Euphytica

, 214:97 | Cite as

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

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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.

Keywords

Tomato Folded leaf Fine mapping ARF4 Mutant 

Notes

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.

Supplementary material

10681_2018_2148_MOESM1_ESM.tif (4.4 mb)
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 (19 kb)
Table S1 Details regarding the molecular markers used for mapping 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)

References

  1. 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):659–672CrossRefPubMedGoogle Scholar
  2. 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):2465–2481CrossRefPubMedPubMedCentralGoogle Scholar
  3. De Jong M, Mariani C, Vriezen WH (2009a) The role of auxin and gibberellin in tomato fruit set. J Exp Bot 60(5):1523–1532CrossRefPubMedGoogle Scholar
  4. 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):160–170CrossRefPubMedGoogle Scholar
  5. 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):4563–4574CrossRefPubMedGoogle Scholar
  6. 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):523–533CrossRefGoogle Scholar
  7. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Report 13:207CrossRefGoogle Scholar
  8. Godin C (2000) Representing and encoding plant architecture: a review. Ann For Sci 57(5):413–438CrossRefGoogle Scholar
  9. 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):351–366CrossRefPubMedPubMedCentralGoogle Scholar
  10. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10(5):453–460CrossRefPubMedGoogle Scholar
  11. 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):273–288CrossRefPubMedGoogle Scholar
  12. Holtan HE, Hake S (2003) Quantitative trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii segmental introgression lines. Genetics 165(3):1541–1550PubMedPubMedCentralGoogle Scholar
  13. 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):603–613CrossRefPubMedGoogle Scholar
  14. Kessler S, Kim M, Pham T, Weber N, Sinha N (2001) Mutations altering leaf morphology in tomato. Int J Plant Sci 162(3):475–492CrossRefGoogle Scholar
  15. Li S, Ma Y (1998) Genetic analysis and mapping the flag leaf roll in rice (Oryza sativa). Sichuan Nongye Daxue Xuebao (in Chinese)Google Scholar
  16. 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):6407–6420CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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):1419–1430CrossRefPubMedPubMedCentralGoogle Scholar
  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408CrossRefPubMedGoogle Scholar
  19. 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):2037–2047CrossRefPubMedGoogle Scholar
  20. 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):1362–1374CrossRefPubMedPubMedCentralGoogle Scholar
  21. Shao Y, Pan C, Chen Z, Zuo S, Zhang Y, Pan X (2005) Fine mapping of an incomplete recessive gene for leaf rolling in rice (Oryza sativa L.). Chin Sci Bull 50(21):2466–2472CrossRefGoogle Scholar
  22. Shi Y, Chen J, Liu W, Huang Q, Shen B, Leung H, Wu J (2009) Genetic analysis and gene mapping of a new rolled-leaf mutant in rice (Oryza sativa L.). Sci Chin Ser C 52(9):885–890CrossRefGoogle Scholar
  23. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19(3):309–319CrossRefPubMedGoogle Scholar
  24. Van Ooijen J (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen 33Google Scholar
  25. Wang H, Qi M, Cutler AJ (1993) A simple method of preparing plant samples for PCR. Nucleic Acids Res 21(17):4153CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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):1428–1452CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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):118–130CrossRefPubMedGoogle Scholar
  28. 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):2059CrossRefPubMedGoogle Scholar
  29. 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):429–438CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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):3575–3589CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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
  32. 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):e84203CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Institute of Vegetables and FlowersChinese Academy of Agricultural SciencesBeijingChina
  2. 2.Department of Vegetable Science, College of HorticultureChina Agricultural UniversityBeijingChina

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