Skip to main content
Log in

Chiba Tendril-Less locus determines tendril organ identity in melon (Cucumis melo L.) and potentially encodes a tendril-specific TCP homolog

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Tendrils are filamentous plant organs that coil on contact with an object, thereby providing mechanical support for climbing to reach more sunlight. Plant tendrils are considered to be modified structure of leaves, stems, or inflorescence, but the origin of cucurbit tendrils is still argued because of the complexity in the axillary organ patterning. We carried out morphological and genetic analyses of the Chiba Tendril-Less (ctl) melon (Cucumis melo) mutant, and found strong evidence that the melon tendril is a modified organ derived from a stem–leaf complex of a lateral shoot. Heterozygous (CTL/ctl) plants showed traits intermediate between tendril and shoot, and ontogenies of wild-type tendrils and mutant modified shoots coincided. We identified the CTL locus in a 200-kb region in melon linkage group IX. A single base deletion in a melon TCP transcription factor gene (CmTCP1) was detected in the mutant ctl sequence, and the expression of CmTCP1 was specifically high in wild-type tendrils. Phylogenetic analysis demonstrated the novelty of the CmTCP1 protein and the unique molecular evolution of its orthologs in the Cucurbitaceae. Our results move us closer to answering the long-standing question of which organ was modified to become the cucurbit tendril, and suggest a novel function of the TCP transcription factor in plant development.

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

Abbreviations

LS:

Lateral shoot

TCP:

TEOSINTE BRANCHED1, CYCLOIDER and PROLIFERATING CELL FACTORS1/2

TF:

Transcription factor

References

  • Aggarwal P, Das Gupta M, Joseph AP, Chatterjee N, Srinivasan N, Nath U (2010) Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22:1174–1189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472

    Article  PubMed Central  PubMed  Google Scholar 

  • Ameha M, Skirvin RM, Mitiku G, Bullock D, Hofmann P (1998) In vitro tendril and flower development in cucumber (Cucumis sativus) may be regulated by gibberellins. J Hort Sci Biotechnol 73:159–163

    CAS  Google Scholar 

  • Bell AD (1991) Plant form: an illustrated guide to flowering plant morphology. Oxford University Press, Oxford

    Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

    Article  CAS  PubMed  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1865) On the movements and habits of climbing plants. J Linn Soc London, Bot 9:1–118

    Article  Google Scholar 

  • Dastur RH, Kapadia GA (1931) Mechanism of curvature in the tendrils of Cucurbitaceae. Ann Bot 45:279–301

    Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Silva I, Eduardo I, Blanca J, Esteras C, Picó B, Nuez F, Arús P, Garcia-Mas J, Monforte AJ (2008) Bin mapping of genomic and EST-derived SSRs in melon (Cucumis melo L.). Theor Appl Genet 118:139–150

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci USA 109:11872–11877

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gerbode SJ, Puzey JR, McCormick AG, Mahadevan L (2012) How the cucumber tendril coils and overwinds. Science 337:1087–1091

    Article  CAS  PubMed  Google Scholar 

  • Gerrath JM, Guthrie TB, Zitnak TA, Posluszny U (2008) Development of the axillary bud complex in Echinocystis lobata (Cucurbitaceae): interpreting the cucurbitaceous tendril. Am J Bot 95:773–781

    Article  PubMed  Google Scholar 

  • Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58

    Article  CAS  PubMed  Google Scholar 

  • Hagerup O (1930) Vergleichende morphologische und systematische Studienüber die Ranken und andere vegetative Organe der Cucurbitaceen und Passifloraceen. Danske Bot Arkiv 6:1–103

    Google Scholar 

  • Hirabayashi T, Oizumi T, Sato K, Kote T, Yoshida S, Matsuo T, Komatsuka T (2007) Breeding of tendril-less type melon cultivar ‘TL Takami’ and its characteristics. Hort Res 6:313–316 (in Japanese with English abstract)

    Article  Google Scholar 

  • Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C et al (2009) Tendril-less regulates tendril formation in Pea leaves. Plant Cell 21:420–428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Jaffe MJ, Galston AW (1968) The physiology of tendrils. Ann Rev Plant Physiol 19:417–434

    Article  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kong Q, Yuan J, Niu P, Xie J, Jiang W, Huang Y, Bie Z (2014) Screening suitable reference genes for normalization in reverse transcription quantitative real-time PCR analysis in melon. PLoS ONE 9:e87197

    Article  PubMed Central  PubMed  Google Scholar 

  • Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348

    Article  CAS  PubMed  Google Scholar 

  • Kumazawa M (1964) Morphological interpretations of axillary organs in the Cucurbitaceae. Phytomorphology 14:287–298

    Google Scholar 

  • Kwack SN (1995) Inheritance of determinate growth habit in Cucurbita moschata Poir. J Kor Soc Hort Sci 36:780–784

    Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lin D, Wang T, Wang Y, Zhang X, Rhodes BB (1992) The effect of the branchless gene bl on plant morphology in watermelon. Cucurbit Genet Coop Rpt 15:74–75

    Google Scholar 

  • Loy B (2012–2013) A recessive tendrilless mutant in ornamental pumpkin. Cucurbit Genet Coop Rpt 35–36:31–32

  • Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799

    Article  CAS  PubMed  Google Scholar 

  • Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39

    Article  PubMed  Google Scholar 

  • Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M, Sato M, Nasu S, Minobe Y (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9:11–17

    Article  CAS  PubMed  Google Scholar 

  • Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407

    Article  CAS  PubMed  Google Scholar 

  • Oizumi T, Hirabayashi T, Kote T, Matsuo T (2005) Growth and Inheritance Characteristics of new melon tendrilless type cultivar “Chiba TL”. Bull Chiba Agric Res Cent 4:69–75 (in Japanese with English summary)

    Google Scholar 

  • Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I et al (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39:787–791

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • Rhodes BB, Zhang XP, Baird VB, Knapp H (1999) A tendrilless mutant in watermelon: phenotype and inheritance. Cucurbit Genet Coop Rep 22:28–30

    Google Scholar 

  • Rowe JT, Bowers JL (1965) The inheritance and potential of an irradiation induced tendrilless character in cucumbers. Proc Am Soc Hort Sci 86:436–441

    Google Scholar 

  • Sensarma P (1955) Tendrils of the Cucurbitaceae: their morphological nature on anatomical evidences. Proc Natl Inst Sci Ind 21:162–169

    Google Scholar 

  • Srinivasan C, Mullins MG (1979) Flowering in Vitis: conversion of tendrils into inflorescences and bunches of grapes. Planta 145:187–192

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Troll W (1939) Vergleichende morphologie der höheren pflanzen. band I: vegetationsorgane. teil II. Gebrüder Borntraeger, Berlin

    Google Scholar 

Download references

Acknowledgments

We thank the agricultural technicians at the Southern Prefectural Horticulture Institute for cultivating the melon plants; Tetsuo Hirabayashi of the Institute for Horticultural Plant Breeding for kindly providing seeds of TL Takami; Tsutomu Hosouchi and Sayaka Shinpo of the Kazusa DNA Research Institute for genome sequencing; and Tomoko Fujiwara, Ruriko Koyano, Kohei Suzuki, Takashi Sudo, Yuuki Yonehana and Wataru Honmo of Chiba University for providing technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shinji Mizuno.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 744 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mizuno, S., Sonoda, M., Tamura, Y. et al. Chiba Tendril-Less locus determines tendril organ identity in melon (Cucumis melo L.) and potentially encodes a tendril-specific TCP homolog. J Plant Res 128, 941–951 (2015). https://doi.org/10.1007/s10265-015-0747-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-015-0747-2

Keywords

Navigation