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Progress and Prospects Andrew H Downloaded from genome.cshlp.org on October 5, 2021 - Published by Cold Spring Harbor Laboratory Press REVIEW Molecular Dissection of Quantitative Traits: Progress and Prospects Andrew H. Paterson1 Department of Soil and Crop Science, Texas A&M University, College Station, Texas 77843-2474 The "molecular dissection" of quantitative traits "complete" genetic maps, encompassing all re- began before the demonstration that DNA is the gions of all chromosomes in a plant or animal hereditary molecule. Opponents of the Mende- species. Complete genetic maps permit compre- lian genetic (particulate) theory argued that hensive analysis of the genome of an organism, many traits showed "blending inheritance," with revealing the locations of QTLs influencing vir- progeny intermediate between parents. This pre- tually any characteristic that can be measured. cipitated one of the great debates in the history of The development of DNA-based genetic genetics, which was eventually resolved by the mapping technology was propelled by the search realization that blending inheritance might be for genes responsible for human genetic diseases accounted for by the independent transmission and other traits (Botstein et al. 1980). QTLs influ- of many different Mendelian factors, together encing medically important phenotypes such as with the modifying effects of environment. high blood pressure (Rapp et al. 1989) and hyper- By early in the twentieth century, associa- tension (Jacob et al. 1991) are being identified in tions of genetic markers with differences in quan- mammalian models. Recent results have illus- titative phenotypes had already been noted. For trated the usefulness of genome mapping in dis- example, Sax (1923) noted association of differ- secting complex behavioral characteristics (Plo- ences in bean seed weight with seed-coat pig- min et al. 1994), such as avoidance, exploration mentation, concluding that "Factor differences for (Neiderheiser et al. 1992), and substance abuse seed weight are ... linked with ... factors which (Crabbe et al. 1994; Quock et al. 1994) in rodents, determine the color o( the pigment. Size differences and reading disability in humans (Cardon et al. may be effected by the independent action of... fac- 1994). In one recent case, the effectiveness of a tors in different linkage groups. These factors, when human disease agent (malaria) at parasitizing its combined, have a cumulative effect. The size factors vector (mosquito) has been dissected into several in different chromosomes may not be equal in their QTLs (Severson et al. 1995). Finally, many com- effect." plex traits mapped in domestic animals, such as The principles outlined by these pioneering obesity (Andersson et al. 1994; Pelleymounter et studies were widely employed, both in model sys- al. 1995), lactation (Georges et al. 1995), and oth- tems and domesticated species. However, until ers (cf. Cockett et al. 1994; Georges et al. 1994) recently most maps contained too few genetic may be relevant to human phenotypes. An ever- markers to permit either identification of suites clearer picture of the correspondence between of quantitative trait loci (QTLs) accounting for the chromosomes of humans and other mam- the bulk of variation in a phenotype, or precise mals helps in the application of such compara- mapping of QTLs to specific chromosomal loca- tive information (cf. O'Brien et al. 1993). tions. As stated by Thoday (1961), "The main Plant breeding has provided a fertile field for practical limitation of the technique seems to be the molecular dissection of quantitative traits. availability of suitable markers, and the time that Charles Darwin recognized that plant breeding can be given to the considerable work involved." programs were very useful for the study of hered- A growing body of molecular tools, first from ity. The realization that crop improvement could protein polymorphisms (Markert and Moller benefit from DNA marker-assisted selection (cf. 1959), and, more recently, from DNA polymor- Paterson et al. 1991b) has led to rapid growth in phisms, has contributed to the development of molecular mapping of agriculturally important crops. Genetic mapping of traits associated with 1E-MAIL [email protected]; FAX (409) 845-0456. many aspects of crop productivity is published or 5:321-333 ©1995 by Cold Spring Harbor Laboratory Press ISSN 1054-9803/95 $5.00 GENOME RESEARCH ~ 321 Downloaded from genome.cshlp.org on October 5, 2021 - Published by Cold Spring Harbor Laboratory Press PATERSON in progress, including basic growth patterns such Darvasi and Weller 1992; Haley and Knott 1992; as plant height (cf. Koester et al. 1993; Lin et al. Knott and Haley 1992; Jansen 1992, 1993, 1994; 1995; M. Pereira, M. Lee, and P. Rayapati, un- Mackinnon and Georges 1992; Darvasi et al. publ.), tillering, rhizomatousness (Paterson et al. 1993; Moreno-Gonzalez 1993; Rodolphe and Le- 1995a), flowering time (cf. Koester et al. 1993; fort 1993; Zeng 1993, 1994; Cardon and Fulker Kowalski et al. 1994; Li et al. 1995a; Lin et al. 1994; Eaves 1994; Haley et al. 1994; Jiang and 1995), and other morphological variants (Ken- Zeng 1995). All share the basic principle of test- nard et al. 1994); yield components such as the ing correlation between marker genotypes and size, number, and harvestability of seed (Stuber et quantitative phenotypes. As a result of the avail- al. 1987, 1992; Abler et al. 1991; Fatokun et al. ability of complete genetic maps, current analyt- 1992; Doebley et al. 1994; Schon et al. 1994; ical methods are able to use information from Paterson et al. 1995a,b), biomass, and/or growth multiple markers that flank a QTL, in contrast to rates (DeVicente and Tanksley 1993; Bradshaw earlier methods that were limited to information and Stettler 1995); quality parameters such as from single markers at unknown distance and di- composition of fruit or seed (Paterson et al. 1988, rection from the QTL. This permits more accurate 1990, 1991a; Weller et al. 1988; DeVicente and estimates of location and phenotypic effect, of Tanksley 1993; Teutonico and Osborn 1994), individual QTLs. Although many procedures to shape of tubers (Van Eck et al. 1994), or specific date have been parametric, approaches to han- gravity of wood (Groover et al. 1994); and the dling nonparametric traits are beginning to impact of adverse factors such as diseases (Bubeck emerge (Kruglyak and Lander 1995). et al. 1993; Leonards-Schippers et al. 1994; Wang Perhaps the single most important consider- et al. 1994; Jung et al. 1995; Li et al. 1995b), in- ation in analysis and interpretation of QTL data sects (Nienhuis et al. 1987; Bonierbale et al. 1994) is the threshold employed for inferring that a and abiotic factors (Martin et al. 1989; Reiter et QTL is statistically significant. Because QTL map- al. 1991), and the evolution of novel organs ping involves many analyses of independent (un- (Doebley et al. 1990). This partial list illustrates linked) genetic markers throughout a genome, the breadth of topics in crop improvement in there are many opportunities for false-positive re- which QTL mapping is affording new insights. sults. Stringent significance thresholds must be In addition to medicine and agriculture, employed to avoid these. Nominal significance QTLs playing critical roles in evolution have been criteria of 99.8% or more for any single QTL are characterized. Bradshaw et al. (1995) recently usually necessary to assure an "experiment-wide" mapped QTLs controlling floral traits that deter- confidence level of 95% for all QTLs reported mine pollinator preference in two Mimulus spe- across a genome. Appropriate criteria are often cies. These species are sympatric (grow in the described in detail when an analytical approach same places) and can produce fertile hybrid prog- is developed (cf. Lander and Botstein 1989). Al- eny-but do not do so in nature, because one ternatively, methods for empirical calculation of species is strictly bumblebee pollinated, and the criteria appropriate to particular data sets have other is strictly hummingbird pollinated. A few been described (Churchill and Doerge 1994; Re- QTLs with large effects determine the floral char- bai et al. 1994, 1995). As new opportunities for acteristics (flower color, nectar volume and con- "comparative analysis" of previously published centration, and stamen and pistil length) that in- QTLs emerge (cf. Lin et al. 1995; Paterson et al. fluence pollinator preference--these mutations 1995b), it becomes ever more important that (QTLs) may represent the initial steps in repro- published QTLs satisfy statistical criteria that ductive isolation of these two species. minimize the likelihood of false-positive results. Analysis and Interpretation of QTL Genetic Basis of Quantitative Variation Mapping Experiments QTL mapping is useful for investigating specific Algorithms have been developed for QTL map- properties of individual genes contributing to ping in a wide range of pedigrees and experimen- quantitative traits. In contrast, classical quantita- tal designs, including F2, backcross, recombinant tive genetics describes the aggregate behavior of inbred, and many other designs (cf. Weller 1986; suites of genes influencing a trait. The aggregate Lander and Botstein 1989; Knapp et al. 1991; Luo descriptions of quantitative genetics are very use- and Kearsey 1991, 1992, Carbonell et al. 1992; ful for guiding manipulation of plant and animal 322 ~I GENOME RESEARCH Downloaded from genome.cshlp.org on October 5, 2021 - Published by Cold Spring Harbor Laboratory Press OIL MAPPING: PROGRESS AND PROSPECIS gene pools by breeders; however, an understand- ing of quantitative inheritance at the molecular level requires detailed descriptions of individual t li Rice33QTII I genes, and this is made possible by QTL mapping. ill The reconciliation of results from QTL map- ~(~ I I I I I I I I I I I ' ping with expectations from classical theory is ZS- B. Sorghum: 37 QTLs progressing but remains incomplete. Basic prop- erties of individual QTLs such as additivity and dominance are readily tested, and a wide range of different modes of gene-action are evident for !iii different QTLs (cf.
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