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

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Abstract

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.

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References

  • 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 62:4267–4280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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) 139:1984–1994

    Article  CAS  Google Scholar 

  • de Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60:1523–1532

    Article  CAS  PubMed  Google Scholar 

  • 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 49:782–791

    Article  CAS  PubMed  Google Scholar 

  • 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 122:471–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 111:545–550

    Article  CAS  PubMed  Google Scholar 

  • George WL, Scott JW, Splittstoesser WE (1984) Parthenocarpy in tomato. Hortic Rev 6:65–84

    Google Scholar 

  • Gillaspy G, Bendavid H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 116:755–767

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagen G, Guilfoyle TJ (1985) Rapid induction of selective transcription by auxins. Mol Cell Biol 5:1197–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 637:213–221

    Article  CAS  Google Scholar 

  • 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 15:634–647

    Article  CAS  PubMed  Google Scholar 

  • Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 287:221–235

    Article  CAS  Google Scholar 

  • 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 56:674–687

    Article  CAS  PubMed  Google Scholar 

  • Mapelli (1978) Relationship between set, development and activities of growth regulators in tomato fruits. Plant Cell Physiol 19:1281–1288

    CAS  Google Scholar 

  • 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 30:405–415

    Article  CAS  Google Scholar 

  • 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 169:1165–1172

    Article  CAS  PubMed  Google Scholar 

  • 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 226:877–888

    Article  CAS  PubMed  Google Scholar 

  • 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 168:1684–1701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:4525–4538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Picken AJF (1984) A Review of pollination and fruit-set in the tomato (Lycopersicon esculentum Mill). J Hortic Sci 59:1–13

    Article  Google Scholar 

  • Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665

    Article  CAS  Google Scholar 

  • 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 1:243–251

    CAS  Google Scholar 

  • Sotelo-Silveira M, Marsch-Martinez N, de Folter S (2014) Unraveling the signal scenario of fruit set. Planta 239:1147–1158

    Article  CAS  PubMed  Google Scholar 

  • 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 17:616–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:251–256

    Article  Google Scholar 

  • 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 86:487–492

    Article  CAS  Google Scholar 

  • 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 17:2676–2692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westfall CS (2010) Modulating plant hormones by enzyme action The GH3 family of acyl acid amido synthetases. Plant Signal Behav 5:1607–1612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:23173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338

    Article  CAS  PubMed  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

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

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Authors and Affiliations

  1. Graduate School of Agriculture, Kyoto University, Kizugawa, 619-0218, Japan

    Rihito Takisawa, Hideto Kusaka, Tetsuya Nakazaki & Akira Kitajima

  2. Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Yuto Nishino, Masahiro Miyashita & Hisashi Miyagawa

Authors
  1. Rihito Takisawa
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  2. Hideto Kusaka
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  3. Yuto Nishino
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  4. Masahiro Miyashita
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  5. Hisashi Miyagawa
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  6. Tetsuya Nakazaki
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  7. Akira Kitajima
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Correspondence to Rihito Takisawa.

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Takisawa, R., Kusaka, H., Nishino, Y. et al. Involvement of Indole-3-Acetic Acid Metabolism in the Early Fruit Development of the Parthenocarpic Tomato Cultivar, MPK-1. J Plant Growth Regul 38, 189–198 (2019). https://doi.org/10.1007/s00344-018-9826-7

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  • DOI: https://doi.org/10.1007/s00344-018-9826-7

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