Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 189–198 | Cite as

Involvement of Indole-3-Acetic Acid Metabolism in the Early Fruit Development of the Parthenocarpic Tomato Cultivar, MPK-1

  • Rihito TakisawaEmail author
  • Hideto Kusaka
  • Yuto Nishino
  • Masahiro Miyashita
  • Hisashi Miyagawa
  • Tetsuya Nakazaki
  • Akira Kitajima


Parthenocarpy, or fruit set and growth without fertilization, is a desirable trait in tomato cultivation as it reduces the cost of tomato production. MPK-1 is a Japanese parthenocarpic tomato cultivar, and the gene responsible for parthenocarpy of MPK-1 is Pat-k. As MPK-1 is a stable parthenocarpic tomato cultivar, we investigated the physiological mechanism of parthenocarpy in this cultivar. Indole-3-acetic acid (IAA) is considered as the main factor contributing to parthenocarpy, as its exogenous application to unpollinated ovaries triggers parthenocarpic fruit development in tomato. In this study, we investigated the level of IAA and its metabolites and the expression of genes involved in IAA metabolism in unpollinated ovaries of MPK-1. We observed an increase in the level of IAA accompanied by an elevated level of expression of an IAA biosynthesis gene, ToFZY5 in parthenocarpic ovaries of MPK-1. Simultaneously, the level of IAA-glutamate (IAA-Glu), one of the IAA conjugates comprising a potential IAA inactivation pathway, was also increased. These results suggest that the increase in IAA levels, driven by the up-regulation of IAA biosynthesis genes, promotes the growth of parthenocarpic fruits in MPK-1, and that the IAA synthesized in parthenocarpic ovaries is primarily metabolized to IAA-Glu. In addition, expression profiles of some genes involved in IAA metabolism were different between pollinated and parthenocarpic ovaries, suggesting that the specific transcriptional regulation of IAA metabolism in parthenocarpic ovaries of MPK-1 differs from that in pollinated ovaries.


Fruit development Indole-3-acetic acid Parthenocarpy Tomato 



This work was supported by a Grant-in-Aid for Young Scientists (B) [15K18639] from the Japan Society for the Promotion of Science.

Compliance with Ethical Standards

Conflict interests

The authors declare that they have no conflict interests.

Supplementary material

344_2018_9826_MOESM1_ESM.xlsx (18 kb)
Supplementary material 1 (XLSX 17 KB)


  1. Böttcher C, Boss PK, Davies C (2011) Acyl substrate preferences of an IAA-amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. J Exp Bot 62:4267–4280CrossRefGoogle Scholar
  2. Cheniclet C, Rong W, Causse M, Frangne N, Bolling L (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant physiology (Bethesda) 139:1984–1994CrossRefGoogle Scholar
  3. de Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532CrossRefGoogle Scholar
  4. Expósito-Rodriguez M, Borges AA, Borges-Perez A, Perez JA (2011) Gene structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like flavin monooxygenases: the ToFZY gene family. Plant Physiol Biochem 49:782–791CrossRefGoogle Scholar
  5. Fos M, Nuez F, Garcia-Martinez JL (2000) The gene pat-2, which induces natural parthenocarpy, alters the gibberellin content in unpollinated tomato ovaries. Plant Physiol 122:471–480CrossRefGoogle Scholar
  6. Fos M, Proano K, Nuez F, Garcia-Martinez J (2001) Role of gibberellins in parthenocarpic fruit development induced by the genetic system pat-3/pat-4 in tomato. Physiol Plant 111:545–550CrossRefGoogle Scholar
  7. George WL, Scott JW, Splittstoesser WE (1984) Parthenocarpy in tomato. Hortic Rev 6:65–84Google Scholar
  8. Gillaspy G, Bendavid H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451CrossRefGoogle Scholar
  9. Gorguet B, van Heusden AW, Lindhout P (2005) Parthenocarpic fruit development in tomato. Plant Biol 7:131–139CrossRefGoogle Scholar
  10. Gorguet B, Eggink PM, Ocana J, Tiwari A, Schipper D, Finkers R, Visser RG, van Heusden AW (2008) Mapping and characterization of novel parthenocarpy QTLs in tomato. Theor Appl Genet 116:755–767CrossRefGoogle Scholar
  11. Hagen G, Guilfoyle TJ (1985) Rapid induction of selective transcription by auxins. Mol Cell Biol 5:1197–1203CrossRefGoogle Scholar
  12. Kataoka K, Okita H, Uemachi A, Yazawa S (2004) A pseudoembryo highly stainable with toluidine blue O may induce fruit growth of parthenocarpic tomato. Acta Hortic 637:213–221CrossRefGoogle Scholar
  13. Klap C, Yeshayahou E, Bolger AM, Arazi T, Gupta SK, Shabtai S, Usadel B, Salts Y, Barg R (2017) Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function. Plant Biotechnol J 15:634–647CrossRefGoogle Scholar
  14. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555CrossRefGoogle Scholar
  15. Kumar R, Agarwal P, Tyagi AK, Sharma AK (2012) Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genom 287:221–235CrossRefGoogle Scholar
  16. Liao D, Chen X, Chen A, Wang H, Liu J, Liu J, Gu M, Sun S, Xu G (2015) The characterization of six auxin-induced tomato GH3 genes uncovers a member, SlGH3.4, strongly responsive to arbuscular mycorrhizal symbiosis. Plant Cell Physiol 56:674–687CrossRefGoogle Scholar
  17. Mapelli (1978) Relationship between set, development and activities of growth regulators in tomato fruits. Plant Cell Physiol 19:1281–1288Google Scholar
  18. Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N (2011) Fruit-set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents. J Plant Growth Regul 30:405–415CrossRefGoogle Scholar
  19. Mignolli F, Mariotti L, Lombardi L, Vidoz ML, Ceccarelli N, Picciarelli P (2012) Tomato fruit development in the auxin-resistant dgt mutant is induced by pollination but not by auxin treatment. J Plant Physiol 169:1165–1172CrossRefGoogle Scholar
  20. Olimpieri I, Siligato F, Caccia R, Mariotti L, Ceccarelli N, Soressi GP, Mazzucato A (2007) Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis. Planta 226:877–888CrossRefGoogle Scholar
  21. Pattison RJ, Csukasi F, Zheng Y, Fei Z, van der Knaap E, Catala C (2015) Comprehensive tissue-specific transcriptome analysis reveals distinct regulatory programs during early tomato fruit development. Plant Physiol 168:1684–1701CrossRefGoogle Scholar
  22. Peat TS, Böttcher C, Newman J, Lucent D, Cowieson N, Davies C (2012) Crystal structure of an indole-3-acetic acid amido synthetase from grapevine involved in auxin homeostasis. Plant Cell 24:4525–4538CrossRefGoogle Scholar
  23. Picken AJF (1984) A Review of pollination and fruit-set in the tomato (Lycopersicon esculentum Mill). J Hortic Sci 59:1–13CrossRefGoogle Scholar
  24. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665CrossRefGoogle Scholar
  25. Sjut V, Bangerth F (1983) Induced parthenocarpy—a way of changing the levels of endogenous hormones in tomato fruit (Lycopersicon esculentum Mill.) 1. Extractable hormones. Plant Growth Regul 1:243–251Google Scholar
  26. Sotelo-Silveira M, Marsch-Martinez N, de Folter S (2014) Unraveling the signal scenario of fruit set. Planta 239:1147–1158CrossRefGoogle Scholar
  27. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627CrossRefGoogle Scholar
  28. Takisawa R, Kataoka K, Kitajima A (2012) Inhibition of seed formation by anomalous ovule in ‘Kyo-temari’, a parthenocarpic tomato (Solanum lycopersicum L.) cultivar. J Jpn Soc Hortic Sci 81:251–256CrossRefGoogle Scholar
  29. Takisawa R, Maruyama T, Nakazaki T, Kataoka K, Saito H, Koeda S, Nunome T, Fukuoka H, Kitajima A (2017) Parthenocarpy in the tomato (Solanum lycopersicum L.) cultivar ‘MPK-1’ is controlled by a novel parthenocarpic gene. Hortic J 86:487–492CrossRefGoogle Scholar
  30. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche´ A, Pech J-C, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692CrossRefGoogle Scholar
  31. Westfall CS (2010) Modulating plant hormones by enzyme action The GH3 family of acyl acid amido synthetases. Plant Signal Behav 5:1607–1612CrossRefGoogle Scholar
  32. Zhang S, Xu M, Qiu Z, Wang K, Du Y, Gu L, Cui X (2016) Spatiotemporal transcriptome provides insights into early fruit development of tomato (Solanum lycopersicum). Sci Rep 6:23173CrossRefGoogle Scholar
  33. Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338CrossRefGoogle Scholar
  34. 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:e84203CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of AgricultureKyoto UniversityKizugawaJapan
  2. 2.Graduate School of AgricultureKyoto UniversityKyotoJapan

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