Manipulation of flowering time and branching by overexpression of the tomato transcription factor SlZFP2

Plant Biotechnology Journal

Volumn 14, Issue 12, 2016, Pages 2310-2321

  Weng, Lin ^a   Bai, Xiaodong ^b   Zhao, Fangfang ^a   Li, Rong ^a   Xiao, Han ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

branching; flowering time; overexpression; RNA sequencing; tomato (Solanum lycopersicum); transcriptional regulation

Indexed keywords

PLANT PROTEIN; PLANT RNA; TRANSCRIPTION FACTOR;

FLOWER; GENE EXPRESSION; GENETICS; METABOLISM; TOMATO;

FLOWERS; GENE EXPRESSION; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; RNA, PLANT; TRANSCRIPTION FACTORS;

EID: 84977495092     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12584     Document Type: Article

References (59)

1. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D. et al. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science, 311, 91–94.
2. Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., Moritz, T. et al. (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl Acad. Sci. USA, 104, 6484–6489.
3. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Ser. B, 57, 289–300.
4. Blumel, M., Dally, N. and Jung, C. (2015) Flowering time regulation in crops-what did we learn from Arabidopsis? Curr. Opin. Biotechnol. 32, 121–129.
5. Busch, B.L., Schmitz, G., Rossmann, S., Piron, F., Ding, J., Bendahmane, A. and Theres, K. (2011) Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell, 23, 3595–3609.
6. Chen, M., MacGregor, D.R., Dave, A., Florance, H., Moore, K., Paszkiewicz, K., Smirnoff, N. et al. (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proc. Natl Acad. Sci. USA, 111, 18787–18792.
7. Dielen, V., Lecouvet, V., Dupont, S. and Kinet, J.M. (2001) In vitro control of floral transition in tomato (Lycopersicon esculentum Mill.), the model for autonomously flowering plants, using the late flowering uniflora mutant. J. Exp. Bot. 52, 715–723.
8. Huang, X., Ding, J., Effgen, S., Turck, F. and Koornneef, M. (2013) Multiple loci and genetic interactions involving flowering time genes regulate stem branching among natural variants of Arabidopsis. New Phytol. 199, 843–857.
9. Jeifetz, D., David-Schwartz, R., Borovsky, Y. and Paran, I. (2011) CaBLIND regulates axillary meristem initiation and transition to flowering in pepper. Planta, 234, 1227–1236.
10. Jiang, K., Liberatore, K.L., Park, S.J., Alvarez, J.P. and Lippman, Z.B. (2013) Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet. 9, e1004043.
11. Kinoshita, T., Ono, N., Hayashi, Y., Morimoto, S., Nakamura, S., Soda, M., Kato, Y. et al. (2011) FLOWERING LOCUS T regulates stomatal opening. Curr. Biol. 21, 1232–1238.
12. Krieger, U., Lippman, Z.B. and Zamir, D. (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459–463.
13. Kumar, S.V., Lucyshyn, D., Jaeger, K.E., Alos, E., Alvey, E., Harberd, N.P. and Wigge, P.A. (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature, 484, 242–245.
14. Lee, R., Baldwin, S., Kenel, F., McCallum, J. and Macknight, R. (2013) FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat. Commun. 4, 2884.
15. Leyser, O. (2005) The fall and rise of apical dominance. Curr. Opin. Genet. Dev. 15, 468–471.
16. Lifschitz, E. and Eshed, Y. (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J. Exp. Bot. 57, 3405–3414.
17. Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z., Alvarez, J.P. et al. (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.
18. Lifschitz, E., Ayre, B.G. and Eshed, Y. (2014) Florigen and anti-florigen – a systemic mechanism for coordinating growth and termination in flowering plants. Front. Plant Sci. 5, 465.
19. Lin, D., Nagawa, S., Chen, J., Cao, L., Chen, X., Xu, T., Li, H. et al. (2012) A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr. Biol. 22, 1319–1325.
20. Liu, H., Yu, X., Li, K., Klejnot, J., Yang, H., Lisiero, D. and Lin, C. (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science, 322, 1535–1539.
21. Liu, Y., Li, X., Li, K., Liu, H. and Lin, C. (2013) Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet. 9, e1003861.
22. Marin-Gonzalez, E., Matias-Hernandez, L., Aguilar-Jaramillo, A.E., Lee, J.H., Ahn, J.H., Suarez-Lopez, P. and Pelaz, S. (2015) SHORT VEGETATIVE PHASE up-regulates TEMPRANILLO2 floral repressor at low ambient temperatures. Plant Physiol. 169, 1214–1224.
23. Martinez-Zapater, J.M., Coupland, G., Dean, C. and Koornneef, M. (1994) The transition to flowering in Arabidopsis, in Arabidopsis. (Meyerowitz, E.M. and Somerville, C.R., eds), pp. 403–433. New York, USA: Cold Spring Harbor Laboratory Press.
24. Mathieu, J., Yant, L.J., Murdter, F., Kuttner, F. and Schmid, M. (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol. 7, e1000148.
25. Michaels, S.D. (2009) Flowering time regulation produces much fruit. Curr. Opin. Plant Biol. 12, 75–80.
26. Molinero-Rosales, N., Latorre, A., Jamilena, M. and Lozano, R. (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta, 218, 427–434.
27. Moon, J., Zhao, Y., Dai, X., Zhang, W., Gray, W.M., Huq, E. and Estelle, M. (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol. 143, 684–696.
28. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621–628.
29. Muller, D. and Leyser, O. (2011) Auxin, cytokinin and the control of shoot branching. Ann. Bot. 107, 1203–1212.
30. Navarro, C., Abelenda, J.A., Cruz-Oro, E., Cuellar, C.A., Tamaki, S., Silva, J., Shimamoto, K. et al. (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature, 478, 119–122.
31. Park, S.J., Jiang, K., Tal, L., Yichie, Y., Gar, O., Zamir, D., Eshed, Y. et al. (2014) Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat. Genet. 46, 1337–1342.
32. Pin, P.A., Benlloch, R., Bonnet, D., Wremerth-Weich, E., Kraft, T., Gielen, J.J. and Nilsson, O. (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science, 330, 1397–1400.
33. Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., Zamir, D. et al. (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development, 125, 1979–1989.
34. Porri, A., Torti, S., Romera-Branchat, M. and Coupland, G. (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development, 139, 2198–2209.
35. Quinet, M., Dielen, V., Batoko, H., Boutry, M., Havelange, A. and Kinet, J.M. (2006a) Genetic interactions in the control of flowering time and reproductive structure development in tomato (Solanum lycopersicum). New Phytol. 170, 701–710.
36. Quinet, M., Dubois, C., Goffin, M.C., Chao, J., Dielen, V., Batoko, H., Boutry, M. et al. (2006b) Characterization of tomato (Solanum lycopersicum L.) mutants affected in their flowering time and in the morphogenesis of their reproductive structure. J. Exp. Bot. 57, 1381–1390.
37. Quinet, M., Kinet, J.M. and Lutts, S. (2010) Flowering response of the uniflora:blind:self-pruning and jointless:uniflora:self-pruning tomato (Solanum lycopersicum) triple mutants. Physiol. Plant. 141, 166–176.
38. Rameau, C., Bertheloot, J., Leduc, N., Andrieu, B., Foucher, F. and Sakr, S. (2015) Multiple pathways regulate shoot branching. Front. Plant Sci. 5, 741.
39. Ruegger, M., Dewey, E., Gray, W.M., Hobbie, L., Turner, J. and Estelle, M. (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev. 12, 198–207.
40. Salehin, M., Bagchi, R. and Estelle, M. (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell, 27, 9–19.
41. Schmitz, G., Tillmann, E., Carriero, F., Fiore, C., Cellini, F. and Theres, K. (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc. Natl Acad. Sci. USA, 99, 1064–1069.
42. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G. and Theres, K. (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl Acad. Sci. USA, 96, 290–295.
43. Shalit, A., Rozman, A., Goldshmidt, A., Alvarez, J.P., Bowman, J.L., Eshed, Y. and Lifschitz, E. (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc. Natl Acad. Sci. USA, 106, 8392–8397.
44. Shu, K., Chen, Q., Wu, Y., Liu, R., Zhang, H., Wang, S., Tang, S. et al. (2016) ABSCISIC ACID-INSENSITIVE 4 negatively regulates flowering through directly promoting Arabidopsis FLOWERING LOCUS C transcription. J. Exp. Bot. 67, 195–205.
45. Song, Y.H., Smith, R.W., To, B.J., Millar, A.J. and Imaizumi, T. (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science, 336, 1045–1049.
46. Teichmann, T. and Muhr, M. (2015) Shaping plant architecture. Front. Plant Sci. 6, 233.
47. Tiwari, S.B., Shen, Y., Chang, H.C., Hou, Y., Harris, A., Ma, S.F., McPartland, M. et al. (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57–66.
48. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105–1111.
49. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L. et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515.
50. Tsuji, H., Taoka, K. and Shimamoto, K. (2010) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr. Opin. Plant Biol. 14, 45–52.
51. Wang, Y., Li, L., Ye, T., Lu, Y., Chen, X. and Wu, Y. (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J. Exp. Bot. 64, 675–684.
52. Weng, L., Zhao, F., Li, R., Xu, C., Chen, K. and Xiao, H. (2015) The zinc finger transcription factor SlZFP2 negatively regulates abscisic acid biosynthesis and fruit ripening in tomato. Plant Physiol. 167, 931–949.
53. Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U. and Weigel, D. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309, 1056–1059.
54. Wilmowicz, E., Kesy, J. and Kopcewicz, J. (2008) Ethylene and ABA interactions in the regulation of flower induction in Pharbitis nil. J. Plant Physiol. 165, 1917–1928.
55. Xiao, H., Radovich, C., Welty, N., Hsu, J., Li, D., Meulia, T. and van der Knaap, E. (2009) Integration of tomato reproductive developmental landmarks and expression profiles, and the effect of SUN on fruit shape. BMC Plant Biol. 9, 49.
56. Xu, Y., Gan, E.S., Zhou, J., Wee, W.Y., Zhang, X. and Ito, T. (2014) Arabidopsis MRG domain proteins bridge two histone modifications to elevate expression of flowering genes. Nucleic Acids Res. 42, 10960–10974.
57. Yan, Y., Shen, L., Chen, Y., Bao, S., Thong, Z. and Yu, H. (2014) A MYB-domain protein EFM mediates flowering responses to environmental cues in Arabidopsis. Dev. Cell, 30, 437–448.
58. Yu, Y., Liu, Z., Wang, L., Kim, S.G., Seo, P.J., Qiao, M., Wang, N. et al. (2016) WRKY71 accelerates flowering via the direct activation of FLOWERING LOCUS T and LEAFY in Arabidopsis thaliana. Plant J. 85, 96–106.
59. Zhang, B., Wang, L., Zeng, L., Zhang, C. and Ma, H. (2015) Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time. Genes Dev. 29, 975–987.