Plant Biol (Stuttg) 2005; 7(2): 118-130
DOI: 10.1055/s-2005-837495
Review Article

Georg Thieme Verlag Stuttgart KG · New York

The Inheritance of Chilling Tolerance in Tomato (Lycopersicon spp.)

J. H. Venema1 , P. Linger2 , A. W. van Heusden3 , P. R. van Hasselt1 , W. Brüggemann4
  • 1Laboratory of Plant Physiology, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands
  • 2Physiologische Chemie der Pflanzen, FB C, Bergische Universität Wuppertal, Gauß-Straße 20, 42097 Wuppertal, Germany
  • 3Plant Research International, P.O. Box 16, 6700 AA Wageningen, The Netherlands
  • 4Botanisches Institut, Box 213, J. W. Goethe-Universität Frankfurt am Main, Postfach 111932, 60054 Frankfurt am Main, Germany
Weitere Informationen

Publikationsverlauf

Received: March 29, 2004

Accepted: October 8, 2004

Publikationsdatum:
21. März 2005 (online)

Abstract

During the past 25 years, chilling tolerance of the cultivated (chilling-sensitive) tomato Lycopersicon esculentum and its wild, chilling-tolerant relatives L. peruvianum and L. hirsutum (and, less intensively studied, L. chilense) has been the object of several investigations. The final aim of these studies can be seen in the increase in chilling tolerance of the cultivated genotypes. In this review, we will focus on low-temperature effects on photosynthesis and the inheritance of these traits to the offspring of various breeding attempts. While crossing L. peruvianum (♂) to L. esculentum (♀) so far has brought the most detailed insight with respect to physiological questions, for practical purposes, e.g., the readily cross ability, crossing programmes with L. hirsutum as pollen donor at present seem to be a promising way to achieve higher chilling-tolerant genotypes of the cultivated tomato. This perspective is due to the progress that has been made with respect to the genetic basis of chilling tolerance of Lycopersicon spp. over the past five years.

References

  • 1 Ali I. A., Kafkafi U., Yamaguchi I., Sugimoto Y., Inanaga S.. Effects of low root temperature on sap flow rate, soluble carbohydrates, nitrate contents and on cytokinin and gibberellin levels in root xylem exudate of sand-grown tomato.  Journal of Plant Nutrition. (1996);  16 619-634
  • 2 Allen D. J., Ort D. R.. Impacts of chilling temperatures on photosynthesis in warmclimate plants.  Trends in Plant Science. (2001);  6 36-42
  • 3 Aroca R., Tognoni F., Irigoyen J. J., Sánchez-Díaz M., Pardossi A.. Different root low temperature response of two maize genotypes differing in their chilling sensitivity.  Plant Physiology and Biochemistry. (2001);  39 1067-1073
  • 4 Babiychuk E., Schantz R., Cherep N., Weil J.-H., Gleba Y., Kushnir S.. Alterations in chlorophyll a/b binding proteins in Solanaceae cybrids.  Molecular and General Genetics. (1995);  249 648-654
  • 5 Bagnall D., Wolfe J., King R. W.. Chill-induced wilting and hydraulic recovery in mung bean plants.  Plant, Cell and Environment. (1983);  6 457-464
  • 6 Bernacchi D., Beck-Bunn T., Eshed Y., Lopez J., Petiard V., Uhlig J., Zamir D., Tanksley S.. Advanced backcross QTL analysis of tomato. I. Identification of QTLs for traits of agronomic importance from Lycopersicon hirsutum. .  Theoretical and Applied Genetics. (1998 a);  97 381-397
  • 7 Bernacchi D., Beck-Bunn T., Emmatty D., Eshed Y., Inai S., Lopez J., Petiard V., Sayama H., Uhlig J., Zamir D., Tanksley S.. Advanced backcross QTL analysis of tomato. II. Evaluation of near-isogenic lines carrying single donor introgressions for desirable wild QTL alleles derived from Lycopersicon hirsutum and L. pimpinellifolium. .  Theoretical and Applied Genetics. (1998 b);  97 1191-1196
  • 8 Besford R. T., Withers A. C., Ludwig L. J.. Ribulose bisphosphate carboxylase activity and photosynthesis during leaf development in tomato.  Journal of Experimental Botany. (1985);  35 495-504
  • 9 Bilger W., Björkman O.. Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossipium hirsutum L. and Malva parviflora L.  Planta. (1991);  184 226-234
  • 10 Bloom A. J., Randall L. B., Meyerhoff P. A., St. Clair D. A.. The chilling sensitivity of root ammonium influx in a cultivated and wild tomato.  Plant, Cell and Environment. (1998);  21 191-199
  • 11 Brücher H.. Lycopersicon esculentum, Lycopersicon humboldtii. . Tropische Nutzpflanzen. Berlin, Heidelberg, New York; Springer (1977): 380-390
  • 12 Brüggemann W.. Low-temperature limitations of photosynthesis in three tropical Vigna species: A chlorophyll fluorescence study.  Photosynthesis Research. (1992 a);  34 301-310
  • 13 Brüggemann W.. Photosynthesis and carbon metabolism of ecotypes of Lycopersicon peruvianum as affected by long-term chilling stress.  Verhandlungen der Gesellschaft für Ökologie. (1992 b);  21 375-378
  • 14 Brüggemann W.. Long-term chilling of young tomato plants under low light. VI. Differential chilling sensitivity of ribulose-1,5-bisphosphate carboxylase/oxygenase is linked to the oxidation of cystein residues.  Plant and Cell Physiology. (1995);  36 733-736
  • 15 Brüggemann W., Dauborn B.. Long-term chilling of young tomato plants under low light. III. Leaf development as reflected by photosynthesis parameters.  Plant and Cell Physiology. (1993);  34 1251-1258
  • 16 Brüggemann W., Linger P.. Long-term chilling of young tomato plants under low light. IV. Differential responses of chlorophyll fluorescence quenching coefficients in Lycopersicon species of different chilling tolerance.  Plant and Cell Physiology. (1994);  35 585-591
  • 17 Brüggemann W., Wolter F.. Decrease of energy-dependent quenching, but no major changes of photosynthesis parameters in Arabidopsis thaliana with genetically engineered phosphatidyl glycerol composition.  Plant Science. (1995);  108 13-21
  • 18 Brüggemann W., van der Kooij T. A. W., van Hasselt P. R.. Long-term chilling of young tomato plants under low light and subsequent recovery. I. Growth, development and photosynthesis.  Planta. (1992 a);  186 172-178
  • 19 Brüggemann W., van der Kooij T. A. W., van Hasselt P. R.. Long-term chilling of young tomato plants under low light and subsequent recovery. II. Chlorophyll fluorescence, carbon metabolism and activity of ribulose-1,5-bisphosphate carboxylase/oxygenase.  Planta. (1992 b);  186 179-187
  • 20 Brüggemann W., Klaucke S., Maas-Kantel K.. Long-term chilling of young tomato plants under low light. V. Kinetic and molecular properties of two key enzymes of the Calvin cycle in a wild and the domestic tomato species.  Planta. (1994);  194 160-168
  • 21 Brüggemann W., Dauborn B., Klaucke S., Linger P., Maas-Kantel K., Wenner A.. Chilling sensitivity of photosynthesis: Ecophysiological studies in two Lycopersicon species of different chilling tolerance.  Acta Physiologia Plantarum. (1995 a);  17 113-122
  • 22 Brüggemann W., Wenner A., Sakata Y.. Long-term chilling of young tomato plants under low light. VII. Increasing chilling tolerance of photosynthesis in Lycopersicon esculentum by somatic hybridization with L. peruvianum. .  Plant Science. (1995 b);  108 23-30
  • 23 Brüggemann W., Linger P., Wenner A., Koornneef M.. Improvement of postchilling photosynthesis in tomato by sexual hybridisation with a Lycopersicon peruvianum accession from elevated altitude.  Advances in Horticultural Science. (1996);  10 215-218
  • 24 Brüggemann W., Beyel V., Brodka M., Poth H., Weil M., Stockhaus J.. Antioxidants and antioxidative enzymes in wild type and transgenic Lycopersicon genotypes of different chilling tolerance.  Plant Science. (1999);  140 145-154
  • 25 Brunet P., Sarrobert B., Paris-Pireyre N., Risterucci A.-M.. Composition chimique de sèves xylémiques du genre Lycopersicon (Solanaceae) en relation avec l'environment. I. Effet de la température.  Canadian Journal of Botany. (1990);  68 1942-1947
  • 26 Capell B., Dörffling K.. Genotype-specific differences in chilling tolerance of maize in relation to chilling-induced changes in water status and abscisic acid accumulation.  Physiologia Plantarum. (1993);  88 636-646
  • 27 Chasan R.. Internal signals: charting a course through the chloroplast.  Plant Cell. (1995);  7 1343-1345
  • 28 Choudhoury B.. Hybridization between Lycoperscion esculentum Mill. and Lycopersicon peruvianum Mill.  Indian Journal of Horticulture. (1959);  16 102-107
  • 29 Clarke J. E., Johnson G. N.. In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley.  Planta. (2001);  212 808-816
  • 30 Daie J., Campbell W. F.. Response of tomato plant to stressful temperatures. Increase in abscisic acid concentration.  Plant Physiology. (1981);  67 26-29
  • 31 Dalziel A. W., Breidenbach R. W.. Physical properties of mitochondrial lipids for Lycopersicon hirsutum. .  Plant Physiology. (1982);  70 376-380
  • 32 Demmig-Adams B., Adams  III W. W.. The role of xanthophyll cycle carotenoids in the protection of photosynthesis.  Trends in Plant Science. (1996);  1 21-26
  • 33 Dauborn B., Brüggemann W.. Genome and plastome effects on photosynthesis parameters in Oenothera species of differential low-temperature tolerance.  Physiologia Plantarum. (1996);  97 79-84
  • 34 Dauborn B., Brüggemann W.. A spontaneous point mutation in the Rubisco large subunit gene impairing holoenzyme assembly renders the IVβ plastome mutant of Oenothera elata spp. hookeri extremely light- and chilling sensitive.  Physiologia Plantarum. (1998);  104 116-124
  • 35 Derks F. H. M., Hakkert J. C., Verbeek W. H. J., Colijn-Hooymans C. M.. Genome composition of asymmetric hybrids in relation to the phylogenetic distance between parents. Nucleus-chloroplast interaction.  Theoretical and Applied Genetics. (1992);  84 930-940
  • 36 Dolstra O., Venema J. H., Groot P. J., van Hasselt P. R.. Low-temperature related growth and photosynthetic performance of alloplasmic tomato (Lycopersicon esculentum Mill.) with chloroplasts from L. hirsutum Humb. et Bonpl.  Euphytica. (2002);  124 407-421
  • 37 Erickson R. O., Michelini F. J.. The plastochron index.  American Journal of Botany. (1957);  44 297-305
  • 38 Evans J. R.. The relationship between carbon dioxide limited photosynthetic rate and Rubisco content in two nuclear-cytoplasmic substitution lines of wheat, and the coordination of ribulose bisphosphate-carboxylation and electron transport capacities.  Planta. (1986);  167 351-358
  • 39 Evans J. R., Austin R. B.. The specific activity of ribulose-1,5-bisphosphatecarboxylase in relation to genotype in wheat.  Planta. (1986);  167 344-350
  • 40 Foolad M. R., Lin G. Y.. Relationship between cold tolerance during seed germination and vegetative growth in tomato: germplasm evaluation.  Journal of the American Society of Horticultural Science. (2000);  125 679-683
  • 41 Foolad M. R., Lin G. Y.. Genetic analysis of cold tolerance during vegetative growth in tomato, Lycopersicon esculentum Mill.  Euphytica. (2001);  122 105-111
  • 42 Fulton T. M., Beck-Bunn T., Emmatty D., Eshed Y., Lopez J., Petiard V., Uhlig J., Zamir D., Tanksley S. D.. QTL analysis of an advanced backcross of Lycopersicon peruvianum to the cultivated tomato and comparison with QTLs found in other wild species.  Theoretical and Applied Genetics. (1997);  95 881-894
  • 43 Gemel J., Sączyńska V., Kaniuga Z.. Galactolipase activity and free fatty acid levels in chloroplasts of domestic and wild tomatoes with different chilling tolerance.  Physiologia Plantarum. (1988);  74 509-514
  • 44 Gilmore A. M.. Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.  Physiologia Plantarum. (1997);  99 197-209
  • 45 Glick R. E., Sears B. B.. Genetically programmed chloroplast dedifferentiation as a consequence of plastome-genome incompatibility in Oenothera. .  Plant Physiology. (1994);  106 367-373
  • 46 Gradziel T. M., Robinson R. W.. Overcoming unilateral breeding barriers between Lycopersicon peruvianum and cultivated tomato, Lycopersicon esculentum. .  Euphytica. (1991);  54 1-9
  • 47 Guye M. G., Wilson J. M.. The effects of chilling and chill-hardening temperatures on stomatal behaviour in a range of chill-sensitive species and cultivars.  Plant Physiology and Biochemistry. (1987);  25 717-721
  • 48 Hagemann R.. Allgemeine Genetik. Jena; Fischer (1986): 280
  • 49 Hall D. O., Rao K. K.. Chloroplast genetics, expression and regulation of genes. In Photosynthesis, 5th ed. Cambridge; University Press (1994): 150-151
  • 50 Hall T. J.. Resistance at the Tm-2 locus in the tomato to tomato mosaic virus.  Euphytica. (1980);  29 189-197
  • 51 Havaux M.. Effects of chilling on the redox state of the primary electron acceptor QA of photosystem II in chilling-sensitive and resistant plant species.  Plant Physiology and Biochemistry. (1987);  25 735-743
  • 52 Heber U.. Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants.  Phytosynthesis Research. (2002);  73 223-231
  • 53 Hiratsuka J., Shimada H., Whittier R.. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals.  Molecular Genome and Genetics. (1989);  217 185-194
  • 54 Jarl C. I., Ljungberg U. K., Bornman C. H.. Correction of chlorophyll-defective male-sterile winter oilseed rape (Brassica napus) through organelle exchange: Characterization of the chlorophyll deficiency.  Physiologia Plantarum. (1988);  72 505-510
  • 55 Jones P., Keane E. M., Osborne B. A.. Effects of alien cytoplasmic variation on carbon assimilation and productivity in wheat.  Journal of Experimental Botany. (1998 a);  49 1519-1528
  • 56 Jones T. L., Tucker D. E., Ort D. R.. Chilling delays circadian pattern of sucrose phosphate synthase and nitrate reductase activity in tomato.  Plant Physiology. (1998 b);  118 149-158
  • 57 Kalloo G.. Interspecific and intergeneric hybridization in tomato. Kalloo, G., ed. Genetic Improvement of Tomato. Heidelberg, New York; Springer (1991): 73-82
  • 58 Knight S., Andersson J., Brändeis C. J.. Crystallographic analysis of ribulose-1,5-bisphosphate carboxylase from spinach at 2,4 Å resolution.  Journal of Molecular Biology. (1990);  215 113-160
  • 59 Koroleva O. Y., Krause G. H., Brüggemann W.. Effects of long-term chilling on xanthophyll cycle activity and non-photochemical fluorescence quenching in Lycopersicon genotypes.  Journal of Plant Physiology. (2000);  156 341-349
  • 60 Kochevenko A. S., Ratushnyak Y. I., Korneev D. Y., Stasik O. O., Shevchenko V. V., Kochubei S. M., Gleba Y. Y.. Photosynthetic apparatus in a cytoplasmic hybrid of cultured tomato carrying the nucleocytoplasmic incompatibility trait.  Russian Journal of Plant Physiology. (1999);  46 474-481
  • 61 Linger P.. Wachstum und Photosynthese in einer Hybridpopulation von Lycopersicon esculentum × Lycopersicon peruvianum: Kausale Zusammenhänge und putative Genorte. PhD thesis, University of Düsseldorf, Germany. (1998)
  • 62 Linger P., Brüggemann W.. Correlations between chlorophyll fluorescence quenching parameters and photosynthesis in a segregating Lycopersicon esculentum × L. peruvianum population as measured under constant conditions.  Photosynthesis Research. (1999);  61 145-156
  • 63 Low L. S., Ort D. R., Cramer W. A., Whitmarsh J., Martin B.. Search for an endotherm in chloroplast lamellar membranes associated with chilling-inhibition of photosynthesis.  Achievements in Biochemistry and Biophysics. (1984);  231 336-344
  • 64 Lyons J. M., Raison J. K.. Oxidative activity of mitochondria isolated from plant tissues sensitive and resistant to chilling injury.  Plant Physiology. (1970);  45 386-389
  • 65 Marangoni A. G., Smith A. K., Yada R. Y., Stanley D. W.. Ultra structural changes associated with chilling injury in mature-green tomato fruit.  Journal of the American Society of Horticultural Science. (1989);  114 958-962
  • 66 Martin F. W.. Complex unilateral hybridization in Lycopersicon hirsutum. .  Genetics. (1961);  47 855-857
  • 67 Martino-Catt S., Ort D. R.. Low temperature interrupts circadian regulation activity in chilling sensitive plants.  Proceedings of the National Academy of Sciences of the USA. (1992);  89 3731-3735
  • 68 Miltau O., Zamir D., Rudich J.. Breeding for chilling tolerance in tomato: an examination of selection criteria.  Eucarpia. (1984);  9 45-50
  • 69 Miltau O., Zamir D., Rudich J.. Growth rates of Lycopersicon species at low temperature.  Zeitschrift für Pflanzenzüchtung. (1986);  96 193-199
  • 70 Monforte A. J., Tanksley S. D.. Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: A tool for gene mapping and gene discovery.  Genome. (2000);  43 803-813
  • 71 Nishida I., Murata N.. Chilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipids.  Annual Review of Plant Physiology and Plant Molecular Biology. (1996);  47 541-568
  • 72 Oyanedel E., Wolfe D. W., Monforte A. J., Tanksley S. D., Owens T. G.. Using Lycopersicon hirsutum as a source of cold tolerance in processing tomato breeding.  Acta Horticulturae. (2001);  542 387-391
  • 73 Parokonny A. S., Marshall J. A., Bennett M. D.. Homologous pairing and recombination in backcross derivatives of tomato somatic hybrids (Lycopersicon esculentum + L. peruvianum).  Theoretical and Applied Genetics. (1997);  94 713-723
  • 74 Patterson B. D.. Genes for cold resistance from wild tomatoes.  HortScience. (1988);  23 794 947
  • 75 Patterson B. D., Graham D.. Effect of chilling temperatures on the proteoplasmic streaming of plants from different climates.  Journal of Experimental Biology. (1977);  28 736-743
  • 76 Patterson B. D., Paull R., Smillie R. M.. Chilling resistance in Lycopersicon hirsutum Humb. and Bonpl., a wild tomato with a wide altitudinal distribution.  Australian Journal of Plant Physiology. (1978);  5 609-617
  • 77 Patterson B. D., Payne L. A.. Screening for chilling resistance in tomato seedlings.  HortScience. (1983);  18 340-341
  • 78 Paull R. E., Patterson B. D., Graham D.. Chilling injury assays for plant breeding. Lyons, J. M., Graham, D., and Raison, J. K., eds. Low Temperature Stress in Crop Plants: The Role of the Membrane. New York; Academic Press (1979): 507-519
  • 79 Pearce R. S.. Molecular analysis of acclimation to cold.  Plant Growth Regulation. (1999);  29 47-76
  • 80 Peter S., Spang O., Medgyesy P., Schäfer C.. Consequences of intergeneric chloroplast transfers on photosynthesis and sensitivity to high light.  Australian Journal of Plant Physiology. (1999);  26 171-177
  • 81 Pérez de Juan J., Irigoyen J. J., Sánchez-Díaz M.. Chilling of drought-hardened and non-hardened plants of different chilling-sensitive maize lines. Changes in water relations and ABA contents.  Plant Science. (1997);  122 71-79
  • 82 Raison J. K., Brown M. A.. Sensitivity of altitudinal ecotypes of wild tomato Lycopersicon hirsutum to chilling injury.  Plant Physiology. (1989);  91 1471-1475
  • 83 Raison J. K., Lyons J. M.. Chilling injury: a plea for uniform terminology.  Plant, Cell and Environment. (1986);  9 685-686
  • 84 Rick C. M.. Potential genetic resources in tomato species: clues from observations in native habitats. Hollaender, A. and Srb, A. M., eds. Genes, Enzymes and Populations. New York; Plenum Press (1973): 255-269
  • 85 Rick C. M.. Reproductive isolation in the Lycopersicon peruvianum complex. D'Arcy, W. G., ed. Solanaceae Biology and Systematics. New York; Columbia University Press (1986): 477-495
  • 86 Rick C. M.. Tomato Lycopersicon esculentum (Solanaceae). Simmons, N. W., ed. Evolution of Crop Plants, 2nd ed. London; Longman (1995): 452-457
  • 87 Sakata Y., Momma S.. Genetic instability of a progeny from a somatic hybrid between tomato (Lycopersicon esculentum) and L. peruvianum. .  Plant Science. (1993);  90 225-232
  • 88 Savitch L. V., Massacci A., Gray G. R., Huner N. P. A.. Acclimation to low temperature or high light mitigates sensitivity to photoinhibition: Roles of the Calvin cycle and the Mehler reaction.  Australian Journal of Plant Physiology. (2000);  27 253-264
  • 89 Sato S., Nakamura Y., Kaneko T., Asamizu E., Tabata S.. Complete structure of the chloroplast genome of Arabidopsis thaliana. .  DNA Research. (1999);  6 283-290
  • 90 Scott S. J., Jones R. A.. Quantifying seed germination responses to low temperatures: variation among Lycopersicon spp.  Environmental and Experimental Botany. (1985);  25 129-137
  • 91 Shinozaki K., Ohme M., Tanaka M.. The complete nucleotide sequence of the tobacco chloroplast genome, its gene organization and expression.  EMBO Journal. (1986);  5 2043-2049
  • 92 Smart D. R., Bloom A. J.. Influence of root NH4 and NO3- content on the temperature response of net NH4 and NO3 - uptake in chilling sensitive and chilling resistant Lycopersicon taxa.  Journal of Experimental Botany. (1991);  42 331-338
  • 93 Smillie R. M., Nott R.. Assay of chilling injury in wild and domestic tomatoes based on photosystem activity of the chilled leaves.  Plant Physiology. (1979);  63 796-801
  • 94 Smith P. G.. Embryo culture of a tomato species hybrid.  Proceedings of the American Society of Horticultural Science. (1944);  44 413-416
  • 95 Stitt M., Schulze D.. Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology.  Plant, Cell and Environment. (1994);  17 465-487
  • 96 Stern D. B., Higgs D. C., Yang J.. Transcription and translation in chloroplasts.  Trends in Plant Science. (1997);  2 308-315
  • 97 Streb P., Shang W., Feierabend J., Blingny R.. Divergent strategies of photoprotection in high-mountain plants.  Planta. (1998);  207 313-324
  • 98 Tanksley S. D., Ganal M. W., Prince J. P., de Vicente M. C., Bonierbale M. W., Broun P., Fulton T. M., Giovannoni J. J., Grandillo S., Martin G. B., Messeguer R., Miller J., Miller L., Paterson A. H., Pineda O., Röder M. S., Wing R. A., Wu W., Young N. D.. High density molecular linkage map of the tomato and potato genomes.  Genetics. (1992);  132 1141-1160
  • 99 Taylor I. B.. Biosystematics of the tomato. Artherton, J. G. and Rudich, J., eds. The Tomato Crop: A Scientific Basis for Improvement. London; Chapmann and Hall (1986): 1-34
  • 100 Taylor W. C.. Regulatory interactions between nuclear and plastid genomes.  Annual Review of Plant Physiology and Plant Molecular Biology. (1989);  40 211-233
  • 101 Torrecillas A., Guillaume C., Alarcón J. J., Ruiz-Sánchez M. C.. Water relations of two tomato species under water stress and recovery.  Plant Science. (1995);  105 169-176
  • 102 Truco M. J., Randall L. B., Bloom A. J., St. Clair D. A.. Detection of QTLs associated with shoot wilting and root ammonium uptake under chilling temperatures in an interspecific backcross population from Lycopersicon esculentum × L. hirsutum. .  Theoretical and Applied Genetics. (2000);  101 1082-1092
  • 103 Vallejos C. E.. Genetic diversity of plants for response to low temperatures and its potential use in crop plants. Lyons, J. M., Graham, D., and Raison, J. K., eds. Low Temperature Stress in Crop Plants: The Role of the Membrane. New York; Academic Press (1979): 473-489
  • 104 Vallejos C. E.. Low night temperatures have a differential effect on the diurnal cycling of gene expression in cold-sensitive and tolerant tomatoes.  Plant, Cell and Environment. (1991);  14 105-112
  • 105 Vallejos C. E., Lyons J. M., Breidenbach R. W., Miller M. F.. Characterization of a differential low-temperature growth response in two species of Lycopersicon: the plastochron as a tool.  Planta. (1983);  159 487-496
  • 106 Vallejos C. E., Pearcy R. W.. Differential acclimation potential to low temperatures in two species of Lycopersicon: photosynthesis and growth.  Canadian Journal of Botany. (1987);  65 1303-1307
  • 107 Vallejos C. E., Tanksley S. D.. Segregation of isozyme markers and cold tolerance in an interspecific backcross of tomato, Lycopersicon esculentum × Lycopersicon hirsutum. .  Theoretical and Applied Genetics. (1983);  96 241-247
  • 108 Van der Kooij T. A. W., Brüggemann W., van Hasselt P. R.. Sugar-starch partitioning in tomato leaves as affected by temperature.  Photosynthetica. (1992);  27 579-584
  • 109 Van Heusden A. W., Koornneef M., Voorrips R. E., Brüggemann W., Pet G., Vrielink - van Ginkel R., Chen X., Lindhout P.. Three QTLs from Lycopersicon peruvianum confer a high level of resistance to Clavibacter michiganensis spp. michiganensis. .  Theoretical and Applied Genetics. (1999);  99 1068-1074
  • 110 Van Ooijen J. W., Maliepaard C.. MapQTL™ version 3.0: Software for the calculation of QTL positions on genetic maps. Wageningen, The Netherlands; CPRO-DLO (1996)
  • 111 Venema J. H.. Low-temperature tolerance of tomato and related wild Lycopersicon species: a comparative study on chloroplast functioning. PhD thesis, University of Groningen, The Netherlands. (2001)
  • 112 Venema J. H., Eekhof M., van Hasselt P. R.. Analysis of low-temperature tolerance of a tomato (Lycopersicon esculentum) cybrid with chloroplasts from a more chilling- tolerant L. hirsutum accession.  Annals of Botany. (2000 a);  85 799-807
  • 113 Venema J. H., Posthumus F., van Hasselt P. R.. Impact of suboptimal temperature on growth, photosynthesis, leaf pigments and carbohydrates of domestic and high altitude wild Lycopersicon species.  Journal of Plant Physiology. (1999 a);  155 711-718
  • 114 Venema J. H., Posthumus F., de Vries M., van Hasselt P. R.. Differential response of domestic and wild Lycopersicon species to chilling under low light: growth, carbohydrate content, photosynthesis and the xanthophyll cycle.  Physiologia Plantarum. (1999 b);  105 81-88
  • 115 Venema J. H., Villerius L., van Hasselt P. R.. Effect of acclimation to suboptimal temperature on chilling-induced photodamage: comparison between a domestic and a high-altitude wild Lycopersicon species.  Plant Science. (2000 b);  152 153-163
  • 116 Von Caemmerer S., Farquhar G. D.. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.  Planta. (1981);  153 376-387
  • 117 Walker M. A., McKersie B. D.. Role of ascorbate-glutathione antioxidant system in chilling tolerance of tomato.  Journal of Plant Physiology. (1993);  141 234-239
  • 118 Walker M. A., McKersie B. D., Pauls K. P.. Effects of chilling on the Biochemical and functional properties of thylakoid membranes.  Plant Physiology. (1991);  97 663-669
  • 119 Walker M. A., Smith D. M., Pauls K. P., McKersie B. D.. A chlorophyll fluorescence screening test to evaluate chilling tolerance in tomato.  HortScience. (1990);  25 334-339
  • 120 Wolters A., Jacobsen E., O'Connell M., Bonnema G., Ramulu K. S., de Jong H., Schoenmakers H., Wijbrandi J., Koornneef M.. Somatic hybridization as a tool for tomato breeding.  Euphytica. (1994);  79 265-277
  • 121 Wolf S., Yakir D., Stevens M. A., Rudich J.. Cold temperature tolerance of wild tomato species.  Journal of the American Society of Horticultural Science. (1986);  111 960-964
  • 122 Yakir D., Rudich J., Bravdo B. A.. Adaptation to chilling: photosynthetic characteristics of the cultivated tomato and a high altitude wild species.  Plant, Cell and Environment. (1986);  9 477-484
  • 123 Zamir D., Gadish I.. Pollen selection for low temperature adaptation in tomato.  Theoretical and Applied Genetics. (1987);  74 545-548
  • 124 Zamir D., Tanksley S. D., Jones R. A.. Low temperature effect on selective fertilization by pollen mixtures of wild and cultivated tomato species.  Theoretical and Applied Genetics. (1981);  59 235-238
  • 125 Zhan H.-X., Blumwald E.. Transgenic salt-tolerant tomato plants accumulate salt in the foliage but not in the fruits.  Nature Biotechnology. (2001);  19 765-768

W. Brüggemann

Botanisches Institut, Box 213
J. W. Goethe-Universität Frankfurt am Main

Postfach 111932

60054 Frankfurt am Main

Germany

eMail: w.brueggemann@em.uni-frankfurt.de

Editor: J. Raven

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