exp Bot 62: 4399-4413. doi: 10. 1093/jxb/err191.
75. 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. doi: 10. 1126/science. 1091761.
76. van Hooijdonk BM, Woolley DJ, Warrington IJ, Tustin DS (2010) Initial alteration of scion architecture by dwarfing apple rootstocks may involve shoot-root-shoot signalling by auxin, gibberellin, and cytokinin. J Hortic Sci Biotechnol 85: 59-65.
77. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar S, Troggio M, Pruss D (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42: 833-839.
78. Webster AD (1995) Rootstock and interstock effects on deciduous fruit tree vigour, precocoity and yield productivity. N Z J Crop Hortic Sci 23: 373-382.
79. Webster AD, Wertheim SJ (2003) Apple rootstocks. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI, Cambridge, MA.
80. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059. doi: 10. 1126/science. 1114358.
81. Wilkie JD, Sedgley M, Olesen T (2008) Regulation of floral initiation in horticultural trees. J Exp Bot 59: 3215-3228. doi: 10. 1093/jxb/ern188.
82. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46: 1175-1189. doi: 10. 1093/pcp/pci151.
83. Yoo SY, Kardailsky I, Lee JS, Weigel D, Ahn JH (2004) Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1). Mol Cells 17: 95-101.
84. Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates SUPPRESSOR OFOVEREXPRESSION OFCONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol 139: 770-778. doi: 10. 1104/pp. 105. 066928.
85. Yoo SJ, Chung KS, Jung SH, Yoo SY, Lee JS, Ahn JH (2010) BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J 63: 241-253. doi: 10. 1111/j. 1365-313X. 2010. 04234. x.
86. Yoo S-C, Chen C, Rojas M, Daimon Y, Ham B-K, Araki T, Lucas WJ (2013) Phloem long-distance delivery of FLOWERING LOCUS T (FT) to the apex. Plant J 75: 456-468. doi: 10. 1111/tpj. 12213.
87. Zhang H, Harry DE, Ma C, Yuceer C, Hsu C-Y, Vikram V, Shevchenko O, Etherington E, Strauss SH (2010) Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J Exp Bot 61: 2549-2560. doi: 10. 1093/jxb/erq092.