QTL Mapping for a Trade-Off between Leaf and Bud Production in a Recombinant Inbred Population of Microseris douglasii and M. bigelovii (Asteraceae, Lactuceae): A Potential Preadaptation for the Colonization of Serpentine Soils

Abstract

The different response to growth on serpentine soil is a major autecological difference between the annual asteracean species Microseris douglasii and M. bigelovii, with nearly non-overlapping distribution ranges in California. Early flowering and seed set is regarded as a crucial character contributing to escape drought and thus is strongly correlated with survival and reproductive success on serpentine as naturally toxic soil. M. bigelovii (strain C94) from non-serpentine soil produces more leaves at the expense of bud production in the first growing phase than M. douglasii (B14) from serpentine soil. A QTL mapping study for this trade-off and for other growth-related traits was performed after six generations of inbreeding (F7) from a single interspecific hybrid between B14 and C94 on plants that were grown on serpentine and alternatively on normal potting soil. The trade-off is mainly correlated with markers on one map region on linkage group 03a (lg03a) with major phenotypic effects (phenotypic variance explained [PVE] = 18.8 - 31.7 %). Plants with the M. douglasii allele in QTL-B1 (QTL-NL1) produce more buds but fewer leaves in the first 119 days on both soil types. Three modifier QTL could be mapped for bud and leaf production. In one modifier (QTL-B2 = QTL-NL4) the M. douglasii allele is again associated with more buds but fewer leaves. QTL mapped for bud set in the F6 co-localize with QTL-B1 (major QTL) and QTL-B3. Two additional QTL for leaf length and red coloration of leaves could be mapped to one map region on lg03a. Co-localization of the two QTL loci with major phenotypic effects on bud and leaf production strongly suggests that a major genetic locus controls the trade-off between the two adaptive traits. The importance of mutational changes in major genes for the adaptation to stressful environments is discussed.

Key words

Trade-off - serpentine soil - QTL - ecological genetics - Microseris.

References

• 1 Bachmann K., Gailing O.. The genetic dissection of the stepwise evolution of morphological characters. Stuessy, T. F., Mayer, V., and Hörandl, E., eds. Deep Morphology: Toward a Renaissance of Morphology in Plant Systematics. Königstein; Koeltz (2003): 35-62
• 2 Bachmann K., Hombergen E.-J.. Mapping genes for phenotypic variation in Microseris (Lactuceae) with molecular markers. Caligari, P. D. S. and Hind, D. J. N., eds. Compositae: Biology and Utilization. Kew; Royal Botanic Gardens (1996): 23-43
• 3 Bachmann K., Hombergen E.-J.. From phenotype via QTL to virtual phenotype in Microseris (Asteraceae): predictions from multilocus marker genotypes.  New Phytologist. (1997);  137 9-18
• 4 Battjes J., Chambers K. L., Bachmann K.. Evolution of microsporangium numbers in Microseris (Asteraceae: Lactuceae).  American Journal of Botany. (1994);  81 641-647
• 5 Beavis W., Grant D.. The power and deceit of QTL experiments: lessons from comparative studies. In Proceedings of the 49^th Annual Corn and Sorghum Industry Research Conference. Chicago, IL; (1994): 250-266
• 6 Bradshaw H. D., Otto K. G., Freven B. E., McKay J. K., Schemske D. W.. Quantitative Trait Loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). .  Genetics. (1998);  149 367-382
• 7 Churchill G. A., Doerge R. W.. Empirical threshold values for quantitative trait mapping.  Genetics. (1994);  138 963-971
• 8 Coyne J. A., Lande R.. The genetic basis of species differences in plants.  American Naturalist. (1985);  126 141-145
• 9 Doebley J., Stec A., Gustus C.. Teosinte branched 1 and the origin of maize: evidence for epistasis and the evolution of dominance.  Genetics. (1995);  141 333-346
• 10 Fisher R. A.. The Genetical Theory of Natural Selection. Oxford; Oxford University Press (1930)
• 11 Fishman L., Kelly A. J., Willis J. H.. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. .  Evolution. (2002);  56 2138-2155
• 12 Gailing O., Bachmann K.. The evolutionary reduction of microsporangia in Microseris (Asteraceae): Transition genotypes and phenotypes.  Plant Biology. (2000);  2 455-461
• 13 Gailing O., Bachmann K.. QTL analysis reveals different and independent modes of inheritance for diagnostic achene characters in Microseris (Asteraceae).  Organisms Diversity and Evolution. (2002);  2 277-288
• 14 Gailing O., Bachmann K.. QTL mapping reveals a two-step model for the evolutionary reduction of inner microsporangia within the Asteracean genus Microseris. .  Theoretical and Applied Genetics. (2003);  107 893-901
• 15 Gailing O., Hombergen E.-J., Bachmann K.. QTL mapping reveals specific genes for the evolutionary reduction of microsporangia in Microseris. .  Plant Biology. (1999);  1 219-225
• 16 Geldermann H.. Investigations on inheritance of quantitative characters in animals by gene markers I. Methods.  Theoretical and Applied Genetics. (1975);  46 319-330
• 17 Gottlieb L. D., Ford V. S.. Genetic studies of the pattern of floral pigmentation in Clarkia gracilis. .  Heredity. (1988);  60 237-246
• 18 Haley C. S., Knott S. A.. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers.  Heredity. (1992);  69 315-324
• 19 Hawthorne D. J., Via S.. Genetic linkage of ecological specialization and reproductive isolation in pea aphids.  Nature. (2001);  412 904-907
• 20 Hombergen E.-J., Bachmann K.. RAPD mapping of three QTLs determining trichome formation in Microseris hybrid H27 (Asteraceae: Lactuceae).  Theoretical and Applied Genetics. (1995);  90 853-858
• 21 Hurme P., Sillanpaa M. J., Arjas E., Repo T., Savolainen O.. Genetic basis of climatic adaptation in scots pine by bayesian quantitative trait locus analysis.  Genetics. (2000);  156 1309-1322
• 22 Kearsey M. J., Farquhar A. G. L.. QTL analysis in plants; where are we now?.  Heredity. (1998);  80 137-142
• 23 Kobayashi Y., Koyama H.. QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. .  Plant Cell Physiology. (2002);  43 1526-1533
• 24 Lander E. S., Botstein D.. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps.  Genetics. (1989);  121 185-199
• 25 Lander E. S., Green P., Abrahamson J., Barlow A., Daly M. J., Lincoln S. E., Newburg L.. MAPMAKER; an interactive computer program for constructing genetic linkage maps of experimental and natural populations.  Genomics. (1987);  1 174-181
• 26 Lauter N., Doebley J.. Genetic variation of phenotypically invariant traits detected in teosinte: implications for the evolution of novel forms.  Genetics. (2002);  160 333-342
• 27 Lin J.-Z., Ritland K.. Quantitative trait loci differentiating the outbreeding Mimulus guttatus from the inbreeding M. platycalyx. .  Genetics. (1997);  146 1115-1121
• 28 Macnair M. R.. Major genes for copper tolerance in Mimulus guttatus. .  Nature. (1977);  268 428-430
• 29 Macnair M. R.. The genetic control of copper tolerance in the yellow monkey flower Mimulus guttatus. .  Heredity. (1983);  50 283-293
• 30 Macnair M. R.. Tansley review No. 49: The genetics of metal tolerance in vascular plants.  New Phytologist. (1993);  124 541-559
• 31 Macnair M. R., Cumbes Q. J.. The genetic architecture of interspecific variation in Mimulus. .  Genetics. (1989);  122 211-222
• 32 Macnair M. R., Cumbes Q. J., Meharg A. A.. The genetics of arsenate tolerance in Yorkshire fog Holcus lanatus. .  Heredity. (1992);  69 325-335
• 33 Macnair M. R., Gardner M.. The evolution of edaphic endemics. Howard, D. J. and Berlocher, S. H., eds. Endless Forms. New York; OUP (1998): 157-171
• 34 Martinez O., Curnow R. N.. Estimating the locations and the sizes of the effects of quantitative trait loci using flanking markers.  Theoretical and Applied Genetics. (1992);  85 480-488
• 35 Martinez O., Curnow R. N.. Missing markers when estimating quantitative trait loci using regression mapping.  Heredity. (1994);  73 198-206
• 36 Mitchell-Olds T.. Genetic constraints on life-history evolution: quantitative-trait loci influencing growth and flowering in Arabidopsis thaliana. .  Evolution. (1996);  50 140-145
• 37 Moritz D. M. L., Kadereit J. W.. The genetics of evolutionary change in Senecio vulgaris L.: A QTL mapping approach.  Plant Biology. (2001);  3 544-552
• 38 Nelson J. C.. QGENE: software for marker-based genomic analysis and breeding.  Molecular Breeding. (1997);  3 239-245
• 39 Orr H. A.. The population genetics of adaptation: The distribution of factors fixed during adaptive evolution.  Evolution. (1998);  52 935-949
• 40 Orr H. A.. The evolutionary genetics of adaptation: a simulation study.  Genetical Research. (1999);  74 207-214
• 41 Orr H. A.. The genetics of species differences.  Trends in Ecology and Evolution. (2001);  16 343-350
• 42 Orr H. A., Coyne J. A.. The genetics of adaptation revisited.  American Naturalist. (1992);  140 725-742
• 43 Reiter R. S., Coors J. G., Sussman M. R., Gabelmann W. H.. Genetic analysis of tolerance to low- phosphorus stress in maize using restriction fragment length polymorphism.  Theoretical and Applied Genetics. (1991);  82 561-568
• 44 Rieseberg L. H., Archer M. A., Wayne R. K.. Transgressive segregation, adaptation and speciation.  Heredity. (1999);  83 363-372
• 45 Rieseberg L. H., Raymond O., Rosenthal D. M., Lai Z., Livingstone K., Nakazato T., Durphy J. L., Schwarzbach A. E., Donovan L. A., Lexer C.. Major ecological transitions in wild sunflowers facilitated by hybridization.  Science. (2003);  301 1211-1216
• 46 Schat H., ten Bookum W. M.. Genetic control of copper tolerance in Silene vulgaris. .  Heredity. (1992);  68 219-229
• 47 Schwarzbach A. E., Donovan L. A., Rieseberg L. H.. Transgressive character expression in a hybrid sunflower species.  American Journal of Botany. (2001);  88 270-277
• 48 Sourdille P., Snape J. W., Cadalen T., Charmet G., Nakata N., Bernard S., Bernard M.. Detection of QTLs for heading time and photoperiod response in wheat using a doubled-haploid population.  Genome. (2000);  43 487-494
• 49 Tanksley S. D.. Mapping polygenes.  Annual Review Genetics. (1993);  27 205-233
• 50 Ungerer M. C., Halldorsdottir S. S., Modliszewski J. L., Mackay T. F., Purugganan M. D.. Quantitative Trait Loci for inflorescence development in Arabidopsis thaliana. .  Genetics. (2002);  160 1133-1151
• 51 Vlot E. C., van Houten W. H. J., Mauthe S., Bachmann K.. Genetic and nongenetic factors influencing deviations from five pappus parts in a hybrid between Microseris douglasii and M. bigelovii (Asteraceae, Lactuceae).  International Journal of Plant Sciences. (1992);  153 89-97
• 52 Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M., Zabeau M.. AFLP: a new technique for DNA fingerprinting.  Nucleic Acids Research. (1995);  23 4407-4414
• 53 Watkins A. J., Macnair M. R.. Genetics of arsenic tolerance in Agrostis capillaries L.  Heredity. (1991);  66 47-54
• 54 Westerbergh A., Doebley J.. Morphological traits defining species differences in wild relatives of maize are controlled by multiple quantitative trait loci.  Evolution. (2002);  56 273-283
• 55 Xu W., Subudhi P. K., Crasta O. R., Rosenow D. T., Mullet J. E., Nguyen H. T.. Molecular mapping of QTLs conferring staygreen in grain sorghum (Sorghum bicolour L. Moench).  Genome. (2000);  43 461-469

Section Editor: F. Salamini