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The grocery-store tomato that looks beautiful but tastes like tart cardboard arises from selection processes favoring phenotypes that make commercial production more reliable. Significant in that selection process was a mutation that reduced the mottled color variations of unripe green tomatoes, leaving them a uniform, pale, green. Powell et al. (p. 1711) analyzed the molecular biology of the mutation. The uniform ripening mutation turns out to disable a transcription factor called Golden 2-like (GLK2). GLK2 expression increases the fruit's photosynthetic capacity, resulting in higher sugar content.

Abstract

Modern tomato (Solanum lycopersicum) varieties are bred for uniform ripening (u) light green fruit phenotypes to facilitate harvests of evenly ripened fruit. U encodes a Golden 2-like (GLK) transcription factor, SlGLK2, which determines chlorophyll accumulation and distribution in developing fruit. In tomato, two GLKs—SlGLK1 and SlGLK2—are expressed in leaves, but only SlGLK2 is expressed in fruit. Expressing GLKs increased the chlorophyll content of fruit, whereas SlGLK2 suppression recapitulated the u mutant phenotype. GLK overexpression enhanced fruit photosynthesis gene expression and chloroplast development, leading to elevated carbohydrates and carotenoids in ripe fruit. SlGLK2 influences photosynthesis in developing fruit, contributing to mature fruit characteristics and suggesting that selection of u inadvertently compromised ripe fruit quality in exchange for desirable production traits.

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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S8
Tables S1 to S8
References (3258)

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Published In

Science
Volume 336 | Issue 6089
29 June 2012

Submission history

Received: 21 March 2012
Accepted: 5 June 2012
Published in print: 29 June 2012

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Acknowledgments

Minimum Information About a Microarray Experiment (MIAME)–compliant microarray data are available at http://ted.bti.cornell.edu. and at http://www.ebi.ac.uk/arrayexpress/ (accession E-MEXP-3652). F. Carrari and A. Fernie provided S. pennellii SlGLK2, and J. Maloof provided S. habrochaites SlGLK2 sequences. The U.S. Department of Agriculture (USDA)/National Institute of Food and Agriculture Solanaceae Coordinated Agricultural Project provided potato data. We are grateful to the Tomato Genome Consortium and the SOL Genomics Network for prepublication access to the tomato genome sequence. The S. pennellii introgression lines were provided by the C. M. Rick Tomato Genetics Resource Center; the S. pimpinellifolium populations were provided by the Instituto de Hortofruticultura Subtropical y Mediterranea “La Mayora,” Consejo Superior de Investigaciones Cientificas; and both populations are available by request from the sources. The AtGLK-expressing lines were provided by Mendel Biotechnology and Seminis/Monsanto Vegetable Seeds. SlGLK2, the corresponding lines, and the F2 10-1 IL x M82 population lines and seeds are available from J.J.G. without restriction. Seminis/Monsanto will make available, upon request, and under a material transfer agreement indicating they are to be used for noncommercial purposes, the following lines: LexA:AtGLK1:p35S:LexA-Gal4; LexA:AtGLK1:pLTP:LexA-Gal4; LexA:AtGLK1:pRbcS:LexA-Gal4; LexA:AtGLK1:pPDS:LexA-Gal4; LexA:AtGLK2:p35S:LexA-Gal4; LexA:AtGLK2:pLTP:LexA-Gal4; LexA:AtGLK2:pRbcS:LexA-Gal4; LexA:AtGLK2:pPDS:LexA-Gal4; plus the T63 control line. Other biological materials are available by request from A.L.T.P. or J.J.G. A.L.T.P., T.H., K.L.-C., R.F.-B., and A.B.B. have filed a provisional U.S. patent application UC #2011-841, “Introduction of wild species GLK genes for improved ripe tomato fruit quality,” through the University of California. A.L.T.P. and A.B.B. have filed the U.S. patent application #2010/0154078, “Transcription factors that enhance traits in plant organs,” through Mendel Biotechnology. Assistance from B. Blanco-Ulate, S. Phothiset, S. Reyes, A. Abraham, L. Gilani, and G. Arellano is gratefully acknowledged. J. Langdale provided helpful advice regarding GLK phylogeny and nomenclature. G. Adamson and P. Kysar, Electron Microscopy (EM) Laboratory, University of California Davis Medical Center did the EM work. University of California Discovery and partners funded the pepper analysis and the initial investigations of the Arabidopsis GLKs. The Vietnam Education Foundation supported C.N. Fundación Genoma España ESPSOL Project provided partial funding to A.G. USDA–Agricultural Research Service, USDA–National Research Initiative (2007-02773), and NSF (Plant Genome Program IOS-0923312) provided support to J.J.G.

Authors

Affiliations

Ann L. T. Powell*, [email protected]
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Cuong V. Nguyen
Departments of Plant Breeding and Genetics and Plant Biology, Cornell University, Ithaca, NY 14853, USA.
Theresa Hill
Plant Sciences Department, University of California, Davis, CA 95616, USA.
KaLai Lam Cheng
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Rosa Figueroa-Balderas
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Hakan Aktas
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Hamid Ashrafi
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Clara Pons
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, Valencia E-46022, Spain.
Rafael Fernández-Muñoz
Instituto de Hortofruticultura Subtropical y Mediterranea La Mayora, Consejo Superior de Investigaciones Científicas–Universidad de Málaga, Málaga E-29750, Spain.
Ariel Vicente
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Centro de Investigación y Desarrollo en Criotecnología de Alimentos (Consejo Nacional de Investigaciones Científicas y Técnicas)–Universidad Nacional de La Plata (UNLP) and Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, CP 1900, Argentina.
Javier Lopez-Baltazar
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Present address: Instituto Tecnologico del Valle de Oaxaca, Oaxaca 68120, Mexico.
Cornelius S. Barry
Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA.
Yongsheng Liu
Boyce Thompson Institute for Plant Research and USDA-ARS Robert W. Holley Center, Cornell University, Ithaca, NY 14853, USA.
Present address: School of Biotechnology and Food Engineering, Hefei University of Technology, Hefei 230009, P. R. China.
Roger Chetelat
Plant Sciences Department, University of California, Davis, CA 95616, USA.
Antonio Granell
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, Valencia E-46022, Spain.
Allen Van Deynze
Plant Sciences Department, University of California, Davis, CA 95616, USA.
James J. Giovannoni* [email protected]
Departments of Plant Breeding and Genetics and Plant Biology, Cornell University, Ithaca, NY 14853, USA.
Boyce Thompson Institute for Plant Research and USDA-ARS Robert W. Holley Center, Cornell University, Ithaca, NY 14853, USA.
Alan B. Bennett
Plant Sciences Department, University of California, Davis, CA 95616, USA.

Notes

*
To whom correspondence should be sent. E-mail: [email protected] (A.L.T.P.); [email protected] (J.J.G.)
These authors contributed equally to this work.
Present address: Department of Horticulture, Faculty of Agriculture, University of Suleyman Demirel, Isparta 32260, Turkey.

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