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To Clone Or Not to Clone Plant Qtls: Present and Future Challenges

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To Clone Or Not to Clone Plant Qtls: Present and Future Challenges Review TRENDS in Plant Science Vol.10 No.6 June 2005 To clone or not to clone plant QTLs: present and future challenges Silvio Salvi and Roberto Tuberosa Department of Agroenvironmental Science and Technology, University of Bologna, Viale Fanin, 44, 40127 Bologna, Italy Recent technical advancements and refinement of studies completed to date indicate an L-shaped distri- analytical methods have enabled the loci (quantitative bution of QTL effects (i.e. most QTLs have a small effect trait loci, QTLs) responsible for the genetic control of and only a few show a strong effect) [5], thus enabling quantitative traits to be dissected molecularly. To date, the identification of QTLs with a major effect on the most plant QTLs have been cloned using a positional phenotype. cloning approach following identification in experi- Currently, QTL mapping is a standard procedure in mental crosses. In some cases, an association between quantitative genetics [6]. QTL mapping usually begins sequence variation at a candidate gene and a phenotype with the collection of genotypic (based on molecular has been established by analysing existing genetic markers) and phenotypic data from a segregating popu- accessions. These strategies can be refined using lation, followed by statistical analysis to reveal all possible appropriate genetic materials and the latest develop- marker loci where allelic variation correlates with the ments in genomics platforms. We foresee that although phenotype. Because this procedure only allows for an QTL analysis and cloning addressing naturally occurring approximate mapping of the QTL, it is usually referred to genetic variation should shed light on mechanisms of as primary (or coarse) QTL mapping. Procedures and plant adaptation, a greater emphasis on approaches strategies for primary QTL mapping are well established relying on mutagenesis and candidate gene validation is [7] and will not be considered here. likely to accelerate the pace of discovering the genes More recent technical progress in the area of molecular underlying QTLs. biology and genomics have made the cloning of QTLs [i.e. the identification of the DNA sequences (coding or non-coding) responsible for QTLs] possible. Here, we present a critical appraisal of the results obtained in this From polygenes to QTL cloning field in plants and discuss the perspectives, with emphasis Classical quantitative geneticists defined ‘polygenes’ [1] as on several major limitations and promising novel the many hypothetical genes, with an equally small effect, approaches. A literature survey shows that although involved in determining a quantitative trait (i.e. a trait w150 research papers reporting original QTL data are influenced by both multiple genetic and environmental published yearly (average of 2000–2004, considering factors). Polygenes have been integrated into most Arabidopsis, soybean, rice, sorghum, maize, barley and quantitative genetics models; in many cases, these models wheat), only a handful of studies have reported the successfully describe complex phenomena such as the cloning of QTLs (Table 1). Besides plants, QTL cloning inheritance of quantitative traits, the effect of selection, is rapidly advancing in humans and livestock [8,9] as well the consequence of mating behaviour and others. How- as in model species such as yeast, Drosophila, mouse and ever, within such models polygenes are usually dealt with rat [10–12]. as a whole, whereas the actual genes remain in what has been defined as a ‘statistical fog’ [2]. Within this frame- work, the problem of understanding the molecular nature Positional cloning of QTLs of quantitative trait variation would have remained Among the handful of QTLs isolated in plants to date, the unsolved. majority have been cloned via positional cloning. Posi- The first steps toward resolving this puzzle were based tional cloning requires several steps (Figure 1) to enable on studies carried out during the first half of the 20th us to assign a QTL to the shortest possible genetic interval century; these showed that genes with a major effect on (QTL fine genetic mapping) and to identify the corre- quantitative traits do exist and can be experimentally sponding interval on the DNA sequence (QTL physical mapped on chromosomes by evaluating the correlation mapping) where candidate genes are selected for evalu- between the quantitative trait value and the allelic states ation. The increase in mapping resolution required by at linked genetic markers [3,4]. This led to the definition of QTL positional cloning is substantial because after a quantitative trait locus (QTL) as a genetic locus where primary mapping a QTL is positioned within a chromo- functionally different alleles segregate and cause signifi- some interval of w10–30 cM, which usually includes cant effects on a quantitative trait. The findings of QTL several hundred genes (Box 1). Eventually, independent Corresponding author: Tuberosa, R. ([email protected]). proof is required to validate the role of the identified allelic Available online 10 May 2005 polymorphism on the observed phenotypic effect. www.sciencedirect.com 1360-1385/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2005.04.008 www.sciencedirect.com Table 1. Summary of the main characteristics of the QTLs cloned in plants 298 Species Trait QTL Gene Function Molecular Candidate R 2 (%)b Plants Resolution ORF Identification Functional proof Refs identification genea (no.)c (kb)d (no.)e of QTN Arabidopsis Flowering time ED1 CRY2 Crypt. Pos. cloning Yes (L) 28–56 1822 45 15 Amino acid Transformation [71] substitution FLW FLM TF Pos. cloning Yes (E) 27 NA 138 38 Deletion of Transformation [31] whole gene Gluc. structure GS-elong MAM MAM synthase Pos. cloning Yes (E) NA 4600 NA NA Nucleotide and No [82] gene indels Root morphology BRX BRX TF Pos. cloning No 80 860 45 10 Premature stop Transformation [83] Review codon Maize Plant architecture Tb1 Tb1 TF Transp. tagging Yes (E) 17–31 NA NA NA No, possibly Complementation [33,42] regulatory Rice Heading time Hd1 Se1 TF Pos. cloning Yes (L) 67 1505 12 2 No Transformation [84] Heading time Hd3a Hd3a Unknown Pos. cloning Yes (L) NA 2207 20 4 No Transformation [23] Heading time Hd6 aCK2 Protein kinase Pos. cloning No NA 2807 26 1 Premature stop Transformation [30] codon Heading time Ehd1 Ehd1 B-type response Pos. cloning No NA O2500 16 3 Amino acid Transformation [85] regulator substitution Tomato Fruit sugar content Brix9-2-5 Lin5 Invertase Pos. cloning Yes (L) NA 7000 0.5 1 Amino acid Complementation [86,87] substitution Fruit shape Ovate Ovate Unknown Pos. cloning No 48–67 3000 55 8 Premature stop Transformation [88] codon TRENDS in Plant Science Fruit weight fw2.2 ORFX Unknown Pos. cloning No 30 3472 92 4 Unknown Transformation [58,89] regulatory variant Abbreviation: crypt., cryptochrome; gluc. structure, glucosinolate structure; MAM synthase, methylthioalkylmalate synthase; NA, not applicable or not available; ORF, open reading frame; pos. cloning, positional cloning; QTL, quantitative trait locus; QTN, quantitative trait nucleotide; TF, transcription factor; transp. tagging; transposon tagging. aEvidence for candidate gene: (E) indicates early evidence, after primary QTL analysis; (L) indicates late evidence, after physical mapping and/or sequencing. bProportion of phenotypic variance explained by the QTL in the primary cross. cDimension of the population used for fine mapping. dDNA physical interval completely linked with the QTL. eNumber of ORFs completely linked with the QTL. Vol.10 No.6 June 2005 intercrossing standard biparental populations increase in geneticgenetic resolution resolution (many rounds can ofof meiosis). also A detection substantial be (segregationshould obtained increase is the efficiency of QTL by expected mapping both in at terms followed by many several loci) cyclescapturing and of much intermating. of Thisated the approach by genetic crossing variationcrossed a populations carefully of chosen the setpartially species, overcome of through the parental use of lines other multiparental inter- populations.the This many imp morechosen, QTLs the segregating collections will for onlylines: segregate the for no same a fraction trait mattergenetic of in variability how as a carefullycollections result of the of using IL parentalconsidered only or are two lines the ABQA parental time are and lines,against effort required as extreme for developing well phenotypes elite as line the coupled with limited chromosome some segments level of from phenotypicanalysis a selection (ABQA) wild method, accessioncan which also within be combines an producedthree backcrossing using tomato the QTLs. advanced[15] NILs backcross suitable QTL forfor positional any cloning segregating QTL. Remarkably, the different same tomato IL IL lines, therefore, potentiallygenome a QTL-NIL should exists introgressed be from completely a donor) the represented exception amongeach of the line a is isogenicintrogression single to libraries (ILs) a short (i.e. background collectionsregion. parental of chromosome QTL-NILs lines line, can where segment with alsoand be selfing efficiently identified individuals within thatparental are genetic heterozygous backgrounds or at (ii) the iteratively(i.e. QTL identifying substitution) ofproduced by one (i) QTLprimary marker-assisted backcross allele mapping introgression into was one carried ormarkers out, can both be QTL-NILs estimated moredistances can precisely. between be conditions, a the QTL is QTL considered Mendelized
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