Advertisement

Planta

, Volume 250, Issue 1, pp 173–185 | Cite as

Overexpression of a basic helix–loop–helix transcription factor gene, SlbHLH22, promotes early flowering and accelerates fruit ripening in tomato (Solanum lycopersicum L.)

  • Muhammad Waseem
  • Ning Li
  • Deding Su
  • Jingxuan Chen
  • Zhengguo LiEmail author
Original Article

Abstract

Main conclusion

The overexpression of SlbHLH22 functioned in controlling flowering time, accelerated fruit ripening, and produced more ethylene-producing phenotypes in tomato.

Abstract

Flowering and fruit ripening are two complex transition processes regulated by various internal and external factors that ultimately lead to fruit maturation and final seed dispersal. The basic helix–loop–helix (bHLH) transcription factor is the largest TF gene family in plants that controls various biological and developmental aspects, but the actual roles of these genes have not been fully studied. Here, we performed a functional characterization of the bHLH gene SlbHLH22 in tomato. SlbHLH22 was fully expressed in tomato flowers, while a moderate expression level was also observed in fruits at different developmental stages. Overexpression of the SlbHLH22 gene revealed that it is highly involved in controlling flowering time, through the activation of the SlSFT or SlLFY genes, and promoting fruit ripening and improved carotenoid accumulation. The expression patterns of carotenoid-related genes (SlPYS1) were also upregulated in transgenic tomato fruits. In transgenic tomato fruit, we observed clear changes in colour from green to orange with enhanced expression of the SlbHLH22 gene. SlbHLH22 was upregulated under exogenous ACC, IAA, ABA, and ethephon. Overexpression of SlbHLH22 also promotes ethylene production. Moreover, ethylene biosynthesis and perception genes (SlACO3, SlACS1, SlACS2, SlACS4, SlACS1a, SlEIN1, SlEIN2, SlEIN3, SlEIN4, SlETR2, SlETR3, SlSAM3, and SlSAMS) were upregulated. Ripening-related genes (SlAP2a, SlCNR, SlNOR, SlMYB, and SlTAG) were consistent in their expression pattern in transgenic plants. Finally, our study provides evidence that tomato bHLH genes play an important role in flowering, fruit ripening, and development.

Keywords

bHLH Ethylene Flowering Perception Phytohormone Pigmentation 

Abbreviations

ACC

1-Aminocyclopropane-1-carboxylate

ACO

1-Aminocyclopropane-1-carboxylate oxidase

ACS

1-Aminocyclopropane-1-carboxylate synthase

bHLH

Basic helix–loop–helix

DPA

Days post-anthesis

TFs

Transcription factors

Notes

Acknowledgements

This work was supported by the National Key Research and Development Program (2016YFD0400101), the National Natural Science Foundation of China (31572175), and the Committee of Science and Technology of Chongqing (cstc2014kjcxljrc0020).

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

425_2019_3157_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 20 kb)

References

  1. Adams DO, Yang SF (1977) Methionine metabolism in apple tissue: implication of s-adenosylmethionine as an intermediate in the conversion of methionine to ethylene. Plant Physiol 60(6):892–896CrossRefGoogle Scholar
  2. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53(377):2039–2055CrossRefGoogle Scholar
  3. Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9(4):525–535CrossRefGoogle Scholar
  4. Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123(3):979–986.  https://doi.org/10.1104/pp.123.3.979 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bernhardt C, Lee MM, Gonzalez A, Zhang F, Lloyd A, Schiefelbein J (2003) The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130(26):6431CrossRefGoogle Scholar
  6. Bird CR, Ray JA, Fletcher JD, Boniwell JM, Bird AS, Teulieres C, Blain I, Bramley PM, Schuch W (1991) using antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes. Bio/Technol 9:635.  https://doi.org/10.1038/nbt0791-635 CrossRefGoogle Scholar
  7. Bramley PM (2002) Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot 53(377):2107–2113.  https://doi.org/10.1093/jxb/erf059 CrossRefPubMedGoogle Scholar
  8. Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, Klein P, Giovannoni J (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64(6):936–947.  https://doi.org/10.1111/j.1365-313X.2010.04384.x CrossRefPubMedGoogle Scholar
  9. Costa F, Alba R, Schouten H, Soglio V, Gianfranceschi L, Serra S, Musacchi S, Sansavini S, Costa G, Fei Z, Giovannoni J (2010) Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol 10:229.  https://doi.org/10.1186/1471-2229-10-229 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dong J, Ni W, Yu R, Deng XW, Chen H, Wei N (2017) Light-dependent degradation of PIF3 by SCFEBF1/2 promotes a photomorphogenic response in Arabidopsis. Curr Biol 27(16):2420–2430.e2426.  https://doi.org/10.1016/j.cub.2017.06.062 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fairchild CD, Schumaker MA, Quail PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14(18):2377–2391PubMedPubMedCentralGoogle Scholar
  12. Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium Tumefaciens vector. Bio/Technol 5:726.  https://doi.org/10.1038/nbt0787-726 CrossRefGoogle Scholar
  13. Fish WW, Perkins-Veazie P, Collins JK (2002) A quantitative assay for lycopene that utilizes reduced volumes of organic solvents. J Food Compos Anal 15(3):309–317.  https://doi.org/10.1006/jfca.2002.1069 CrossRefGoogle Scholar
  14. Forth D, Pyke KA (2006) The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. J Exp Bot 57(9):1971–1979.  https://doi.org/10.1093/jxb/erj144 CrossRefPubMedGoogle Scholar
  15. Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol 105(1):405–413CrossRefGoogle Scholar
  16. Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, Kasumi T, Ito Y (2012) Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235(6):1107–1122.  https://doi.org/10.1007/s00425-011-1561-2 CrossRefPubMedGoogle Scholar
  17. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53(5):717–730.  https://doi.org/10.1111/j.1365-313X.2007.03362.x CrossRefGoogle Scholar
  18. Gao Y, Wei W, Zhao X, Tan X, Fan Z, Zhang Y, Jing Y, Meng L, Zhu B, Zhu H, Chen J, Jiang C-Z, Grierson D, Luo Y, Fu D-Q (2018) A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic Res 5:75–75.  https://doi.org/10.1038/s41438-018-0111-5 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gao Y, Zhu N, Zhu X, Wu M, Jiang C-Z, Grierson D, Luo Y, Shen W, Zhong S, Fu D-Q, Qu G (2019) Diversity and redundancy of the ripening regulatory networks revealed by the fruit ENCODE and the new CRISPR/Cas9 CNR and NOR mutants. Hortic Res 6:39–39.  https://doi.org/10.1038/s41438-019-0122-x CrossRefPubMedPubMedCentralGoogle Scholar
  20. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180.  https://doi.org/10.1105/tpc.019158 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Giovannoni JJ, Noensie EN, Ruezinsky DM, Lu X, Tracy SL, Ganal MW, Martin GB, Pillen K, Alpert K, Tanksley SD (1995) Molecular genetic analysis of the ripening-inhibitor and non-ripening loci of tomato: a first step in genetic map-based cloning of fruit ripening genes. Mol Gen Genet 248(2):195–206CrossRefGoogle Scholar
  22. Groszmann M, Paicu T, Smyth DR (2008) Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant J 55:40–52.  https://doi.org/10.1111/j.1365-313X.2008.03469.x CrossRefPubMedGoogle Scholar
  23. Hiwasa K (2003) Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit. J Exp Bot 54(383):771–779.  https://doi.org/10.1093/jxb/erg073 CrossRefPubMedGoogle Scholar
  24. Hu ZL, Chen XQ, Chen GP, Lü LJ, Donald G (2007) The influence of co-suppressing tomato 1-aminocyclopropane-1-carboxylic acid oxidase I on the expression of fruit ripening-related and pathogenesis-related protein genes. Agric Sci China 6(413):406–413.  https://doi.org/10.1016/S1671-2927(07)60063-7 CrossRefGoogle Scholar
  25. Ichihashi Y, Horiguchi G, Gleissberg S, Tsukaya H (2010) The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant Cell Physiol 51(2):252–261.  https://doi.org/10.1093/pcp/pcp184 CrossRefPubMedGoogle Scholar
  26. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60(6):1081–1095.  https://doi.org/10.1111/j.1365-313X.2009.04064.x CrossRefPubMedGoogle Scholar
  27. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55(2):212–223.  https://doi.org/10.1111/j.1365-313X.2008.03491.x CrossRefPubMedGoogle Scholar
  28. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Toki S (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun 467(1):76–82.  https://doi.org/10.1016/j.bbrc.2015.09.117 CrossRefPubMedGoogle Scholar
  29. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Shima Y, Nakamura N, Kotake-Nara E, Kawasaki S, Toki S (2017) Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nat Plants 3(11):866–874.  https://doi.org/10.1038/s41477-017-0041-5 CrossRefPubMedGoogle Scholar
  30. Jones S (2004) An overview of the basic helix-loop-helix proteins. Genome Biol 5(6):226.  https://doi.org/10.1186/gb-2004-5-6-226 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23(3):923–941.  https://doi.org/10.1105/tpc.110.081273 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kneissl ML, Deikman J (1996) The tomato E8 gene influences ethylene biosynthesis in fruit but not in flowers. Plant Physiol 112(2):537–547CrossRefGoogle Scholar
  33. Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6(4):521–530.  https://doi.org/10.1105/tpc.6.4.521 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Li S, Xu H, Ju Z, Cao D, Zhu H, Fu D, Grierson D, Qin G, Luo Y, Zhu B (2018) The RIN-MC fusion of MADS-box transcription factors has transcriptional activity and modulates expression of many ripening genes. Plant Physiol 176(1):891.  https://doi.org/10.1104/pp.17.01449 CrossRefPubMedGoogle Scholar
  35. Lifschitz E, Eshed Y (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J Exp Bot 57:3405–3414CrossRefGoogle Scholar
  36. Lincoln JE, Fischer RL (1988a) Diverse mechanisms for the regulation of ethylene-inducible gene expression. Mol Gen Genet 212(71):71–75.  https://doi.org/10.1007/BF00322446 CrossRefPubMedGoogle Scholar
  37. Lincoln JE, Fischer RL (1988b) Regulation of gene expression by ethylene in wild-type and rin tomato (Lycopersicon esculentum) fruit. Plant Physiol 88(2):370–374.  https://doi.org/10.1104/pp.88.2.370 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lincoln JE, Cordes S, Read E, Fischer RL (1987) Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proc Natl Acad Sci USA 84(9):2793–2797.  https://doi.org/10.1073/pnas.84.9.2793 CrossRefPubMedGoogle Scholar
  39. Liu L, Wei J, Zhang M, Zhang L, Li C, Wang Q (2012) Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates. J Exp Bot 63(16):5751–5761.  https://doi.org/10.1093/jxb/ers224 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liu Y, Li X, Li K, Liu H, Lin C (2013) Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet 9(10):e1003861.  https://doi.org/10.1371/J.pgen.1003861 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liu M, Pirrello J, Chervin C, Roustan J-P, Bouzayen M (2015) Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol 169(4):2380–2390.  https://doi.org/10.1104/pp.15.01361 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  43. Luengo E, Álvarez I, Raso J (2014) Improving carotenoid extraction from tomato waste by pulsed electric fields. Front Nutr 1:12–12.  https://doi.org/10.3389/fnut.2014.00012 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157(3):1568–1579.  https://doi.org/10.1104/pp.111.181107 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613.  https://doi.org/10.1038/nbt0602-613 CrossRefPubMedGoogle Scholar
  46. Molinero-Rosales N, Latorre A, Jamilena M, Lozano R (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta 218(3):427–434.  https://doi.org/10.1007/s00425-003-1109-1 CrossRefPubMedGoogle Scholar
  47. Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118(4):1295–1305CrossRefGoogle Scholar
  48. Navarro C, Abelenda JA, Cruz-Oro E, Cuellar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478(7367):119–122.  https://doi.org/10.1038/nature10431 CrossRefGoogle Scholar
  49. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95(5):657–667.  https://doi.org/10.1016/S0092-8674(00)81636-0 CrossRefPubMedGoogle Scholar
  50. Nukumizu Y, Wada T, Tominaga-Wada R (2013) Tomato (Solanum lycopersicum) homologs of TRIPTYCHON (SlTRY) and GLABRA3 (SlGL3) are involved in anthocyanin accumulation. Plant Signal Behav 8(7):e24575.  https://doi.org/10.4161/psb.24575 CrossRefPubMedPubMedCentralGoogle Scholar
  51. O’Donnell PJ, Schmelz E, Block A, Miersch O, Wasternack C, Jones JB, Klee HJ (2003) Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol 133(3):1181–1189.  https://doi.org/10.1104/pp.103.030379 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Oeller PW, Lu MW, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254(5030):437–439.  https://doi.org/10.1126/science.1925603 CrossRefPubMedGoogle Scholar
  53. Oetiker JH, Olson DC, Shiu OY, Yang SF (1997) Differential induction of seven 1-aminocyclopropane-1-carboxylate synthase genes by elicitor in suspension cultures of tomato (Lycopersicon esculentum). Plant Mol Biol 34(2):275–286.  https://doi.org/10.1023/A:1005800511372 CrossRefPubMedGoogle Scholar
  54. Ohno S, Hosokawa M, Hoshino A, Kitamura Y, Morita Y, Park K II, Nakashima A, Deguchi A, Tatsuzawa F, Doi M, Iida S, Yazawa S (2011) A bHLH transcription factor, DvIVS, is involved in regulation of anthocyanin synthesis in dahlia (Dahlia variabilis). J Exp Bot 62(14):5105–5116.  https://doi.org/10.1093/jxb/err216 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Olson DC, White JA, Edelman L, Harkins RN, Kende H (1991) Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proc Natl Acad Sci USA 88(12):5340–5344.  https://doi.org/10.1073/pnas.88.12.5340 CrossRefPubMedGoogle Scholar
  56. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330(6009):1397–1400.  https://doi.org/10.1126/science.1197004 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena—an overview. Crit Rev Food Sci 47(1):1–19.  https://doi.org/10.1080/10408390600976841 CrossRefGoogle Scholar
  58. Qiu Z, Wang X, Gao J, Guo Y, Huang Z, Du Y (2016) The tomato Hoffman’s Anthocyaninless gene encodes a bHLH transcription factor involved in anthocyanin biosynthesis that is developmentally regulated and induced by low temperatures. PLoS One 11(3):e0151067.  https://doi.org/10.1371/J.pone.0151067 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Roy SK (1973) Simple and rapid methods for the estimation of total carotenoids pigments in mango. J Food Sci Technol 10(1):45–46Google Scholar
  60. Seo PJ, Hong SY, Kim SG, Park CM (2011) Competitive inhibition of transcription factors by small interfering peptides. Trends Plant Sci 16(10):541–549.  https://doi.org/10.1016/j.tplants.2011.06.001 CrossRefPubMedGoogle Scholar
  61. Sorensen A, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33(2):413–423.  https://doi.org/10.1046/j.1365-313X.2003.01644.x CrossRefPubMedGoogle Scholar
  62. Su L, Diretto G, Purgatto E, Danoun S, Zouine M, Li Z, Roustan JP, Bouzayen M, Giuliano G, Chervin C (2015) Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance. BMC Plant Biol 15:114.  https://doi.org/10.1186/s12870-015-0495-4 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sun H, Fan HJ, Ling HQ (2015) Genome-wide identification and characterization of the bHLH gene family in tomato. BMC Genomics 16:9.  https://doi.org/10.1186/s12864-014-1209-2 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Tani E, Tsaballa A, Stedel C, Kalloniati C, Papaefthimiou D, Polidoros A, Darzentas N, Ganopoulos I, Flemetakis E, Katinakis P, Tsaftaris A (2011) The study of a SPATULA-like bHLH transcription factor expressed during peach (Prunus persica) fruit development. Plant Physiol Biochem 49(6):654–663.  https://doi.org/10.1016/j.plaphy.2011.01.020 CrossRefPubMedGoogle Scholar
  65. Tiwari SB, Shen Y, Chang HC, Hou Y, 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(1):57–66.  https://doi.org/10.1111/j.1469-8137.2010.03251.x CrossRefGoogle Scholar
  66. Tominaga-Wada R, Iwata M, Nukumizu Y, Sano R, Wada T (2012) A full-length R-like basic-helix-loop-helix transcription factor is required for anthocyanin upregulation whereas the N-terminal region regulates epidermal hair formation. Plant Sci 183:115–122.  https://doi.org/10.1016/j.plantsci.2011.11.010 CrossRefPubMedGoogle Scholar
  67. Ververidis P, John P (1991) Complete recovery in vitro of ethylene-forming enzyme activity. Phytochemistry 30(3):725–727.  https://doi.org/10.1016/0031-9422(91)85241-Q CrossRefGoogle Scholar
  68. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296(5566):343–346.  https://doi.org/10.1126/science.1068181 CrossRefPubMedGoogle Scholar
  69. Wang F, Lin R, Feng J, Qiu D, Chen W, Xu S (2015) Wheat bHLH transcription factor gene, TabHLH060, enhances susceptibility of transgenic Arabidopsis thaliana to Pseudomonas syringae. Physiol Mol Plant 90:123–130.  https://doi.org/10.1016/j.pmpp.2015.04.007 CrossRefGoogle Scholar
  70. Weng L, Bai X, Zhao F, Li R, Xiao H (2016) Manipulation of flowering time and branching by overexpression of the tomato transcription factor SlZFP2. Plant Biotechnol J 14(12):2310–2321.  https://doi.org/10.1111/pbi.12584 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 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(5737):1056–1059.  https://doi.org/10.1126/science.1114358 CrossRefGoogle Scholar
  72. Xie X, Li S, Zhang R, Zhao J, Chen Y, Zhao Q, Yao Y, You C, Zhang X, Hao Y (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ 35(11):1884–1897.  https://doi.org/10.1111/j.1365-3040.2012.02523.x CrossRefPubMedGoogle Scholar
  73. Xu R, Goldman S, Coupe S, Deikman J (1996) Ethylene control of E4 transcription during tomato fruit ripening involves two cooperative cis elements. Plant Mol Biol 31(6):1117–1127.  https://doi.org/10.1007/BF00040829 CrossRefPubMedGoogle Scholar
  74. Yin J, Chang X, Kasuga T, Bui M, Reid MS, Jiang C-Z (2015) A basic helix-loop-helix transcription factor, PhFBH4, regulates flower senescence by modulating ethylene biosynthesis pathway in petunia. Hortic Res 2:15059.  https://doi.org/10.1038/hortres.2015.59 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yu Y, Liu Z, Wang L, Kim S-G, Seo PJ, Qiao M, Wang N, Li S, Cao X, Park C-M, Xiang F (2016) WRKY71 accelerates flowering via the direct activation of FLOWERING LOCUS T and LEAFY in Arabidopsis thaliana. Plant J 85(1):96–106.  https://doi.org/10.1111/tpj.13092 CrossRefPubMedGoogle Scholar
  76. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling H-Q (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385.  https://doi.org/10.1038/cr.2008.26 CrossRefGoogle Scholar
  77. Zhu Z, Chen G, Guo X, Yin W, Yu X, Hu J, Hu Z (2017) Overexpression of SlPRE2, an atypical bHLH transcription factor, affects plant morphology and fruit pigment accumulation in tomato. Sci Rep 7(1):5786.  https://doi.org/10.1038/s41598-017-04092-y CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Life SciencesChongqing UniversityChongqingPeople’s Republic of China
  2. 2.Key Laboratory of Functional Gene and Regulation Technologies Under Chongqing Municipal Education CommissionChongqingPeople’s Republic of China

Personalised recommendations