Abstract
The flowering integrator gene FLOWERING LOCUS T (FT) in Arabidopsis thaliana is conserved between diverse plant species and is thought to be the flowering signal ‘‘florigen’’, a universal long-distance mobile signal. In soybean, two FT homologs having a function to induce flowering in Arabidopsis have been identified. In this study, we showed that the expression of FT from Arabidopsis by the Apple latent spherical virus (ALSV) vector promoted precocious flowering and terminated vegetative growth in a wide range of genotypes of soybean, without using a short-day treatment. Four determinate and two indeterminate cultivars, infected with ALSV expressing FT (FT-ALSV), set flower buds on shoot apices and terminated vegetative growth at the fourth- to seventh-node stages under long-day conditions. In contrast, non-infected, healthy plants did not set flower buds on shoot apices at the same stage under the same conditions. After flowering, soybean cultivars infected with FT-ALSV, belonging to different maturity groups and stem growth habits, matured and produced seeds. The results suggest that the basic flowering pathway controlled by FT in A. thaliana might also be conserved in soybean. A system for precocious flowering and shortening of generation time using FT-ALSV would be a useful and novel technology for efficient soybean breeding.
Similar content being viewed by others
Abbreviations
- ALSV:
-
Apple latent spherical virus
- FT :
-
FLOWERING LOCUS T
- CO :
-
CONSTANS
- bZIP:
-
Basic region–leucine zipper
- SD:
-
Short-day
- LD:
-
Long-day
- TFL1 :
-
TERMINAL FLOWER1
- dpi:
-
Days post-inoculation
- RT-PCR:
-
Reverse transcription-polymerase chain reaction
References
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
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:10.1038/sj.emboj.7600950
Bernard RL (1972) Two genes affecting stem termination in soybeans. Crop Sci 12:235–239
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
Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16(Suppl):S18–S31. doi:10.1105/tpc.015958
Carmona MJ, Calonje M, Martinez-Zapater JM (2007) The FT/TFL1 gene family in grapevine. Plant Mol Biol 63:637–650. doi:10.1007/s11103-006-9113-z
Carpentieri-Pípolo V, Almeida LA, Kiihl RAS (2002) Inheritance of a long juvenile period under short-day conditions in soybean. Genet Mol Biol 25:463–469. doi:10.1590/S1415-47572002000400016
Cober ER, Tanner JW, Voldeng HD (1996) Genetic control of photoperiod response in early-maturing, near isogenic soybean lines. Crop Sci 36:601–605
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
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 trifoliate L. Raf). Transgenic Res 14:703–712. doi:10.1007/s11248-005-6632-3
Fukui J (1963) Ecological studies of soybean varieties on the basis of day-length sensibility. J Centr Agric Exp Stn 3:19–78 (in Japanese with English abstract)
Fukui J, Arai M (1951) Ecological studies on Japanese soy-bean varieties. I. Classification of soy-bean varieties on the basis of the days from germination to blooming and from blooming to ripening with special reference to their geographical differentiation. Jpn J Breed 1:27–39 (in Japanese with English abstract)
Gyllenstrand N, Clapham D, Kallman T, Lagercarntz 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
Hayama R, Agashe B, Luley E, King R, Coupland G (2007) A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988–3000. doi:10.1105/tpc.107.052480
Hecht V, Foucher F, Ferrándiz C, MacKnight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltrán JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420–1434. doi:10.1104/pp.104.057018
Hiraoka K, Daimon Y, Araki T (2008) FT protein: a universal long-distance mobile signal in seed plants? Plant Morphol 19:3–13 (in Japanese with English abstract)
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
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
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
Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535. doi:10.1146/annurev.arplant.55.031903.141644
Kong F, Liu B, Xia Z, Sato S, Kim B, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, Abe J (2010) Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. doi:10.1104/pp.110.160796
Kotoda N, Hayashi H, Suzuki M, Igarashi M, Hatsuyama Y, Kidou S, 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
Li C, Sasaki N, Isogai M, Yoshikawa N (2004) Stable expression of foreign proteins in herbaceous and apple plants using Apple latent spherical virus RNA2 vectors. Arch Virol 149:1541–1558. doi:10.1007/s00705-004-0310-2
Li C, Zhang K, Zeng X, Jackson S, Zhou Y, Hong Y (2009) A cis element within Flowering Locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA. J Virol 83:3540–3548. doi:10.1128/JVI.02346-08
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 USA 103:6398–6403. doi:10.1073/pnas.0601620103
Lin MK, Belanger H, Lee YJ, Varkonyi-Gasic E, Taoka K, Miura E, Xoconostle-Cazares 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. Plant Cell 19:1488–1506. doi:10.1105/tpc.107.051920
Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180:995–1007. doi:10.1534/genetics.108.092742
Liu B, Watanabe S, Uchiyama T, Kong F, Kanazawa A, Xia Z, Aria M, Yamada T, Kitamura K, Masuta C, Harada K, Abe J (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol 153:198–210. doi:10.1104/pp.109.150607
Mathieu J, Warthman 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
McBrain BA, Bernard RL (1987) A new gene affecting the time of flowering and maturity in soybeans. J Hered 178:68–70
Nakamura K, Yamagishi N, Isogai M, Komori S, Ito T, Yoshikawa N (2010) Seed and pollen transmission of Apple latent spherical virus in apple. J Gen Plant Pathol (in press)
Neumaier N, James AT (1993) Exploiting the long juvenile trait to improve adaptation of soybeans to the tropics. Food Legume Newsl 18:12–14
Orf JH, Diers BW, Boerma HR (2004) Genetic improvement: conventional and molecular-based strategies. In: Boerma HR, Specht JE (eds) SOYBEANS: improvement, production, and uses, 3rd edn. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, WI, pp 417–450
Parcy F, Bomblies K, Weigel D (2002) Interaction of LEAFY, AGAMOUS and TERMINAL FLOWER1 in maintaining floral meristem identity in Arabidopsis. Development 129:2519–2527
Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. doi:10.1038/nature08670
Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Liftchitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci USA 106:8392–8397. doi:10.1073/pnas.0810810106
Shanmugasundaram S (1981) Varietal differences and genetic behavior for the photoperiodic responses in soybeans. Bull Inst Trop Agric Kyushu Univ 4:1–61
Shoemaker RC, Cregan PB, Vodkin LO (2004) Soybean genomics. In: Boerma HR, Specht JE (eds) SOYBEANS: improvement, production, and uses, 3rd edn. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, WI, pp 235–264
Summerfield RJ, Roberts EH (1985) Glycine max. In: Halevy AH (ed) CRC handbook of flowering, vol 1. CRC, Boca Raton, FL, pp 100–117
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036. doi:10.1126/science.1141753
Tasma IM, Shoemaker RC (2003) Mapping flowering time gene homologs in soybean and their association with maturity (E) loci. Crop Sci 43:319–328
Tazawa A, Miyoshi T, Tanaka Y, Kanno H, Tezuka M, Kousaka H (2008) Development of soybean breeding line Shoku-kei 32 with high resistance to soybean dwarf virus disease derived from ‘‘WILIS’’. Bull Hokkaido Prefect Agric Exp Stn 92:51–60 (in Japanese)
Thakare D, Kumudini S, Dinkins RD (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and LD conditions. Planta 231:951–963. doi:10.1007/s00425-010-1100-6
Tian Z, Wang X, Lee R, Li Y, Specht JE, Nelson RL, McClean PE, Qiu L, Ma J (2010) Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci USA 107:8563–8568. doi:10.1073/pnas.1000088107
Tsuji H, Tamaki S, Komiya R, Shimamoto K (2008) Florigen and the photoperiodic control of flowering in rice. Rice 1:25–35. doi:10.1007/s12284-008-9005-8
Watanabe S, Hideshima R, Xia Z, Tsubokura Y, Sato S, Nakamoto Y, Yamsnaka N, Takahashi R, Ishimoto M, Anai T, Tabata S, Harada K (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262. doi:10.1534/genetics.108.098772
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
Wong CE, Singh MB, Bhalla PL (2009) Molecular processes underlying the floral transition in the soybean shoot apical meristem. Plant J 57:832–845. doi:10.1111/j.1365-313X.2008.03730.x
Yamagishi N, Yoshikawa N (2009) Virus-induced gene silencing in soybean seeds and the emergence stage of soybean plants with Apple latent spherical virus vectors. Plant Mol Biol 71:15–24. doi:10.1007/s11103-009-9505-y
Yamanaka N, Ninomiya S, Hoshi M, Tsubokura Y, Yano M, Nagamura Y, Sasaki T, Harada K (2001) An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. DNA Res 8:61–72. doi:10.1093/dnares/8.2.61
Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586. doi:10.1073/pnas.0607142103
Acknowledgments
We are grateful to Dr. Shuji Yokoi (Iwate University) for critical reading of the manuscript, and to Drs. Shinji Sakai and Soh Hidaka (National Agricultural Research Center Tohoku region), and Dr. Noriyuki Furutani (Kyoto Prefectural Institute of Agriculture) for helpful suggestions. We also thank Dr. Makoto Tougou (National Agricultural Research Center Tohoku region) and the National Agricultural Research Center Tohoku region for supplying soybean seeds of cultivars ‘Jack’, ‘Suzukari’, and ‘Hatayutaka’ and ‘Dewamusume’ and ‘Nemasirazu’. This work was supported in part by Grants-in-Aid from KAKENHI (no. 20380025) and the Ministry of Education, Culture, Sports, Science and Technology of Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yamagishi, N., Yoshikawa, N. Expression of FLOWERING LOCUS T from Arabidopsis thaliana induces precocious flowering in soybean irrespective of maturity group and stem growth habit. Planta 233, 561–568 (2011). https://doi.org/10.1007/s00425-010-1318-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-010-1318-3