Mendelian Factors Underlying Quantitative Traits in Tomato: Comparison Across Species, Generations, and Environments

INVESTIGATIONS

Mendelian Factors Underlying Quantitative Traits in Tomato: Comparison Across Species, Generations, and Environments

A. H. Paterson, S. Damon, J. D. Hewitt, D. Zamir, H. D. Rabinowitch, S. E. Lincoln, E. S. Lander and S. D. Tanksley
Department of Plant Breeding and Biometry, Cornell University, Ithaca, New York 14853 Current address: E. I. DuPont de Nemours, Wilmington, Delaware 19880-0402, and Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19711.

As part of ongoing studies regarding the genetic basis of quantitative variation in phenotype, we have determined the chromosomal locations of quantitative trait loci (QTLs) affecting fruit size, soluble solids concentration, and pH, in a cross between the domestic tomato (Lycopersicon esculentum Mill.) and a closely-related wild species, L. cheesmanii. Using a RFLP map of the tomato genome, we compared the inheritance patterns of polymorphisms in 350 F(2) individuals with phenotypes scored in three different ways: (1) from the F(2) progeny themselves, grown near Davis, California; (2) from F(3) families obtained by selfing each F(2) individual, grown near Gilroy, California (F(3)-CA); and (3) from equivalent F(3) families grown near Rehovot, Israel (F(3)-IS). Maximum likelihood methods were used to estimate the approximate chromosomal locations, phenotypic effects (both additive effects and dominance deviations), and gene action of QTLs underlying phenotypic variation in each of these three environments. A total of 29 putative QTLs were detected in the three environments. These QTLs were distributed over 11 of the 12 chromosomes, accounted for 4.7-42.0% of the phenotypic variance in a trait, and showed different types of gene action. Among these 29 QTLs, 4 were detected in all three environments, 10 in two environments, and 15 only in a single environment. The two California environments were most similar, sharing 11/25 (44%) QTLs, while the Israel environment was quite different, sharing 7/20 (35%) and 5/26 (19%) QTLs with the respective California environments. One major goal of QTL mapping is to predict, with maximum accuracy, which individuals will produce progeny showing particular phenotypes. Traditionally, the phenotype of an individual alone has been used to predict the phenotype of its progeny. Our results suggested that, for a trait with low heritability (soluble solids), the phenotype of F(3) progeny could be predicted more accurately from the genotype of the F(2) parent at QTLs than from the phenotype of the F(2) individual. For a trait with intermediate heritability (fruit pH), QTL genotype and observed phenotype were about equally effective at predicting progeny phenotype. For a trait with high heritability (mass per fruit), knowing the QTL genotype of an individual added little if any predictive value, to simply knowing the phenotype. The QTLs mapped in the L. esculentum X L. cheesmanii F(2) appear to be at similar locations to many of those mapped in a previous cross with a different wild tomato (L. chmielewskii). One possible explanation of this similarity is that genetic factors at some of the same loci may affect the traits in the two distantly-related wild species. Potentially major implications of such similarity across broad genetic distances are discussed, in regard to plant and animal breeding, germplasm introgression, and cloning of QTLs.

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				D. Zhong, A. Pai, and G. Yan Costly Resistance to Parasitism: Evidence From Simultaneous Quantitative Trait Loci Mapping for Resistance and Fitness in Tribolium castaneum Genetics, April 1, 2005; 169(4): 2127 - 2135. [Abstract] [Full Text] [PDF]

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				K. D. Jermstad, D. L. Bassoni, K. S. Jech, G. A. Ritchie, N. C. Wheeler, and D. B. Neale Mapping of Quantitative Trait Loci Controlling Adaptive Traits in Coastal Douglas Fir. III. Quantitative Trait Loci-by-Environment Interactions Genetics, November 1, 2003; 165(3): 1489 - 1506. [Abstract] [Full Text] [PDF]

				H. E. E. Holtan and S. Hake Quantitative Trait Locus Analysis of Leaf Dissection in Tomato Using Lycopersicon pennellii Segmental Introgression Lines Genetics, November 1, 2003; 165(3): 1541 - 1550. [Abstract] [Full Text] [PDF]

				R. C. Babu, B. D. Nguyen, V. Chamarerk, P. Shanmugasundaram, P. Chezhian, P. Jeyaprakash, S. K. Ganesh, A. Palchamy, S. Sadasivam, S. Sarkarung, et al. Genetic Analysis of Drought Resistance in Rice by Molecular Markers: Association between Secondary Traits and Field Performance Crop Sci., July 1, 2003; 43(4): 1457 - 1469. [Abstract] [Full Text] [PDF]

				B. T. Campbell, P. S. Baenziger, K. S. Gill, K. M. Eskridge, H. Budak, M. Erayman, I. Dweikat, and Y. Yen Identification of QTLs and Environmental Interactions Associated with Agronomic Traits on Chromosome 3A of Wheat Crop Sci., July 1, 2003; 43(4): 1493 - 1505. [Abstract] [Full Text] [PDF]

				S. A. Flint-Garcia, M. D. McMullen, and L. L. Darrah Genetic Relationship of Stalk Strength and Ear Height in Maize Crop Sci., January 1, 2003; 43(1): 23 - 31. [Abstract] [Full Text] [PDF]

				G. Jung, H. M. Ariyarathne, D. P. Coyne, and J. Nienhuis Mapping QTL for Bacterial Brown Spot Resistance under Natural Infection in Field and Seedling Stem Inoculation in Growth Chamber in Common Bean Crop Sci., January 1, 2003; 43(1): 350 - 357. [Abstract] [Full Text] [PDF]

				G. M. Timmerman-Vaughan, T. J. Frew, A. C. Russell, T. Khan, R. Butler, M. Gilpin, S. Murray, and K. Falloon QTL Mapping of Partial Resistance to Field Epidemics of Ascochyta Blight of Pea Crop Sci., November 1, 2002; 42(6): 2100 - 2111. [Abstract] [Full Text] [PDF]

				M. R. Knox and T. H. N. Ellis Excess Heterozygosity Contributes to Genetic Map Expansion in Pea Recombinant Inbred Populations Genetics, October 1, 2002; 162(2): 861 - 873. [Abstract] [Full Text] [PDF]

				G. B. Seymour, K. Manning, E. M. Eriksson, A. H. Popovich, and G. J. King Genetic identification and genomic organization of factors affecting fruit texture J. Exp. Bot., October 1, 2002; 53(377): 2065 - 2071. [Abstract] [Full Text] [PDF]

				R. W. Jessup, B. L. Burson, G. B. Burow, Y.-W. Wang, C. Chang, Z. Li, A. H. Paterson, and M. A. Hussey Disomic Inheritance, Suppressed Recombination, and Allelic Interactions Govern Apospory in Buffelgrass as Revealed by Genome Mapping Crop Sci., September 1, 2002; 42(5): 1688 - 1694. [Abstract] [Full Text] [PDF]

				T. C. Nesbitt and S. D. Tanksley Comparative Sequencing in the Genus Lycopersicon: Implications for the Evolution of Fruit Size in the Domestication of Cultivated Tomatoes Genetics, September 1, 2002; 162(1): 365 - 379. [Abstract] [Full Text] [PDF]