Skip to main content
SpringerLink
Log in

Over-expression of Peach PpIAA19 in Tomato Alters Plant Growth, Parthenocarpy, and Fruit Shape

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The auxin/indole acetic acid (Aux/IAA) genes encode a large family of short-lived proteins that regulate auxin signaling in plants. Previous attempts to understand the role of auxin during fruit development in peach (Prunus persica) found that expression of the Aux/IAA gene PpIAA19 was upregulated during fruit ripening, but the biological significance of the PpIAA19 protein is still unknown. The current study detected PpIAA19 transcripts in all peach plant tissues but found higher levels of accumulation in fruit S1 and S4II stages. During fruit ripening, the expression level of the PpIAA19 gene in melting flesh (MF) peach fruit was unsurprisingly higher than in stony hard (SH) peach fruit. Tomato (Solanum lycopersicum cv. ‘Micro-Tom’) was used as a model for investigating the phenotypic and molecular changes associated with over-expression of PpIAA19. This revealed that PpIAA19 was involved in regulating tomato lateral root number, stem elongation, parthenocarpy, and fruit shape. Molecular analyses of transgenic tomato plants over-expressing PpIAA19 indicated that the observed phenotypic changes were partially mediated by regulating the expression of auxin response genes. This result extends the functional characterization of PpIAA19 in tomato, and broadens our understanding of the role of auxin signaling in regulating plant growth and development.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Audran-Delalande C, Bassa C, Mila I, Regad F, Zouine M, Bouzayen M (2012) Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol 53:659–672

    Article  CAS  PubMed  Google Scholar 

  • Bargman BOR, Estelle M (2014) Auxin perception: in the IAA of the beholder. Physiol Plant 151:52–61

    Article  CAS  Google Scholar 

  • Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012) Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol 53:1583–1595

    Article  CAS  PubMed  Google Scholar 

  • Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP, Hao Y, Yifhar T, Yasuor H, Zouine M, Bouzayen M, Granell RA, Rogachev I, Aharoni A (2016) AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genet 12:e1005903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaabouni S, Jones B, Delalande C, Wang H, Li Z, Mila I. Frasse P, Latché A, Pech JC, Bouzayen M (2009a) Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J Exp Bot 60:1349–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaabouni S, Latché A, Pech JC, Bouzayen M (2009b) Tomato Aux/IAA3 and HOOKLESS are important actors of the interplay between auxin and ethylene during apical hook formation. Plant Signal Behav 4:559–560

    Article  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  CAS  PubMed  Google Scholar 

  • Deng W, Yang Y, Ren Z, Audran-Delalande C, Mila I, Wang X, Song H, Hu Y, Bouzayen M, Li Z (2012) The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytol 194:379–390

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  CAS  PubMed  Google Scholar 

  • El-Sharkawy I, Sherif S, El Kayal W, Jones B, Li Z, Sullivan AJ, Jayasankar S (2016) Overexpression of plum auxin receptor PslTIR1 in tomato alters plant growth, fruit development and fruit shelf-life characteristics. BMC Plant Biol 16:56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168

    Article  CAS  PubMed  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Hammerschlag FA, Bauchan GR, Scorza R (1987) Factors influencing in vitro multiplication and rooting of peach cultivars. Plant Cell Tissue Organ Cult 8:235–242

    Article  CAS  Google Scholar 

  • Hao YW, Hu GJ, Breitel D, Liu MC, Mila I, Frasse P, Fu YY, Aharoni A, Bouzayen M, Zouine M (2015) Auxin response factor SlARF2 is an essential component of the regulatory mechanism controlling fruit ripening in tomato. PLoS Genet 11:e1005649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, Latché A, Pech JC, Bouzayen M (2002) Down-regulation of DR12, an auxin response factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J 32:603–613

    Article  CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Kloosterman B, Visser RG, Bachem CW (2006) Isolation and characterization of a novel potato Auxin/Indole-3-Acetic Acid family member (StIAA2) that is involved in petiole hyponasty and shoot morphogenesis. Plant Physiol Biochem 44:766–775

    Article  CAS  PubMed  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950

    Article  CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan L, Zeng W, Niu L, Lu Z, Liu H, Cui G, Zhu Y, Chu J, Li W, Fang W, Cai Z, Li G, Wang Z (2015) PpYUC11, a strong candidate gene for the stony hard phenotype in peach (Prunus persica L. Batsch), participates in IAA biosynthesis during fruit ripening. J Exp Bot 66:7031–7044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Z, Liu R, Gu W, Dong X (2017) The Solanum lycopersicum auxin response factor SlARF2 participates in regulating lateral root formation and flower organ senescence. Plant Sci 256:103–111

    Article  CAS  PubMed  Google Scholar 

  • Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373

    Article  CAS  PubMed  Google Scholar 

  • Su LY, Audran C, Bouzayen M, Roustan JP, Chervin C (2015) The Aux/IAA, Sl-IAA17 regulates quality parameters over tomato fruit development. Plant Signal Behav 10:e1071001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun HJ, Uchii S, Watanabe S, Ezura H (2006) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47:426–431

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatsuki M, Nakajima N, Fujii H, Shimada T, Nakano M, Hayashi KI, Hayama H, Yoshioka H, Nakamura Y (2013) Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch). J Exp Bot 64:1049–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Bio 7:847–859

    Article  CAS  Google Scholar 

  • Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721

    CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308

    Article  CAS  PubMed  Google Scholar 

  • Uehara T, Okushima Y, Mimura T, Tasaka M, Fukaki H (2008) Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana. Plant Cell Physiol 49:1025–1038

    Article  CAS  PubMed  Google Scholar 

  • Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel LA, Decroocq V, Sosinski B, Prochnik S, Mitros T, Policriti A, Cipriani G, Dondini L, Ficklin S, Goodstein DM, Xuan P, Del Fabbro C, Aramini V, Copetti D, Gonzalez S, Horner DS, Falchi R, Lucas S, Mica E, Maldonado J, Lazzari B, Bielenberg D, Pirona R, Miculan M, Barakat A, Testolin R, Stella A, Tartarini S, Tonutti P, Arús P, Orellana A, Wells C, Main D, Vizzotto G, Silva H, Salamini F, Schmutz J, Morgante M, Rokhsar DS (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché A, Pech JC, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché A, Pech JC, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and-independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21:1428–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zažímalová E, Petrášek J, Benková E (2014) Auxin and its role in plant development, vol 136. Springer, Vienna, pp 2675–2688

    Book  Google Scholar 

  • Zeng W, Pan L, Liu H, Niu L, Lu Z, Cui G, Wang Z (2015) Characterization of 1-aminocyclopropane-1-carboxylic acid synthase (ACS) genes during nectarine fruit development and ripening. Tree Genet Genomes 11:1–10

    Article  Google Scholar 

  • Zeng W, Wang X, Pan L, Niu L, Lu Z, Cui G, Wang Z (2017) Identification and expression profiling of Aux/IAA family gene during peach fruit ripening. Acta Hortic Sin 44:233–244

    Google Scholar 

  • Zouine M, Fu Y, Chateigner-Boutin AL, Mila I, Frasse P, Wang H, Audran C, Roustan JP, Bouzayen M (2014) Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS ONE 9:e84203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The research was financially supported by the National Natural Science Foundation of China (No. 31501732), the Agricultural Science and Technology Innovation Program (ASTIP) (CAAS-ASTIP-2018-ZFRI), and Central Public-interest Scientific Institution Basal Research Fund (1610192017103).

Author information

Author notes

    Authors and Affiliations

    1. Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, 450009, People’s Republic of China

      Yifeng Ding, Wenfang Zeng, Xiaobei Wang, Yan Wang, Liang Niu, Lei Pan, Zhenhua Lu, Guochao Cui & Zhiqiang Wang

    2. Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

      Yifeng Ding & Guohuai Li

    Authors
    1. Yifeng Ding
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Wenfang Zeng
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xiaobei Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yan Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Liang Niu
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Lei Pan
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Zhenhua Lu
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Guochao Cui
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Guohuai Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Zhiqiang Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Contributions

    WZ and ZW conceived the experiments; YD, XW, and YW collected plant materials and conducted the experiments; LN, LP, ZL, and GC performed phenotyping; YD and WZ analyzed the data; and WZ, GL, and ZW wrote the manuscript.

    Corresponding authors

    Correspondence to Guohuai Li or Zhiqiang Wang.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Yifeng Ding and Wenfang Zeng have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 2244 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Ding, Y., Zeng, W., Wang, X. et al. Over-expression of Peach PpIAA19 in Tomato Alters Plant Growth, Parthenocarpy, and Fruit Shape. J Plant Growth Regul 38, 103–112 (2019). https://doi.org/10.1007/s00344-018-9813-z

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00344-018-9813-z

    Keywords

    Search

    Navigation