Skip to main content
SpringerLink
Log in

The tomato early fruit specific gene Lefsm1 defines a novel class of plant-specific SANT/MYB domain proteins

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

We describe here a novel plant-specific gene, Lefsm1 (fruit SANT/MYB-like 1) harboring a single SANT/MYB domain. The expression of Lefsm1 is specific to the very early stages of tomato (Lycopersicon esculentum) fruit development. Ectopic expression of Lefsm1 results in severe developmental alterations manifested in retarded growth, and reduced apical dominance during tomato and Arabidopsis seedling development. A promoter sequence residing 1.0 kb upstream to the translation initiation codon confers the organ-specific expression of the gene. Lefsm1 belongs to a novel small gene family consisting of five to six members in tomato, Arabidopsis and rice. The SANT/MYB domain of LeFSM1 and its orthologs in Arabidopsis and rice differs from that of all other plant or animal MYB proteins and from the SANT domains found in part of the chromatin remodeling proteins. Together, our results indicate that Lefsm1 is a founding member of a small family of proteins containing a novel MYB/SANT domain which is likely to participate in the regulation of a plant-specific developmental program.

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. 2a–c
Fig. 3a, b
Fig. 4a–d
Fig. 5a–e
Fig. 6a–c
Fig. 7a–c

Similar content being viewed by others

References

  • Aasland R, Stewart AF, Gibson T (1996) The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional c-repressor N-CoR and TFIIIB. Trends Biochem Sci 21:87–88

    Article  CAS  PubMed  Google Scholar 

  • Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Maś P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883

    Article  CAS  PubMed  Google Scholar 

  • Baranowskij N, Frohberg C, Prat S, Willmitzer L (1994) A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J 13:5383–5392

    CAS  PubMed  Google Scholar 

  • Barg R, Meir E, Lapushner D, Frankel R, Salts Y (1990) Differential regulation of fruit specific 62 kDa protein in developing parthenocarpic (pat-2/pat-2) and seeded tomato fruits. Physiol Plant 80:417–424

    Article  CAS  Google Scholar 

  • Barg R, Shabtai S, Salts Y (2001) Transgenic tomato (Lycopesicon esculentum). In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, transgenic crops II. Springer, Berlin Heidelberg New York, pp 212–233

    Google Scholar 

  • Becker D, Kemper E, Schell J, Masterson R (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol Biol 20:1195–1197

    CAS  PubMed  Google Scholar 

  • Bilaud T, Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser SM, Gilson E (1996) The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res 24:1294–1303

    Article  CAS  PubMed  Google Scholar 

  • Bohner J, Bangerth F (1988) Cell number, cell size and hormone level in semi-isogenic mutants of L. pimpinellifolium differing in fruit size. Physiol Plant 72:316–320

    CAS  Google Scholar 

  • Boyer LA, Langer MR, Crowley KA, Tan S, Denu JM, Peterson CL (2002) Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol Cell 10:935–942

    Article  CAS  PubMed  Google Scholar 

  • Braun EL, Grotewold E (1999) Newly discovered plant c-myb-like genes rewrite the evolution of the plant myb gene family. Plant Physiol 121:21–24

    Article  CAS  PubMed  Google Scholar 

  • Busi MV, Bustamante C, D’Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52 801–815

    Article  CAS  PubMed  Google Scholar 

  • Carmi N, Salts Y, Dedicova B, Shabtai S, Barg R (2003) Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta 217:726–735

    Article  CAS  PubMed  Google Scholar 

  • Chmelnitsky I, Sobolev I, Barg R, Shabtai S, Salts Y (2003) Isolation and preliminary characterization of tomato petal- and stamen-specific cDNAs from a subtracted and equilibrated cDNA library. Euphytica 129:229–236

    Article  CAS  Google Scholar 

  • Feldbrugge M, Sprenger M, Hahlbrock K, Weisshaar B (1997) PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J 11:1079–1093

    Google Scholar 

  • Foos G, Grimm S, Klempnauer KH (1992) Functional antagonism between members of the myb family: B-myb inhibits v-myb-induced gene activation. EMBO J 11:4619–4629

    CAS  PubMed  Google Scholar 

  • Fransz PF, de Jong JH (2002) Chromatin dynamics in plants. Curr Opin Plant Biol 5:560–567

    Article  CAS  PubMed  Google Scholar 

  • Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Goodstadt L, Ponting CP (2001) CHROMA: consensus-based colouring of multiple alignments for publication. Bioinformatics 17:845–846

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Jiang C, Gu J, Chopra S, Gu X, Peterson T (2004) Ordered origin of the typical two- and three-repeat Myb genes. Gene 326:13–22

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41:577–585

    Article  CAS  PubMed  Google Scholar 

  • Joubes J, Chevalier C (2000) Endoreduplication in higher plants. Plant Mol Biol 43:735–745

    Article  CAS  PubMed  Google Scholar 

  • Joubes J, Phan TH, Just D, Rothan C, Bergounioux C, Raymond P, Chevalier C (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol 121:857–869

    Article  CAS  PubMed  Google Scholar 

  • Joubes J, Walsh D, Raymond P, Chevalier C (2000) Molecular characterization of the expression of distinct classes of cyclins during the early development of tomato fruit. Planta 211:430–439

    Article  CAS  PubMed  Google Scholar 

  • Joubes J, Lemaire-Chamley M, Delmas F, Walter J, Hernould M, Mouras A, Raymond P, Chevalier C (2001) A new C-type cyclin-dependent kinase from tomato expressed in dividing tissues does not interact with mitotic and G1 cyclins. Plant Physiol 126:1403–1415

    Article  CAS  PubMed  Google Scholar 

  • Kosugi S, Ohashi Y, Nakajima K, Arai Y (1990) An improved assay for β-glucuronidase in transformed cells: methanol almost completely suppresses a putative endogenous β-glucuronidase activity. Plant Sci 70:133–140

    Article  CAS  Google Scholar 

  • Kvarnheden A, Yao JL, Zhan X, O’Brien I, Morris BA (2000) Isolation of three distinct CycD3 genes expressed during fruit development in tomato. J Exp Bot 51:1789–1797

    Article  CAS  PubMed  Google Scholar 

  • Lee MM, Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14:611–618

    Article  CAS  PubMed  Google Scholar 

  • Lipsick JS (1996) One billion years of Myb. Oncogene 13:223–235

    CAS  PubMed  Google Scholar 

  • Liu J, Cong B, Tanksley SD (2003) Generation and analysis of an artificial gene dosage series in tomato to study the mechanisms by which the cloned quantitative trait locus fw2.2 controls fruit size. Plant Physiol 132:292–299

    Article  CAS  PubMed  Google Scholar 

  • Lu CA, Ho TH, Ho SL, Yu SM (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression. Plant Cell 14:1963–1980

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trends Genet 13:67–73

    Article  CAS  PubMed  Google Scholar 

  • Meyerowitz EM (2002) Plants compared to animals: the broadest comparative study of development. Science 295:1482–1485

    Article  CAS  PubMed  Google Scholar 

  • Nesbitt TC, Tanksley SD (2001) fw2.2 directly affects the size of developing tomato fruit, with secondary effects on fruit number and photosynthate distribution. Plant Physiol 127:575–583

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    CAS  PubMed  Google Scholar 

  • Quinn PG (2002) Mechanisms of basal and kinase-inducible transcription activation by CREB. Prog Nucleic Acid Res Mol Biol 72:269–305

    CAS  PubMed  Google Scholar 

  • Rabinowicz PD, Braun EL, Wolfe AD, Bowen B, Grotewold E (1999) Maize R2R3 Myb genes: sequence analysis reveals amplification in the higher plants. Genetics 153:427–444

    CAS  PubMed  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G-L (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  Google Scholar 

  • Rose A, Meier I, Wienand U (1999) The tomato I-box binding factor LeMYBI is a member of a novel class of myb-like proteins. Plant J 20:641–652

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Servillo G, Della Fazia MA, Sassone-Corsi P (2002) Coupling cAMP signaling to transcription in the liver: pivotal role of CREB and CREM. Exp Cell Res 275:143–154

    Article  CAS  PubMed  Google Scholar 

  • Solovyev VV (2002) Finding genes by computer: probabilistic and discriminative approaches. In: Jiang T, Smith T, Xu Y, Zhang M (eds) Current topics in computational biology. MIT Press, Cambridge, pp 365–401

    Google Scholar 

  • Stockinger EJ, Mao Y, Regier MK, Triezenberg SJ, Thomashow MF (2001) Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res 29:1524–1533

    Article  CAS  PubMed  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16 Suppl:S181–9

    Article  CAS  PubMed  Google Scholar 

  • Vancanneyt G, Schmidt R, O’Connor-Sanchez A, Willmitzer L, Rocha-Sosa M (1990) Construction of an intron-containing marker gene: splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation. Mol Gen Genet 220:245–250

    CAS  PubMed  Google Scholar 

  • Varga A, Bruinsma J (1986) Tomato. In: Monselise SP (ed) CRC handbook of fruit set and development. CRC Press, Boca Raton, pp 461–481

    Google Scholar 

  • Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116

    Article  CAS  PubMed  Google Scholar 

  • Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–5419

    Article  CAS  PubMed  Google Scholar 

  • Wagner D (2003) Chromatin regulation of plant development. Curr Opin Plant Biol 6:20–28

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9:491–507

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2(5):E104

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The plasmid pGPVT-KAN was a generous gift of Dr. D. Becker (Germany). This project was supported in part by the Israeli Ministry of Science (MOST) grant number 9446, and in part by the Israeli Ministry of Agriculture Chief Scientist Fund grant number 261–0414. This publication is contribution no. 105/2004 of the Volcani Center, ARO.

Author information

Authors and Affiliations

  1. Department of Plant Genetics, Institute of Field and Garden Crops, The Volcani Center, ARO, P.O.Box 6, Bet Dagan, 50250, Israel

    Rivka Barg, Irina Sobolev, Tali Eilon, Inna Chmelnitsky, Sara Shabtai & Yehiam Salts

  2. Faculty of Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel

    Amit Gur

  3. Department of Plant Cellular and Molecular Biology and Plant Biotechnology Center, The Ohio State University, 206 Rightmire Hall, 1060 Carmack Road, Columbus, OH, 43210, USA

    Erich Grotewold

Authors
  1. Rivka Barg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irina Sobolev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tali Eilon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amit Gur
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Inna Chmelnitsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sara Shabtai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Erich Grotewold
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yehiam Salts
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rivka Barg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barg, R., Sobolev, I., Eilon, T. et al. The tomato early fruit specific gene Lefsm1 defines a novel class of plant-specific SANT/MYB domain proteins. Planta 221, 197–211 (2005). https://doi.org/10.1007/s00425-004-1433-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-004-1433-0

Keywords

Search

Navigation