SpringerLink
Log in

Analysis and fine map** of a gene controlling the folded-leaf phenotype of a mutant tomato line

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Tomato (Solanum lycopersicum L.) is one of the most popular cultivated vegetables worldwide. Tomato leaves are determinate organs with important functions affecting plant growth and development. In addition to the other leaf phenotypes, folded leaves have recently been observed in several tomato varieties. In the present study, an F2 population was generated from a cross between tomato inbred lines 14g-677 (i.e., folded leaves) and 14g-683 (i.e., wild-type leaves). A genetic analysis of the folded-leaf trait in 199 F2 individuals revealed this leaf phenotype is controlled by a single recessive gene, which was designated as fl. This gene was initially localized to chromosome 11 based on insertion/deletion (InDel) markers and a bulked segregant analysis (BSA). According to a genetic map consisting of new markers and recombinants, the fl gene was mapped between the SNP-1 and dcaps-10 markers at the distal end of the long arm of tomato chromosome 11. The physical distance between the two markers was approximately 62.2 kb. The annotation and functional characterization of the genes in this region indicated fl may be ARF4, which encodes an auxin response factor. A sequence analysis revealed that the ARF4 of line 14g-677 is missing a single C in the third exon region. Furthermore, a quantitative real-time polymerase chain reaction detected an approximate fourfold difference in ARF4 transcript abundance between lines 14g-677 and 14g-683. Thus, a mutation to ARF4 is likely responsible for the folded-leaf phenotype of tomato mutants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Audran-Delalande C, Bassa C, Mila I, Regad F, Zouine M, Bouzayen M (2012) Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol 53(4):659–672

    Article  PubMed  CAS  Google Scholar 

  • Chitwood DH, Kumar R, Headland LR, Ranjan A, Covington MF, Ichihashi Y, Fulop D, Jiménez-Gómez JM, Peng J, Maloof JN (2013) A quantitative genetic basis for leaf morphology in a set of precisely defined tomato introgression lines. Plant Cell 25(7):2465–2481

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Jong M, Mariani C, Vriezen WH (2009a) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60(5):1523–1532

    Article  PubMed  CAS  Google Scholar 

  • De Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009b) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57(1):160–170

    Article  PubMed  CAS  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132(20):4563–4574

    Article  PubMed  CAS  Google Scholar 

  • Frary A, Fritz LA, Tanksley SD (2004) A comparative study of the genetic bases of natural variation in tomato leaf, sepal, and petal morphology. Theor Appl Genetics 109(3):523–533

    Article  Google Scholar 

  • Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Report 13:207

    Article  CAS  Google Scholar 

  • Godin C (2000) Representing and encoding plant architecture: a review. Ann For Sci 57(5):413–438

    Article  Google Scholar 

  • Goetz M, Hooper LC, Johnson SD, Rodrigues JCM, Vivian-Smith A, Koltunow AM (2007) Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol 145(2):351–366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10(5):453–460

    Article  PubMed  CAS  Google Scholar 

  • Guillon F, Philippe S, Bouchet B, Devaux M-F, Frasse P, Jones B, Bouzayen M, Lahaye M (2008) Down-regulation of an auxin response factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 59(2):273–288

    Article  PubMed  CAS  Google Scholar 

  • Holtan HE, Hake S (2003) Quantitative trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii segmental introgression lines. Genetics 165(3):1541–1550

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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(4):603–613

    Article  PubMed  CAS  Google Scholar 

  • Kessler S, Kim M, Pham T, Weber N, Sinha N (2001) Mutations altering leaf morphology in tomato. Int J Plant Sci 162(3):475–492

    Article  CAS  Google Scholar 

  • Li S, Ma Y (1998) Genetic analysis and map** the flag leaf roll in rice (Oryza sativa). Sichuan Nongye Daxue Xuebao (in Chinese)

  • Li J, Sima W, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y (2012) Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. J Exp Bot 63(18):6407–6420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61(5):1419–1430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  • Martí E, Gisbert C, Bishop GJ, Dixon MS, García-Martínez JL (2006) Genetic and physiological characterization of tomato cv. Micro-Tom. J Exp Bot 57(9):2037–2047

    Article  PubMed  CAS  Google Scholar 

  • Sagar M, Chervin C, Mila I, Hao Y, Roustan J-P, Benichou M, Gibon Y, Biais B, Maury P, Latché A (2013) SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol 161(3):1362–1374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shao Y, Pan C, Chen Z, Zuo S, Zhang Y, Pan X (2005) Fine map** of an incomplete recessive gene for leaf rolling in rice (Oryza sativa L.). Chin Sci Bull 50(21):2466–2472

    Article  CAS  Google Scholar 

  • Shi Y, Chen J, Liu W, Huang Q, Shen B, Leung H, Wu J (2009) Genetic analysis and gene map** of a new rolled-leaf mutant in rice (Oryza sativa L.). Sci Chin Ser C 52(9):885–890

    Article  CAS  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19(3):309–319

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen J (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen 33

  • Wang H, Qi M, Cutler AJ (1993) A simple method of preparing plant samples for PCR. Nucleic Acids Res 21(17):4153

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché A, Pech J-C, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and-independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21(5):1428–1452

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43(1):118–130

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, Yu X, Lu G (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep 30(11):2059

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Wang Y, Shen H, Yang W (2014) In silico identification and experimental validation of insertion-deletion polymorphisms in tomato genome. DNA Res 21(4):429–438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y (2012) Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24(9):3575–3589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu D, Lin X, Cao W (2001) Comparison of leaf photosynthetic characteristics among rice hybrids with different leaf rolling index. Zuo Wu Xue Bao 27(3):329–333 (in Chinese)

    Google Scholar 

  • Zouine M, Fu Y, Chateigner-Boutin A-L, Mila I, Frasse P, Wang H, Audran C, Roustan J-P, Bouzayen M (2014) Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing. PLoS ONE 9(1):e84203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31471874), the National Key Research and Development Program of China (2016YFD0101703), and the Key Laboratory of Horticultural Crops Genetic Improvement, Ministry of Agriculture of the People’s Republic of China.

Author information

Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, No. 12 Zhongguancun Nandajie, Haidian District, Bei**g, 100081, China

    **aomei Su, Zejun Huang, **aoxuan Wang, Yanmei Guo, Yongchen Du & Jianchang Gao

  2. Department of Vegetable Science, College of Horticulture, China Agricultural University, No. 2 Yuanmingyuan **lu, Bei**g, 100193, China

    **aomei Su & Wencai Yang

Authors
  1. **aomei Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wencai Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zejun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. **aoxuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanmei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yongchen Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianchang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yongchen Du or Jianchang Gao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10681_2018_2148_MOESM1_ESM.tif

Fig. S1 Agarose gel electrophoresis separation of PCR fragments amplified from 14 tomato lines using the dCAPS marker. a = homozygous like the 14g-677 mutant parent, b = homozygous like the 14g-683 wild parent, F = folded leaf, N = normal leaf. Supplementary material 1 (TIFF 4545 kb)

10681_2018_2148_MOESM2_ESM.docx

Table S1 Details regarding the molecular markers used for map** the fl locus in tomato. Note: a construct a genetic map, b construct a genetic map of the target region, c analyze recombinants. Supplementary material 2 (DOCX 19 kb)

Rights and permissions

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-018-2148-9

Keywords

Search

Navigation