Skip to main content
Log in

SmARF8, a transcription factor involved in parthenocarpy in eggplant

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Parthenocarpic fruit is a very attractive trait for consumers and especially in eggplants where seeds can lead to browning of the flesh and bitterness. However, the molecular mechanisms underlying parthenocarpy in eggplant still remain unknown. Some auxin response factors have been previously shown in model species, such as Arabidopsis and tomato, to play an important role in such a process. Here, we have identified a natural parthenocarpic mutant and showed that ARF8 from eggplant (SmARF8), is down-regulated in buds compared to wild-type plants. Further characterization of SmARF8 showed that it is a nuclear protein and an active transcriptional regulator. We determined that amino acids 629–773 of SmARF8 act as the transcriptional activation domain, the C terminus of SmARF8 is the protein-binding domain, and that SmARF8 might form homodimers. Expression analysis in eggplant showed that SmARF8 is expressed ubiquitously in all tissues and organs and is responsive to auxin. Eggplant transgenic lines harboring RNA interference of SmARF8 exhibited parthenocarpy in unfertilized flowers, suggesting that SmARF8 negatively regulates fruit initiation. Interestingly, SmARF8-overexpressing Arabidopsis lines also induced parthenocarpy. These results indicate that SmARF8 could affect the dimerization of auxin/indole acetic acid repressors with SmARF8 via domains III and IV and thus induce fruit development. Furthermore, the introduction of SmARF8 full-length cDNA could partially complement the parthenocarpic phenotypes in Arabidopsis arf8-1 and arf8-4 mutants. Collectively, our results demonstrate that SmARF8 may act as a key negative regulator involved in parthenocarpic fruit development of eggplant. These findings give more insights into the conserved mechanisms leading to parthenocarpy in which auxin signaling plays a pivotal role, and provide potential target for eggplant breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bao CL, Du LM, Hu TH, Zhu QM, Hu HJ, Mao WH (2014) Optimization of the transgenic system and genetic transformation of SmARF8 gene RNAi vector in Red-purple Long eggplant. Acta Hortic Sin 41:1105–1114

    CAS  Google Scholar 

  • Carmi N, Salts Y, Dedicova B, Shabtai S, Barg R (2003) Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta 217:726–735

    Article  PubMed  CAS  Google Scholar 

  • Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Covington MF, Harme SL (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5:1773–1784

    Article  CAS  Google Scholar 

  • de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  PubMed  CAS  Google Scholar 

  • Du LM, Mao WH, Bao CL, Hu TH, Zhu QM, Hu HJ (2009) Cloning and characterization of ARF family gene SmARF8 in Solanum melongena L. Sci Agric Sin 42:2434–2441

    CAS  Google Scholar 

  • Ficcadenti N, Sestili S, Pandolfini T, Cirillo C, Rotino GL, Spena A (1999) Genetic engineering of parthenocarpic fruit development in tomato. Mol Breed 5:463–470

    Article  Google Scholar 

  • Fos M, Nuez F (1997) Molecular expression of genes involved in parthenocarpic fruit set in tomato. Physiol Plant 98:165–171

    Article  Google Scholar 

  • Gillaspy G, Ben-David H, Gruisserri W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Goetz M, Adam VS, Johnson DS, Koltunow AM (2006) AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18:1873–1886

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Goetz M, Hooper CL, Johnson DS, Rodrigues J, Adam VS (2007) Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol 145:351–366

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gorguet B, van Heusden AW, Lindhout P (2005) Parthenocarpic fruit development in tomato. Plant Biol 7:131–139

    Article  PubMed  CAS  Google Scholar 

  • Gray WM, Del Pozo JC, Walker L, Hobbie L, Risseeuw E (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2001) Auxin response factors: recent advances in auxin biology. J Plant Growth Regul 10:281–291

    Article  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle T, Hagen G, Ulmasov T, Murfett J (1998) How does auxin turn on genes? Plant Physiol 118:341–347

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297:793–797

    Article  PubMed  CAS  Google Scholar 

  • Jenik PD, Barton MK (2005) Surge and destroy: the role of auxin in plant embryogenesis. Development 132:3577–3585

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 285:245–260

    Article  PubMed  CAS  Google Scholar 

  • Mezzetti B, Landi L, Scortichini L, Rebori A, Spena A, Pandolfini T (2002) Genetic engineering of parthenocarpic fruit development in strawberry. Acta Hortic 567:101–104

    Article  Google Scholar 

  • Mezzetti B, Landi L, Pandolfini T, Spena A (2004) The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnol 15:1–4

    Google Scholar 

  • Miyatake K, Saito T, Negoro S, Yamaguchi H, Nunome T (2012) Development of selective markers linked to a major QTL for parthenocarpy in eggplant (Solanum melongena L.). Theor Appl Genet 124:1403–1413

    Article  PubMed  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  PubMed  CAS  Google Scholar 

  • Pandolfini T, Rotino GL, Camerini S, Defez R, Spena A (2002) Optimisation of transgene action at the post-transcriptional level: high quality parthenocarpic fruits in industrial tomatoes. BMC Biotechnol 2:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson RW, Reiners S (1999) Parthenocarpy in summer squash. HortScience 34:715–717

    Google Scholar 

  • Rogg LE, Bartel B (2001) Auxin signaling: derepression through regulated proteolysis. Dev Cell 1:595–604

    Article  PubMed  CAS  Google Scholar 

  • Rotino GL, Elena P, Michela Z, Hans S, Spena A (1997) Genetic engineering of parthenocarpic plants. Nat Biotechnol 15:1398–1401

    Article  PubMed  CAS  Google Scholar 

  • Talon M, Zacarias L, Primomillo E (1992) Gibberellins and parthenocarpic ability in developing ovaries of seedless mandarins. Plant Physiol 99:1575–1581

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tian C, Muto H, Higuchi K, Matamura T, Tatematsu K (2004) Disruption and overexpression of Auxin Response Factor8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40:333–343

    Article  PubMed  CAS  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tiwari A, Vivian-Smith A, Voorrips RE, Habets ME, Xue LB (2011) Parthenocarpic potential in Capsicum annuum L. is enhanced by carpelloid structures and controlled by a single recessive gene. BMC Plant Biol 11:143

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997a) ARF1, a transcription factor that binds auxin response elements. Science 276:1865–1868

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997b) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin response factors. Proc Natl Acad Sci USA 96:5844–5849

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319

    Article  PubMed  CAS  Google Scholar 

  • Varoquaux F, Blanvillain R, Delseny M, Gallois P (2000) Less is better: new approaches for seedless fruit production. Trends Biotechnol 18:233–242

    Article  PubMed  CAS  Google Scholar 

  • Vivian-Smith AM, Koltunow A (1999) Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol 121:437–452

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Vivian-Smith A, Luo M, Chaudhury A, Koltunow A (2001) Fruit development is actively restricted in the absence of fertilization in Arabidopsis. Development 128:2321–2331

    PubMed  CAS  Google Scholar 

  • Waller F, Furuya M, Nick P (2002) OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol Biol 50:415–425

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24

    Article  PubMed  CAS  Google Scholar 

  • Zouine M, Fu Y, Chateigner-BoutinAL Mila I, Frasse P, WangH AudranC, RoustanJP BouzayenM (2014) Characterization of the Tomato ARF Gene Family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS ONE 9:e84203

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Kotaro Yamamoto for supplying arf8-1 seeds and Marc Goetz for supplying arf8-4. This research was partially funded by the Zhejiang Provincial major Agricultural Science and Technology Projects of New Varieties Breeding (2012C12903), National High Technology Research and Development Program (“863”Program) of China (#2012AA100103).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Weihai Mao.

Ethics declarations

Conflict of interest

Liming Du declares that she has no conflict of interest. Chonglai Bao declares that he has no conflict of interest. Tianhua hu declares that he has no conflict of interest. Qinmei Zhu declares that she has no conflict of interest. Haijiao Hu declares that she has no conflict of interest. Qunyan He declares that she has no conflict of interest. Weihai Mao declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Du, L., Bao, C., Hu, T. et al. SmARF8, a transcription factor involved in parthenocarpy in eggplant. Mol Genet Genomics 291, 93–105 (2016). https://doi.org/10.1007/s00438-015-1088-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1088-5

Keywords

Navigation