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Planta

, Volume 232, Issue 3, pp 755–764 | Cite as

Expression analysis of the auxin efflux carrier family in tomato fruit development

  • Sogo Nishio
  • Ryo Moriguchi
  • Hiroki Ikeda
  • Hideki Takahashi
  • Hideyuki Takahashi
  • Nobuharu Fujii
  • Thomas J. Guilfoyle
  • Koki Kanahama
  • Yoshinori KanayamaEmail author
Original Article

Abstract

Auxin transport network, which is important in the integration of plant developmental signals, depends on differential expression of the auxin efflux carrier PIN gene family. We cloned three tomato PIN (referred as SlPIN) cDNAs and examined their expression patterns in fruit and other organs. The expression of SlPIN1 and SlPIN2 was highest in very young fruit immediately after anthesis, whereas the expression of SlPIN3 was low at this same stage of fruit development. SlPIN2::GUS was expressed in ovules at anthesis and in young developing seeds at 4 days after anthesis, while SlPIN1::GUS was expressed in whole fruit. The DR5::GUS auxin-responsive reporter gene was expressed in the fruit and peduncle at anthesis and was higher in the peduncle 4 days after anthesis. These studies suggest that auxin is likely transported from young seeds by SlPIN1 and SlPIN2 and accumulated in peduncles where SlPIN gene expression is low in tomato. The possible role of SlPINs in fruit set was discussed.

Keywords

Auxin DR5 Fruit PIN Tomato 

Abbreviation

GUS

β-Glucuronidase

References

  1. Amemiya T, Kanayama Y, Yamaki S, Yamada K, Shiratake K (2005) Fruit-specific V-ATPase suppression in antisense-transgenic tomato reduces fruit growth and seed formation. Planta 223:1272–1280CrossRefPubMedGoogle Scholar
  2. An G (1986) Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoter in transformed tobacco cells. Plant Physiol 81:86–91CrossRefPubMedGoogle Scholar
  3. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefPubMedGoogle Scholar
  4. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44CrossRefPubMedGoogle Scholar
  5. Carraro N, Forestan C, Canova S, Traas J, Varotto S (2006) ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol 142:254–264CrossRefPubMedGoogle Scholar
  6. Casimiro I, Marchant A, Bhalerao R, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero P, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852CrossRefPubMedGoogle Scholar
  7. Deguchi M, Bennett AB, Yamaki S, Yamada K, Kanahama K, Kanayama Y (2006) An engineered sorbitol cycle alters sugar composition, not growth, in transformed tobacco. Plant Cell Environ 29:1980–1988CrossRefPubMedGoogle Scholar
  8. Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559CrossRefPubMedGoogle Scholar
  9. Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673CrossRefPubMedGoogle Scholar
  10. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical basal axis of Arabidopsis. Nature 426:147–153CrossRefPubMedGoogle Scholar
  11. Fujii N, Hotta T, Kim DH, Kamada M, Miyazawa Y, Kim KM, Takahashi H (2005) Isolation of cucumber auxin efflux carrier cDNAs and expression of corresponding mRNA in cucumber seedlings. Space Util Res 21:294–297Google Scholar
  12. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230CrossRefPubMedGoogle Scholar
  13. Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451CrossRefPubMedGoogle Scholar
  14. Hamamoto H, Shishido Y, Furuya S, Yasuda K (1998) Growth and development of tomato fruit as affected by 2,3,5-triiodobenzonic acid (TIBA) applied to the peduncle. J Japan Soc Hort Sci 67:210–212Google Scholar
  15. Hong SB, Sexton R, Tucker ML (2000) Analysis of gene promoters for two tomato polygalacturonases expressed in abscission zones and the stigma. Plant Physiol 123:869–881CrossRefPubMedGoogle Scholar
  16. Jefferson R, Kavanagh T, Bevan M (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene marker in higher plants. EMBO J 6:3901–3907PubMedGoogle Scholar
  17. 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 32:603–613CrossRefPubMedGoogle Scholar
  18. Kanayama K, Dai N, Granot D, Petreikov M, Schaffer A, Bennett AB (1997) Divergent fructokinase genes are differentially expressed in tomato. Plant Physiol 113:1379–1384CrossRefPubMedGoogle Scholar
  19. Lemaire-Chamley M, Petit J, Garcia V, Just D, Baldet P, Germain V, Fagard M, Mouassite M, Cheniclet C, Rothan C (2005) Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato. Plant Physiol 139:750–769CrossRefPubMedGoogle Scholar
  20. Odanaka S, Bennett AB, Kanayama Y (2002) Distinct physiological roles of fructokinase isozymes revealed by gene-specific suppression of Frk1 and Frk2 expression in tomato. Plant Physiol 129:1119–1126CrossRefPubMedGoogle Scholar
  21. Olimpieri I, Siligato F, Caccia R, Soressi GP, Mazzucato A, Mariotti L, Ceccarelli N (2007) Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis. Planta 226:877–888CrossRefPubMedGoogle Scholar
  22. Oliveros-Valenzuela M, Reyes D, Sánchez-Bravo J, Acosta M, Nicolás C (2007) The expression of genes coding for auxin carriers in different tissues and along the organ can explain variations in auxin transport and the growth pattern in etiolated lupin hypocotyls. Planta 227:133–142CrossRefPubMedGoogle Scholar
  23. Parry G, Marchant A, May S, Swarup R, Swarup K, James N, Graham N, Allen T, Martucci T, Yemm A, Napier R, Manning K, King G, Bennett M (2001) Quick on the uptake: characterization of a family of plant auxin influx carriers. J Plant Growth Regul 20:217–225CrossRefGoogle Scholar
  24. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260CrossRefPubMedGoogle Scholar
  25. Serrani JC, Fos F, Atares A, García-Martínez JL (2007a) Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv Micro-Tom of tomato. J Plant Growth Regul 26:211–221CrossRefGoogle Scholar
  26. Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, García-Martínez JL (2007b) Gibberellin regulation of fruit-set and growth in tomato. Plant Physiol 145:246–257CrossRefPubMedGoogle Scholar
  27. 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 47:426–431CrossRefPubMedGoogle Scholar
  28. Tucker ML, Whitelaw CA, Lyssenko NN, Nath P (2002) Functional analysis of regulatory elements in the gene promoter for an abscission-specific cellulase from bean and isolation, expression, and binding affinity of three TGA-type basic leucine zipper transcription factors. Plant Physiol 130:1487–1496CrossRefPubMedGoogle Scholar
  29. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971CrossRefPubMedGoogle Scholar
  30. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016CrossRefPubMedGoogle Scholar
  31. Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127:5157–5165PubMedGoogle Scholar
  32. Vieten A, Vanneste S, Wisniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531CrossRefPubMedGoogle Scholar
  33. Vogel G (2006) Auxin begins to give up its secrets. Science 313:1230–1231CrossRefPubMedGoogle Scholar
  34. Vriezen WH, Feron R, Maretto F, Keijman J, Mariani C (2008) Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol 177:60–76PubMedGoogle Scholar
  35. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché A, Pech JC, Bouzayena M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692CrossRefPubMedGoogle Scholar
  36. Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Sogo Nishio
    • 1
    • 4
  • Ryo Moriguchi
    • 1
  • Hiroki Ikeda
    • 1
  • Hideki Takahashi
    • 1
  • Hideyuki Takahashi
    • 2
  • Nobuharu Fujii
    • 2
  • Thomas J. Guilfoyle
    • 3
  • Koki Kanahama
    • 1
  • Yoshinori Kanayama
    • 1
    Email author
  1. 1.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  2. 2.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  3. 3.Department of BiochemistryUniversity of Missouri, ColumbiaColumbiaUSA
  4. 4.National Institute of Fruit Tree ScienceTsukubaJapan

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