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Analysis of Natural Allelic Variation at Flowering Time Loci in the Landsberg erecta and Cape Verde Islands Ecotypes of Arabidopsis thaliana
Carlos Alonso-Blancoa, Salah El-Din El-Assala, George Couplandb, and Maarten Koornneefaa Graduate School Experimental Plant Science, Laboratory of Genetics, Wageningen Agricultural University, 6703 HA Wageningen, The Netherlands
b Department of Molecular Genetics, John Innes Centre, Norwich NR4 7UH, United Kingdom
Corresponding author: Maarten Koornneef, Laboratory of Genetics, Wageningen Agricultural University, Dreijenlaan 2, 6703 HA Wageningen, The Netherlands, maarten.koornneef{at}botgen.el.wau.nl (E-mail).
Communicating editor: V. SUNDARESAN
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We have analyzed the flowering behavior of two Arabidopsis ecotypes: the laboratory strain Landsberg erecta (Ler) and an ecotype from the tropical Cape Verde Islands (Cvi). They differ little in their flowering phenotypes and in their responses to photoperiod length changes and to vernalization treatment. However, segregating populations derived from crosses between them showed a much larger variation. An approach of quantitative trait locus (QTL) mapping in recombinant inbred lines (RILs) grown under three environments differing in day-length and/or vernalization treatment has been used to detect and locate flowering loci. Four main QTLs were identified, designated early day-length insensitive (EDI), flowering F, G, and H (FLF, FLG, and FLH, respectively), to which most of the flowering behavior differences could be attributed. To further characterize the individual loci, near isogenic lines were constructed by introgressing Cvi early alleles of EDI and FLH into the Ler genetic background. EDI-Cvi alleles produce earliness under both long- and short-day photoperiods, rendering Ler plants almost day-length neutral. In addition, RILs were selected to analyze FLF and FLG. These loci interact epistatically and RILs carrying late alleles at FLF and FLG were very responsive to vernalization and showed an increased response to photoperiod length changes. The possible role of these loci for the control of flowering is discussed in the context of the current Arabidopsis model.
TO reproduce successfully, plants must flower under favorable environmental conditions, and therefore the time of flowering is likely to have an important adaptative significance (
In addition to induced mutations, genetic variation for flowering time has been found among natural populations (ecotypes) of Arabidopsis (
The identification of natural allelic variation of smaller effect has required the combination of genetic maps with statistical methods to locate quantitative trait loci (QTLs). Flowering QTL analyses have been performed in crosses between late and early ecotypes (
The analysis of QTL by environment (QTL x E) interactions in these populations enables the detection of loci causing the G x E interactions (
In the present study we have analyzed the allelic variation affecting flowering time in two early ecotypes: the laboratory strain Landsberg erecta (Ler) and an ecotype originating from the Cape Verde Islands (Cvi). A QTL mapping approach in RILs has been used to identify and locate the loci responsible for the flowering variation in three environments differing in photoperiod length and/or vernalization treatment. The four largest effect QTLs have been further characterized genetically and physiologically in relation to the flowering responses to day-length and vernalization. For that, NILs containing Cvi early alleles in a Ler genetic background and several selected RILs carrying Cvi late alleles have been analyzed. The possible role of these loci for the control of flowering is discussed in the context of the current Arabidopsis model.
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant material:
A set of 162 recombinant inbred lines (RILs) derived from crosses between the laboratory strain Landsberg erecta (Ler) originating from Northern Europe (
Selected RILs were crossed with the following late flowering genotypes, in a predominantly Ler genetic background: (i) the FRI-M73 introgression line containing the FRI locus from the genotype M73 (
Construction of NILs:
As a first step to constructing near isogenic lines (NILs), early flowering Cvi alleles were introgressed into Ler genetic background by phenotypic selection under LD light conditions. Selection was basically performed to introgress nonrecessive Cvi alleles with relatively large effect. Three early flowering inbred lines were obtained with four backcross generations, and three final selfing generations. These lines were genotyped using 370 AFLP and CAPS markers. One line, referred to as S10, appeared to be completely Ler for chromosomes 2, 3, and 4, and contained Cvi introgressions at three genomic regions: top and bottom of chromosome 1 (genetic segments of ~25 and 20 cM, respectively), and bottom of chromosome 5 (~10 cM). This line was backcrossed to Ler and an F2 was genotyped for CAPS markers in the segregating regions. Two different F2 plants for each of the three different homozygous introgression genotypes were selected as the final NILs. These lines are designated EDI-Cvi, FLH-Cvi, and EDI-Cvi,FLH-Cvi, because they contain Cvi alleles at the loci EDI and/or FLH, respectively. Lines containing Cvi alleles at the bottom of chromosome 1 were constructed but they were removed from the analysis because no significant effect on flowering could be detected.
Growth conditions:
In experiments without vernalization treatment, seeds were sown in petri dishes on water-soaked filter paper and incubated for 3 days in a growth chamber at 24° with 16 hr light (for LD light conditions) or 8 hr light per day [for short-day (SD) light conditions]. The vernalization treatment was given as described in
RIL evaluations: The complete set of RILs, parental lines, and reciprocal F1 hybrids were evaluated for flowering under three different environmental conditions: LDs with and without vernalization treatment, and SD photoperiod conditions without vernalization. RILs were grown under both LD conditions, with and without vernalization treatment, in the same experiment and therefore the nonvernalized seeds were also sown on MS-10 medium. Twelve plants for each RIL and 24 for the parental lines and F1 hybrids, were grown per treatment in a two-block design. Blocks were divided in rows of 12 plants, and the 6 plants of each genotype per block were grown in half a row, lines being completely randomized. For the SD experiment, 12 plants per line were grown in two pots sorted in a two-block design. Lines were completely randomized within the blocks.
NIL evaluations: The early flowering near isogenic lines, parents, and F1 hybrids were evaluated under four different environments, namely LD and SD photoperiod conditions either with or without vernalization treatment. The vernalized and nonvernalized treated lines were grown together and therefore all seeds were sown on MS-10 medium. The design was basically similar to that described above for the RIL experiments, but 24 plants per genotype and treatment were grown.
Evaluations of F1 hybrids and F2 populations involving selected RILs, FRI-M73, and ld: The F1 hybrids and F2 populations involving the Ler/Cvi RILs 40, 104, and 130, the parental lines, and the introgression lines FRI-M73 and ld were grown under LD condition experiments. For the F1 hybrids, 24 plants per genotype were grown in a two-block design as described above for the RIL evaluations. This experiment was repeated and similar flowering data were collected on both occasions. Only data from the most complete experiment are presented. The six different derived F2 populations were grown together in a single LD experiment. Each population consisted of 100–120 plants. Twenty-four plants of each parental line were grown in every experiment.
Measurement of flowering:
The flowering phenotype was measured following two criteria: flowering time (FT) and total leaf number (TLN). FT was recorded as the number of days from the date of planting until the opening of the first flower. TLN was scored as the number of rosette leaves (RLN) plus the number of cauline leaves (CLN).
Statistical and QTL analyses:
To map QTLs using the RIL population, a set of 99 markers covering most of the Arabidopsis genetic map was selected from the RIL Ler/Cvi map (
For every trait and environment the contribution of each QTL to the phenotypic variance was estimated by analysis of variance components. For each analysis, the closest linked markers to the corresponding detected QTLs were used as random factors in ANOVA (the same markers used as cofactors in the MQM mapping with MapQTL). Because for all traits and environments the two markers corresponding to the QTLs located in the upper arm of chromosome 5 showed a highly significant interaction, and none of the remaining two-way interactions among the QTL markers was significant (P > 0.005), the interaction term between these two factors was included in the linear models. Thus, the contribution of this interaction was also estimated.
For FT and TLN a search for interactions between QTLs was performed using the computer program EPISTAT (
The overall G x E interaction was tested for each trait by a two-factor ANOVA using genotypes (RILs) and environments as classifying factors. For each trait and for each putative QTL, QTL x E interaction was tested by repeated measures ANOVA using the corresponding marker and the environment (repeated measurements of the RILs) as classifying factors (P < 0.005). The General Linear Model module of the statistical package SPSS version 7.5 was used for the ANOVAs and for the variance component analyses from the Type III sum of squares ANOVA.
Molecular markers:
The introgresion lines containing early flowering Cvi alleles were genotyped using AFLP marker analysis, which was performed according to
CAPS and microsatellite markers previously mapped in the Ler/Cvi RILs and/or the Ler/Col RILs (
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Flowering behavior of Ler, Cvi, and the RI lines:
The flowering phenotype of the parental ecotypes Ler and Cvi, the reciprocal F1 hybrids, and a set of 162 Ler/Cvi RILs was evaluated under three different environmental conditions: LD photoperiod, with and without vernalization treatment, and SDs (Figure 1 and Table 1). Comparison of the flowering phenotypes between the SD and LD environments provided an estimate of the response to photoperiod length, and comparison of LD conditions with and without vernalization treatment provided an estimate of the vernalization response. Both ecotypes flower at rather similar times under LD conditions and can be considered as early flowering. The later flowering time of Ler under SD indicates that Cvi responds less than Ler to photoperiod length changes. In contrast, Cvi shows a more pronounced response to the vernalization treatment. The F1 hybrids flower earlier or similar to the earliest parent (Table 1), although the FT means of the nonvernalized reciprocal F1s grown under LD conditions were significantly different (P < 0.001; which was observed consistently and was even more pronounced in two other experiments not shown). Reciprocal differences have been observed previously in crosses between other Arabidopsis ecotypes suggesting a certain influence of maternal factors on flowering (
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Although the flowering differences between Ler and Cvi are small, transgressive variation in both directions was observed in the RIL population under the three environments, indicating the presence in the two parental lines of alleles increasing and reducing flowering time (Figure 1; Table 1). A large amplification of the flowering range was observed in the RIL population when grown under SDs, and three major classes of flowering time appeared. In contrast, a reduction in the flowering range occurs when vernalizing the RILs (Figure 1; Table 1). The G x E interactions were highly significant (P < 0.001) when the flowering responses to vernalization or to photoperiod length were compared in the RIL population. This indicates the presence of allelic variation, whose effect is expressed differentially with the environments to control the different responses of the RILs to photoperiod length changes and to vernalization treatment.
The flowering phenotype was measured as FT and as TLN. As shown in Figure 2, both traits are tightly correlated in the RIL population and therefore both are expected to be mostly under the same genetic control as that observed previously with mutant genotypes (
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Mapping loci that control the flowering behavior differences between Ler, Cvi, and the RILs:
To identify and locate the loci controlling the flowering behavior differences between Ler and Cvi, the phenotypic values of the 162 RILs collected under the three environments were used for QTL analysis. Four flowering-related traits (FT, TLN, RLN and CLN) were analyzed separately for each environment (LD with and without vernalization treatment, and SD) using the MQM method of MapQTL (see MATERIALS AND METHODS). The use of cofactors strongly improved the mapping accuracy of linked QTLs, which could not be separated with interval mapping. Figure 3 shows the QTL likelihood maps obtained for TLN under the three environmental conditions, indicating the genetic intervals where the putative QTLs were mapped. A total of 11 QTLs were detected along the five linkage groups. However, a clear distinction can be made between large effect (major) and small effect (minor) loci (Table 2). Allelic variation at four loci mapping, respectively, on top of chromosome 1, and on top, middle and bottom of chromosome 5, had a large effect on both TLN and FT (15% of the phenotypic variance could be attributed in at least one environment). We have named them EDI, and FLF, FLG and FLH, respectively. Cvi alleles produce earliness at EDI and FLH and lateness at FLF and FLG, this allelic variation accounting for nearly all the RIL phenotypic variance in the three environments and for the parental phenotypes (see Figure 4 in which FLH has not been included but its effect is in agreement with the phenotypes of Ler and Cvi). The remaining seven QTLs had small additive effects (in general less than 5% of the variance could be attributed to each one) and were detected under only the LD with vernalization environment.
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The QTLs detected for FT and TLN were in most cases mapped in the same intervals, indicating pleiotropy at these loci. The four main QTLs showed comparable contributions to the phenotypic variance of both traits (Table 2). However, two small effect QTLs on chromosome 2 appeared as significantly affecting FT but not TLN (markers FD.81 and DF.140C) and two others as significant for TLN but not for FT (BF.325L and HH.171C-Col). These putative QTLs were considered either significant or not on the basis of the 2.4 LOD threshold, but the likelihood values for both traits always increased around the corresponding positions (see, for instance, chromosome 2 in Figure 3). In agreement with this, one of the small QTLs affecting FT but not TLN (DF.140C) was significant for RLN. Only the QTL located at the bottom of chromosome 4 (around DHS1) appeared to affect CLN but not RLN and FT in the LD conditions. Therefore, most of the QTLs identified affected FT and TLN, although small differences might exist in their relative effect on both traits, or in their relative contribution to RLN or CLN.
Epistasis between QTLs was analyzed by performing a genome-wide search for two-way interactions. The two major QTLs located on the top and middle of chromosome 5 (FLF and FLG) show very significant synergistic interaction for all traits and all environments (P < 0.0001; see Table 2 and Figure 4). These loci have relatively small additive effects individually (FLF shows practically no effect while FLG has small effect), and lateness in the three environmental conditions is mainly observed when both Cvi alleles are present. Interactions were also detected between these regions and markers at the bottom of chromosome 1. However, because pseudolinkage is observed in the RIL population between markers at the bottom of chromosome 1 and the top of chromosome 5 (22% recombination frequency due to the lack of RILs of one of the recombinant genotypes) these interactions were rejected as not true epistasis. Another significant epistatic interaction was detected between the QTL linked to BF.325L on chromosome 2, and the marker HH.440L on chromosome 3, which had not been associated previous to flowering.
The significant interaction of the three environments with EDI, FLF, and FLG (Table 2) indicates that these are the loci responsible for the different flowering responses in the RILs. The QTL on chromosome 1 around AD.121C also showed significant QTL x E interaction but it was due to its genetic linkage with EDI, since it was not significant when analyzing the interaction of both QTLs simultaneously. The remaining QTLs did not show significant interactions with the environments and therefore were not considered as environment specific. The overall effect of the three major loci on the flowering responses was examined. The responses of each RIL were quantified as the difference in TLN between the LD and SD conditions (photoperiod length response) and between the LD and the LD with vernalization treatment (vernalization response). Figure 4 shows the TLN frequency distributions of the RILs classified according to these three loci under the three environments. Several conclusions can be summarized as follows:
(1) EDI, FLF, and FLG are the loci controlling the differences in photoperiod length response. RILs carrying late alleles at EDI, or at FLF and FLG, not only flower later but responded more to photoperiod length than the RILs carrying early alleles at these loci. An extremely low response was shown by the genotypes EDI-Cvi,FLF-Ler,FLG-Ler, which led to the naming of this locus as early, day-lenth insensitive (EDI). Therefore, to "abolish" the photoperiod response in the Ler/Cvi RILs required early alleles at the three loci.
(2) FLF and FLG are the main loci controlling the differences in vernalization response. The FLF and FLG effects are much smaller under vernalization conditions than in normal LDs. In other words, the lateness observed under LDs in RILs carrying FLF-Cvi,FLG-Cvi alleles, is very much diminished by a 3-wk vernalization treatment. It is expected that a longer vernalization treatment would have reduced even more the effect of these loci, since saturation of the vernalization response in late-flowering responsive genotypes requires longer treatments (
Characterization of Cvi early alleles: the loci EDI and FLH:
Near isogenic lines containing Cvi alleles at EDI, and/or FLH in a Ler genetic background were constructed by phenotypic and genotypic selection (see Figure 5 and MATERIAL AND METHODS). The introgression line containing Cvi alleles only in the EDI region was used for further genetic mapping, analyzing an F2 population under SD conditions where the flowering segregation could be classified qualitatively and behaved as monogenic. The location of EDI was narrowed to a segment smaller than 10 cM comparable to the 2 LOD support interval established in the QTL analysis (data not shown). The genetic length of the introgression segment in the monogenic FLH-Cvi NIL (10 cM approximately) confirmed the FLH position obtained in the MQM analysis of the RILs.
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The NILs and the line S10, from which they were derived, were analyzed under LD and SD photoperiod conditions, with and without vernalization treatment (Figure 5). The Cvi allele of EDI was largely dominant, which was particularly manifest under SD conditions where Ler plants flowered on average with 18.9 more leaves than the EDI-Cvi plants. EDI-Cvi plants flowered with almost the same TLN under both photoperiod length conditions, thus behaving as an almost day-length neutral genotype. These plants responded little to vernalization, showing a comparable response to Ler. At the FLH locus, the slight earliness produced by the Cvi allele behaved on average codominantly. However, its effect was almost absent under LD conditions without vernalization, differing from the effect estimate obtained in the RIL population. This suggests FLH might be involved in some undetected epistatic interaction, or that some introgressed fragment not detected in the extensively genotyped lines affected flowering time. In contrast, under SDs, FLH-Cvi plants flower on average with 3.4 fewer leaves than Ler plants, an effect not detected in the QTL analysis. These plants responded to photoperiod length in a comparable way to Ler. However, it is remarkable that they responded more than Ler to vernalization, an effect that was mainly observed under SD conditions. The allelic effects at EDI and FLH were basically additive because plants of the EDI-Cvi,FLH-Cvi line flowered earlier than the monogenic introgression lines in all environments.
Characterization of Cvi late alleles: the loci FLF and FLG:
Three RILs were selected on the basis of their genotype as being Ler at EDI and FLH (and as much as possible in the rest of the genome), but carrying Cvi alleles at FLF and/or FLG. RIL 130 was selected as genotype FLF-Cvi,FLG-Cvi, RIL 104 as FLF-Cvi,FLG-Ler, and RIL 40 as FLF-Ler,FLG-Cvi (the chromosome 5 regions of RILs 40 and 104 are not overlapping). To confirm the presence of two linked flowering loci we performed a reconstruction experiment, under LD conditions, to obtain the expected late flowering genotype when the homozygotes FLF-Cvi and FLG-Cvi are combined. For that, an F1 hybrid between the genotypes FLF-Cvi (RIL 104) and FLG-Cvi (RIL 40) (heterozygote in repulsion for both loci) was crossed with the line FLF-Cvi,FLG-Cvi (RIL 130) (Figure 6). This population was partially genotyped for the microsatellite markers nga158 and nga139, closely linked to the support intervals established, respectively, for FLF and FLG in the QTL analyses (Figure 3). Indeed, 10 out of the 13 latest plants of this population originated from recombinant gametes between both markers, thus confirming the presence of two flowering linked loci at a genetic distance of at least 15 cM. The flowering phenotypes of the different genotypic classes of this population and of the F1 hybrids between these RILs and Ler (Figure 6 and Figure 7), indicate that late Cvi alleles at both FLF and FLG behave additively (codominantly); i.e., their allelic effects are dosage dependent.
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Another locus, FLC, at which natural allelic variation has been reported previously, maps in the region of FLF (
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(1) FLG-Cvi behaves additively with ld to produce lateness and shows a weak synergistic interaction with FRI-M73. The phenotypes of the corresponding F1 hybrids and F2 populations were in agreement, confirming that both FLG-Cvi and FRI-M73 are partly dominant and ld is recessive.
(2) FLF-Cvi behaves as a late allele of FLC in its synergistic interaction with FRI-M73, and with ld, although it must be a weaker allele than FLC-Sf2 or FLC-Col when compared with TLNs reported previously (
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In this article we have analyzed the flowering behavior of two early Arabidopsis ecotypes: the laboratory strain Ler originating from Northern Europe (
Late alleles at two of the major loci identified in the Ler/Cvi population, FLF and FLG, interact synergistically. A similar type of interaction has been previously shown to occur between natural late alleles at FRI and FLC (
The Cvi ecotype shows a slightly reduced response to photoperiod length changes and a more pronounced vernalization response than the Ler ecotype. The three major loci, EDI, FLF, and FLG, control most of the response differences to photoperiod and vernalization, as shown by their strong QTL x E interactions. Early alleles at these loci not only reduced flowering time but also diminished the response to photoperiod length. In fact, as shown with the near isogenic line EDI-Cvi in Ler genetic background, the combination of EDI-Cvi alleles with FLF-Ler,FLG-Ler is able to render Arabidopsis practically day-length neutral in its flowering behavior. On the other hand, FLF,FLG accounted for much of the vernalization response, the late-flowering effect of Cvi alleles being eliminated by a 3-wk vernalization treatment. In agreement with these results, the Cvi ecotype flowered at almost similar times under LD and SD conditions when vernalized; i.e., Cvi eventually behaved as almost day-length neutral when the effect of FLF-Cvi,FLG-Cvi was physiologically removed by the vernalization treatment. In other Arabidopsis populations where QTL x E interactions have been analyzed, the largest effect QTLs also showed significant interaction (
Many of the Arabidopsis flowering loci have been characterized genetically and physiologically in relation to the vernalization and photoperiod responses and a model for the control of the transition from the vegetative to the reproductive phase is being developed (reviewed in
Late alleles at the FLF and FLG loci are very responsive to vernalization and confer a more pronounced response to photoperiod length, as seen from the behavior of the EDI-Ler,FLF-Cvi,FLG-Cvi RILs, features also shared with the late alleles at FRI and FLC (
Considering together the behavior of the three loci EDI, FLF, and FLG, it is worth noting that RILs EDI-Cvi,FLF-Cvi,FLG-Cvi respond to photoperiod length, in contrast to the EDI-Cvi NILs. Under the discussed model, in such genotypes the photoperiod pathway would be promoting flowering at the same level in both day-lengths. This photoperiod response would therefore imply that under SDs there is also an inhibition (or lack of promotion) of the autonomous flowering pathway, which would operate through FLF,FLG. In agreement with this, similar genetic behavior has been observed in double mutants between nonresponsive and responsive loci, which show mostly an intermediate, additive, day-length response (
The allelic variation at the FLH locus has a rather mild effect on flowering, Cvi alleles responding like Ler to day-length changes. The additive behavior of EDI and FLH together with the more pronounced response of FLH-Cvi alleles to a vernalization treatment, suggest that FLH might be involved in the autonomous flowering promotion pathway. However, opposite to FLF,FLG and to other vernalization responsive loci, at FLH it is the early allele which increases the response; i.e., FLH-Cvi early alleles make Ler more vernalization responsive. This might suggest its role in the control of the vernalization response.
Figure 9 shows a scheme of the current general model for the control of flowering initiation (
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, promotive effect; 
, inhibitory effect.
We have shown that the Ler/Cvi allelic variation probably concerns loci involved in different flowering pathways. Comparison of map positions between identified QTLs and mutant loci might suggest putative candidate genes at which this natural variation occurs. Nevertheless, cautions must be taken given the inaccuracy of the QTL mapping and the large number of known mutant loci affecting flowering behavior, which appeared scattered over the five linkage groups (
It is expected that part of the natural variation will correspond to alleles of mutant flowering genes. Nevertheless, it is evident that the spectrum of natural genetic variation will be different from the spectrum obtained by artificial mutational analyses, partly due to the limitations of the small number of ecotypes used to generate mutants. Some alleles might not be functional in some ecotypes, as is likely to be the case for FRI alleles in many early ecotypes (
| ACKNOWLEDGMENTS |
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We thank Prof. A. R. KRANZ for sending the original Cvi seeds, and Dr. J. W. VAN OOIJEN for providing MapQTL and his helpful assistance in the QTL mapping. The flowering work in the laboratories of M.K and G.C. is supported by the European Union (E.U.) project BIO4-CT97-2340. C.A.-B. was supported by the Biotechnology TDR program of the E.U. (BIO4-CT96-5008) and S.E. by a grant from the government of Egypt.
Manuscript received February 4, 1998; Accepted for publication March 20, 1998.
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