Comparative Analysis of QTLs Affecting Plant Height and ... · Poaceae, more frequently than would be expected by chance. Possible homoeologous QTLs were found within both the maize

Copyright 0 1995 by the Genetics Society of America

Comparative Analysis of QTLs Affecting Plant Height and Maturity Across the Poaceae, in Reference to an Interspecific Sorghum Population

Yann-Rong Lin,* Keith F. %hertzt and Andrew H. Patemon”

*Department of Soil and Crop Sciences, Texas A&M University and tUSDA-ARS, College Station, Texas 77843-2474

Manuscript received March 30, 1995 Accepted for publication June 16, 1995

ABSTRACT Correspondence among QTLs affecting height and/or flowering was investigated across the five races

of sorghum, an interspecific sorghum F2 population, and 32 previously published sorghum, maize, rice, wheat, and barley populations revealing 185 QTLs or discrete mutants. Among nine QTLs mapped in the interspecific sorghum population (six affecting height and three affecting flowering), at least seven (78%) are associated with “conversion,” backcross-introgression of alleles imparting reduced height or earlier flowering from cultivated sorghums into one or more exotic Sorghum bicolor races. One chromosomal region was “converted” in all S. bicolmraces-in the interspecific F p , this region explained 54.8% of height variation (putatively the Dw2 gene) and 85.7% of flowering time variation (putatively Mal). Comparative data suggest that Mal and Dw2 orthologs influence height and flowering of other Poaceae taxa and support classical dogma that the sorghum phenotypes attributed to Mal and Dw2 (respectively) are due to different genetic loci. Other sorghum QTLs also showed correspondence with those in other Poaceae, more frequently than would be expected by chance. Possible homoeologous QTLs were found within both the maize and sorghum genomes. Comparative QTL mapping provides a means to unify, and thereby simplify, molecular analysis of complex phenotypes.

T HE relationship between height and flowering time is particularly important in the grass family, Poaceae,

in which apical growth is terminated by flowering. Domes tication and breeding of the Poaceae, largely of tropical origin, has involved selection for reduced height and day- neutral flowering. In natural populations, tall stature affords a competitive advantage for light and increases the effectiveness of seed dispersal (HARPER 1977). However, in agriculture, reduced height is necessary for machine harvest and to avoid wind or other hazards. In most crops, series of height mutations, e.g., Rhtl-RhtlO in wheat (cf: GALE 1985) and d ld9 in maize (CJ: COE and NEUFFER 1993), have been preserved or induced and play a prominent role in breeding. Moreover, because most wild (trop ical) Poaceae flower under short days, photoperiod-insensitive (day-neutral) mutations have been selected to adapt them to temperate agriculture, e.g., m a l in sorghum (QUINBY and KARPER 1945) and se-1, se-2, and se-3 in rice (KINOSHITA and TAKAHASHI 1991).

In sorghum [Sorghum bicolor (L.) Moench.], classical results suggest that height and flowering are each largely controlled by four genetic loci (DwI-4 and Mal- 4, respectively) with residual variation in each trait, sug- gesting additional genes of smaller effect (QUINBY and KARPER 1945, 1954). One flowering gene, Mal , is specifically regulated by photoperiod, while all are influenced to some extent by temperature (QUINBY and KARPER 1945).

Corresponding authm: Andrew H. Paterson, Department of Soil and Crop Sciences, Texas A&M University, College Station, TX 77843-2474.

Genetics 141: 391 -41 1 (September, 1995)

As is true of most crops, improvement of sorghum grown in the United States relies heavily on genetic variation found in exotic germplasm. Because most exotic sorghum is tall, and flowers only under short daylength, a “sorghum conversion program” was inau- gurated in the 1960s, using backcrossing plus selection to reduce height and adjust flowering of exotic sorghums to be suitable for temperate breeding programs ($ STEPHENS et al. 1967; ROSENOW and CLARK 1987). “Conversion” takes a minimum of 12 generations, and 4 yr (STEPHENS et al. 1967). Such programs are also utilized in maize (SALAMINI 1985; HOLLEY and GOOD- MAN 1988), cotton (MCCARTY and JENKINS 1992), and other temperate cultigens of tropical origin. A “converted” sorghum is a homozygous genotype putatively comprised of 96% recurrent (exotic-tropical) parent genome, thus most remaining “donor” (temperate) chromatin is likely to contain alleles for reduced height and long-day (photoperiod-insensitive) flowering; these alleles have been introgressed from the temperate donor.

Extensive conservation in gene repertoire and order across the Poaceae (6 HULBERT et al. 1990; WHITKUS et al. 1992; &IN and TANKSLEY 1993; A H N et al. 1993; BENNETZEN and FREELING 1993; HELENTJARIS 1993; SHIELDS 1993; KURATA et al. 1994) affords the opportu- nity to study correspondence of QTLs affecting common phenotypes in reproductively isolated taxa. We used a highly polymorphic cross between temperate and tropical Sorghum species, S. bicolor X S. p-opinquum (Kunth.) Hitchc., to investigate correspondence of height and flowering loci across the Poaceae. The high

392 Y.-R. Lin, K. F. Schertz and A. H. Paterson

TABLE 1

Genetic stocks of nine exotic sorghum accessions and their converted derivatives

Race (abbreviation) Exotic accessionb Working group‘ Origin Percentage conversiond

bicolor (Bl) IS12526 Subglabrescens Ethiopia 9.4 caudatum (Cl) IS2801 Caudatum Sudan 21.1 caudatum (C2) IS12661 Zera-Zera Ethiopia 4.3 caudatum (C3) IS3071 Dobbs Sudan 4.8 durra (Dl) IS12553 Durra Ethiopia 8.3 durra (D2) IS1121 Nandyal India 10.0 guinea (Gl) IS7419 Conspicuum Nigeria 14.3 guinea-caudatum (G2) IS7254 Caudatum-Guinea Nigeria 13.0 kafir-caudatum IK1) IS2508 Caudatum-Kafir Sudan 11.5

“According to HARLAN and DE WET (1972). In all cases, the “converted” stock is designated simply by a suffix “C”. According to MURTY et al. (1967).

dRefers to percentage of loci that detect polymorphism between indicated race and BTx406, and also show conversion (introgression).

level of polymorphism between S. bicolor and S. popinquum afforded segregation for phenotypically significant variants at many genetic loci. Moreover, allelic variants at DNA marker loci revealed by heterologous probes facilitated integration of the sorghum map with those of maize and other Poaceae. Specifically, we sought to map QTLs affecting height and flowering time in a cross between temperate and tropical sorghums, determine if these QTLs account for variation in height and flowering across “conversion lines” representing the five races of s. bicolor, evaluate the correspondence of genes influencing height and flowering in sorghum, maize, rice, wheat, and barley, and reexam- ine the relationship between height and flowering, in sorghum and other Poaceae.

MATERIALS AND METHODS

Measurement of phenotypes: A total of 370 F2 progeny of S. bicolor X S. popinquum were grown near College Station in summer 1992. Seedlings were hand-transplanted to the field on 30 April 1992, 2 weeks after planting, at spacing of 100 cm between plants and 200 cm between rows, but otherwise grown under standard agricultural conditions. Plant height was measured from the base of the plant to the tip of the inflorescence for main culm and both tallest and shortest flowering tillers for each individual. Days to flowering (pollen shed) was recorded for the main culm and (up to) the first four flowering tillers. RFLP analysis A total of 71 DNA probes linked at distances

of 5 2 0 cM to 91% of the sorghum genome map (CHITTENDEN et al. 1994) were applied to the interspecific F2 population, and the exotic/converted sorghum pairs. Additional RFLPs were subsequently used for further characterization of exotic and converted sorghums. Heterologous probes diagnostic of height and flowering genes in other species (see Tables 3 and 4) were mapped in 56 interspecific F2 progenies previously described (CHITTENDEN et al. 1994), and corresponding locations on the 370 F2 progeny studied herein were inferred (Figure 4). The prefixes of DNA markers are; pSB: sorghum PstIgenomic DNA bnl and umc: maize PstZgenomic DNA or cDNA, and csu: maize cDNA kindly provided by (alphabeti- cally) E. COE and J. GARDINER, University of Missouri; rz: rice

cDNA probes; rg: rice genomic DNA; cdo: oat cDNA kindly provided by S. R. MCCOUCH, M. SORRELLS, and S. D. TANK- S L N , Cornell University. DNA extraction, restriction enzyme digestion, blotting, probe hybridization, and autoradiogra- phy, were as described previously (CHITTENDEN et al. 1994).

Data analysis and interpretation: Trait means and standard deviations were calculated using Microsoft Excel (Microsoft, Tacoma, WA). Phenotypic correlations were calculated using the SAS Proc CORR function (SAS Institute 1990).

Linkage mapping used MAPMAKER version 2.0 (LANDER et al. 1987) for the Macintosh, and the Kosambi mapping function (KOSAMBI 1944). QTL analysis used MAPMAKER- QTL version 0.9, and a significance threshold of LOD 2.5, as suitable (LANDER and BOTSTEIN 1989) for a map of the marker density and length observed.

For both plant height and flowering time, pronounced bimodal distributions suggested that a gene with a very large effect was segregating in the population. The phenotypic variation attributable to such a gene would be likely to obscure QTLs with smaller effects (LANDER and BOTSTEIN 1989). We took two approaches to seeking such QTLs of smaller effect with similar results. Each approach seeks to “eliminate” the phenotypic effect of the “major gene” from the “residual” (error) term in analysis of the significance of other QTLs. Because the location of the major gene was readily determined, nearby DNA markers could be used to accurately assess genotype at this locus. Similar approaches to this problem have recently been published independently (JANSEN and STAM 1994; ZENC 1994). Specifically, we considered:

1. Adjustment of the phenotypic value of individual plants for the major gene effects. Using the maximum likelihood phenotypic effect (determined by MAPMAKER-QTL) associated with each of the three genotypes at the RFLP marker nearest the “major gene,” the phenotype of an individual was “adjusted” by subtracting the effect attributable to this locus. For example, if an individual is heterozygous at the nearest RFLP marker, the adjusted phenotypic data would be the original phenotypic data minus “ a + d” (the additive effect of one allele substitution, plus the dominance deviation expected for that heterozygote). If the individual is homozygous for the S. popinquum allele, the adjustment would be to subtract twice the additive effect ( 2 4 . After adjustment for the LG D locus, the F2 data for both height and maturity exhibited a normal distribution, and only small residual effects on height and maturity remained (LOD 47.39 to LOD 1.65, and LOD 90.94 to LOD 0.24, respectively).

Correspondence Among Poaceae QTLs 393

23 kb - 9kb - 6kb - 4kb -

2.2 kb - 2.0 kb -

“-

No polymorphism

1

Polymorphism, no conversion

(e.g., Locus is not associated with “conversion” of wild-type height or flowering alleles.)

n “MAKER-OTL: the 2. Use of the “fix OTL” alnorithm l i largest LOD forlheight Cnd maturity was “fixed” ~MDER and BOTSTEIN 1989) to eliminate the effects of the major gene (LG D) and the genome was rescanned to seek QTLs with smaller effects.

Such approaches incur a risk that a fraction of the “residual” (error) variance will be removed from the experimental model, due to chance correlation with the “fixed” parameters, artificially reducing the remaining “error” term, and increasing the likelihood of false positives. However, we present independent results from analysis of exotic and converted sorghums that corroborate inferences based on data “adjusted” for effects of major genes.

Identification of introgressed segments in sorghum conversion lines: Nine exotic accessions of S. bicolorand their corresponding “converted” derivatives (as described in introduction, and provided by D. T. ROSENOW, Lubbock, TX), representing each of the five races of S. bicolor (as per HARLAN and DE WET 1976; see Table l), were chosen based on visual observation that the exotic and converted strains were cor- rectly identified. Two individuals from each exotic strain, and each “converted” derivative, were examined with the probes used for QTL mapping, to provide a representative set of loci across the genome. Pilot studies had shown relatively little heterogeneity within the exotic and converted strains, and rarely did the two plants from an exotic strain or its converted derivative show different alleles. “Conversion” (introgression of an allele from the donor) was inferred when both represen- tatives of the converted line differed from both representa- tives of the recurrent (exotic) parent by an allele found in the donor parent (Figure 1).

Correspondence between QTLs in different taxa: The hy- pergeometric probability distribution (sampling without re- placement) ($ LARSEN and MARX 1985) affords formal evaluation of correspondence between QTLs (J. TAYLOR, personal communication). The average genomic interval over which we judged that correspondence between QTLs could be as- sessed was -30 cM, and present data afforded comparisons across ca. 75% (1500 cM) of the ca. 2000 cM genomes of maize, rice, and sorghum-consequently n (the number of intervals that could be compared) was estimated at 50 (1500/ 30). A match was declared between two taxa when corresponding intervals harbored QTLs in each. For fixed n, the probability p that m “matches” between QTLs from two taxa would occur by chance is determined jointly by the larger ( I )

Conversion

(e.g., Locus may be associated with “conversion” of wild-type

height or flowering alleles.)

FIGURE 1.-Strategy for identi- fylng “conversion” of a genomic region in an exotic sorghum genotype. (a) The exotic line and its converted derivative are identical to the donor parent-thus it cannot be discerned whether conversion of the genomic region of interest has occurred or not. (b) The exotic line is different from the donor parent, but the “converted” versions of this exotic line are the same as the exotic parent- thus this genomic region is not converted. (c) The exotic parent is different from the donor parent, and the converted line is the same as the donor parent-thus this genomic region is “converted.”

and smaller (s) number of QTLs found in the taxa, respectively, according to the equation:

(l)(r-3 p = (3

RESULTS

QTL analysis of plant height and flowering time in sorghum

Segregation and recombination: The linkage map of the 370 F2 individuals (Figure 4), comprised 78 loci covering 91% of the previous linkage map and an estimated 85% of the sorghum genome ( CHITTENDEN et al. 1994). The map included 11 linkage groups spanning 935 cM, with an average distance between markers of 14 cM. Both segregation and recombination were similar to data previously reported for 56 individuals from the same F2 population (CHITTENDEN et al. 1994)- except that herein we could not discern linkage between pSB419a and pSB395a on LG E (CHITTENDEN et al. 1994), accounting for the extra linkage group. These 370 individuals also afforded sufficient map resolution to discern between alternate locus orders that could not be ruled out previously, on linkage groups (LGs) A, B, D, F, H, and I.

Mapping QTLs affecting height of interspecific sorghum progenies: The average height of the main culm, tallest, and shortest flowering tillers for S. bicolm cv. “BTx623” was 109 ? 6 cm (mean -+ SE), for S. p-opinquum was 396 -+ 40 cm, and for the F2 population was 290 2 99 cm. The phenotypic distribution of F2 progeny was bimodal (Figure 2).

A total of six QTLs collectively accounted for 71.0%


35 + S propinqulrm

x = 396.0 (540.3) F? population -

Plant Height (cm)

FIGURE 2.-Frequency distribution for plant height in sorghum. The F2 population exhibits a bimodal distribution, due to unequal gene effects (see text). The numbers in parentheses represent the standard deviations for parents and F2 population.

of phenotypic variation in height (Table 2). Based on the average height s f the main culm, tallest and shortest tillers (unadjusted for the major gene), three QTLs were detected on LGs D, G (HtAvgGI), and J. The QTL on LG D explained 54.8% of phenotypic variation, with additive effect of 87.9 cm and dominance deviation of 63.9 cm. After adjustment to reduce the influence of this “major gene” (see MATERIALS AND METHODS), additional QTLs were detected on LGs A and C . Finally, a sixth QTL (on LG G: HtMG2) was significant (LOD = 2.68) based on the height of the main culm (Table 2, Figure 4), although marginally below significance (LOD = 2.30) based on average height of the main culm, tallest, and shortest tillers. Two different LOD

peaks occurred on LG G, separated by ca. 60 cM, and with a drop of more than LOD 2 (100-fold) between the peaks. Analysis of each QTL with the other “fixed” (see above) indicated independence (as per PATERSON et al. 1988, 1991).

For five of the six (83%) height QTLs, the S. propinguum alleles exerted a positive additive effect (ie., increased height). Among these five, four (HtAvgAl, HtAvgCI, HLAvgDI, HtAvgJI) showed dominance or overdominance for increased height and one ( H t A v f i I ) was clearly additive. One QTL, HtMG2, was clearly overdominant ( d > a = 0 ) , with the heterozygote taller than either parent.

Mapping QTLs affecting maturity in sorghum: The

TABLE 2

Biometrical parameters of individual QTLs affecting flowering time or plant height in the interspecific FP, S. bicolor X S. propinguum

LOCUS“ LOD Percentage Var a d d/n Mode

4.67 90.94

2..53

3.30 3.34

47.39 4.27 2.68

13.77

8.3 85.7

4.2

6.3 5.1

54.8 6.7 7.2

23. 1

6.7 40.3 10.5

11.4 22.6 87.9 35.3 -3.1 31.5

-10.8 29.1 .5.0

32.6 27.9 63.9

1.4 58.1 53.9

- 1.61 0.72 0.48

2.85 1.24 0.73 0.04

- 18.74 1.71

R D DA

D DA D A RDA D

” FlrAvg, the average flowering day to anthesis of the main culm plus the first four tillers; FlrFst, the flowering day of the first flowering tiller; HtAvg, the average plant height of the main culm, tallest, and shortest tillers; HtM, the plant height of the main culm. Individual QTI, loci are named by thc trait abbreviation and linkage group (A-J). Mode indicates the gene action of individual QTLs, A, additive; D, dominant; R, recessive (PATERSON p t nl. 1991) .


50

45

40

2 35

3 3

g 30

2 25

c L .-

z 20

15

10

5

0

(hr) ( O )

14.5 - 40

I4.O ” 35

13.5 ” 30

13.0 ” 25

12.5 ” 20

12.0

11.5 ” 15

11.0 ” IO

10.5 -- 5

-

FIGURE 3.-Frequency distribution for flowering time in the F2 population of S. bicolor X S. propinquum. The numbers in parentheses represent the standard deviations for parents and F2 population. Daylength (at M a y intervals indicated by XXX)

and temperature (averages calculated during M a y intervals: low temperature indicated by - - - and high temperature indicated by -), are also shown. The distribution is bimodal, and approximately twice as many individuals are late-flowering as early- flowering. The genotype at pSB428u, the marker nearest to the likelihood peak for the photoperiodic flowering QTL, is shown for plants flowering in each 5day interval. B, homozygote for S. bicolor alleie; H, heterozygote: P, homozygote for 5. propinquum allele.

average number of days from planting to flowering of the main culm and (up to) the first five tillers for the S. hicolw parent was 115.5 5 7.8, for S. propinquum was 189 ? 1.9, and for the F2 population was 149.7 2 37.7. Because 12 F2 progeny had not yet flowered by frost (28 November 1992, 233 days), and were deemed “missing data”, the data were slightly conservative (biased in fa- vor of early flowering). The phenotypic distribution of F2 progeny was bimodal (Figure 3).

Three QTL5 collectively accounted for 86.7% of the phenotypic variation in average days to flowering. Based on analysis of original (unadjusted) average flowering of the main culm and (up to) the first four tillers, only one QTL was detected (on LC D). This QTL, FlrAvgDl, alone could explain 85.7% of phenotypic variance, with additive effect of 40.3 days and dominance deviation of 29.1 days. After phenotypic adjustment or “fix QTL”, a second QTL (klrAvgB1) was detected on LC B. A third QTL on LG G, HrFstGl, was significant (LOD = 2.53) based on the date of the first flower (Table 2, Figure 4; the LOD for average flowering date of five tillers was 2.31).

For all three flowering QTLs, the S. popinquum alleles exerted a positive additive effect (ie., late flowering). The S. popinquum alleles of RrAvgDl and FlrFstCl were dominant, and of FlrAvgBl was recessive (Table 2).

Correspondence between sorghum QTLs affecting

height and flowering: The phenotypic correlation between height and flowering was highly significant ( r = 0.79). Two of the three QTLs affecting flowering time were associated with height QTLs. Specifically, the QTLs, FlrAvgDl and HtAvgDl, mapped within overlap ping 90% confidence intervals on LC D, explaining 85.7% and 54.8% of phenotypic variation, respectively, and showing similar gene action ( d / a = 0.72 and 0.73). The QTLs, FlrFstCl and HtAvgGI, mapped within overlapping 90% confidence intervals on LC G, with somewhat different gene action ( d / a = 0.48 and 0.04, respectively), but both with appreciable additive effects.

Interactions between QTLs: Two-way interactions between all QTLs associated with each trait, respectively, were examined by analysis of variance (Proc GLM). Only one interaction was significant at even a nominal level ( P = 0.04), between QTLs on LC B (pSBlOl) and LC G (pSB445) affecting flowering. Among the 15 possible interactions, finding one (6.7%) significant at P = 0.04 could very well occur by chance.

Distribution of introgressed chromosome segments in “converted” sorghum, relative to QTLs affecting plant height or flowering time

The strategy for identifying “conversion” is shown in Figure 1. The average “converted” sorghum was

396

Distance cM

0

20

40

60

80

100

120

140

160

180

Y.-R. Lin, K. F. Schertz and A. H. Paterson

Linkage Group A Linkage Group B D D C C C G G B K 1 2 1 2 3 1 2 1 1

pSB129

pSB443a

pSB379 pSB3SO r.2543 (M3.X:RI 1 csu29 (M2.3) r.7244 (M3.8:RS)

pSB613

urn63 csujl

pSB289 rg598a

SH065 umcl6a

wnc60a csul1Oa

pSBO79

pSB443c

pSBIO9

pSB243 pSBOS3

pSB174

FIGURE 4.-Genomic regions influencing height and flowering of S. bicolor X S. popinqwrn F2 population and sorghum conversion lines. Genetic distances are presented along the abscissa, in centimorgans (Kosnunl 1944). DNA markers indicated by arrows were mapped in a smaller population of the Same pedigree (CHIITENDEN pt 01. 1994). and locations on the present map werc inferred relative to flanking anchor loci. Bars along the linkage groups indicate 90% (1 - LOD) likelihood support intcnrals for position of the QTLs, and lines extending out from the bars indicate 99% (2-LOD) likelihood support intervals for position of the QTLs (<[ PAWRSON et 01. 1988). The genotype of each sorghum conversion line is indicated by square boxes next to the markers used (rcfcr to Figure 1 for explanation). Conversion line abbreviations are as listed in Table 1. Corresponding map locations in other species (Tahles 3 and 4) were determined by mapping heterologous DNA markers in sorghum. The heterologous marker prefixes are defined in MATERIAIS AND METMOIIS. The corresponding maize (M), rice (R), and/or wheat (M’) chromosomes arc indicated by number.

comprised of 10.7% donor RFLP alleles, almost three accessions and 78 RFLP loci studied, -22% of RFLP times the proportion expected for four generations of loci showed conversion in at least one accession. random backcrossing with no selection. Across the nine Conversion is found in the vicinity of most height or

Correspondence Among Poaceae QTLs

Linkage Group C Linkage Group D

397

pSBO97

pSB195 rg463b

csul I Ib SUO68

- (R4:W21)

u FIGURE 4.- Continud

flowering QTLs mapped in the interspecific cross. Six plant height and three flowering QTLs mapped to seven different intervals of six different chromosomes, with 2-LOD likelihood intervals that cover only 26% (246 cM/935 cM) of this sorghum map. However, seven (78%) of the nine QTLs affecting height and/or flowering coincided with conversion in at least one accession. Evidence of conversion at HtAvgJl was equivocal (thus counted as not associated), as markers in the QTL likelihood interval were not informative-however, the nearest informative markers flanking the QTL interval did show conversion. Only HtAvgCl showed no indica- tions of conversion, although a distal marker in one of the two race guinea accessions is converted.

Conversion in one region of LG D is detected in all nine (100%) accessions. Additional markers were applied to better delineate the region of conversion- the region coincides closely with the locations of height and flowering QTLs (putatively Dw2and M a l of QU~NRV and KARPER 1945). In addition, the region of HtAvgJl was also enriched with DNA markers, but no additional conversion was found.

Conversion is found along regions of LGs E, F, and H, which showed no QTLs in this study. This is consis- tent with the hypothesis (F. MILLER, personal communication) that the S. bicolmstrain used (“BTx623”) retains wild-type height and flowering alleles at some loci affecting these traits. We have made crosses between the


Linkage Group E D D C C C G G B K LinkageGroupF D D C C C G G B K 1 2 1 2 3 1 2 1 1 1 2 1 2 3 1 2 1 1

f n446 (M4,5:R2)

, CSu30 (M3) ; ~ m ~ l 3 0 (M10)

pSB504 0 0 ~ 0 0 0 . rr143a (M4.6:RB)

- pSB200 pooooilJLJWg

. pSBo47 oorrmooog

FIGURE 4. - Continued

rr87 (M5:RZ) d 0 0 b (M1:RlO)

exotic and converted races and are presently testing the phenotypic consequences of this conversion.

Evidence of conversion corroborates “fix-QTL” analysis, and independence of linked QTLs: A height QTL on LC A and a flowering QTL on LC B, the effects of which were deemed significant only after adjustment for the effects of the LC D QTL(s), were supported by the finding of “conversion” in one, and three exotic/ converted pair(s), respectively.

Moreover, the inference (above) of two different QTLs on LG G (above) is supported by data for pSB069. This marker exhibits polymorphism but no conversion, and lies in between HtAugGl and HtMG2, both of which are associated with conversion in race bicolor.

Comparative mapping of height and maturity QTLs across the Poaceae

A detailed search of literature for mapped mutants and QTLs affecting height and/or flowering in maize

is summarized in Tables 3 and 4. DNA markers closely linked to mutants and QTLs associated with plant height and flowering time in maize, barley, rice, and wheat, were mapped in 56 F2 individuals of S. bicolor X S. prapinquum (CHITTENDEN et al. 1994; Tables 3 and 4), to test the correspondence among QTLs mapped herein, and those mapped previously in other Poaceae. QTL locations were determined in reference to the maize genetic map (COE and NEUFFER 1993), based on markers used in prior studies or nearby markers inferred from comparative mapping (AHN and TANKSLEY 1993). Precision in estimating chromosomal locations of QTLs varied-uncertain cases were (conservatively) accommodated by assigning QTLs to groups of adjacent intervals (e.g., 1.08- 1.10). To further accommodate differences in environmental factors, measurement factors, statistical criteria employed by different groups, and methods of publishing map positions, comparative analysis emphasized those intervals of the maize genome that showed QTL effects in four or more different

Correspondence Among Poaceae QTLs

Linkage Group D D C C C G G B K 1 2 1 2 3 1 2 1 1

studies (including both maize and sorghum). Specifi- cally, we focused on regions spanning 16.0 and 12.1% of the maize genome, which accounted for 51% of height QTLs and 47% of flowering QTLs, respectively.

QTIs or mutations affecting flowering time in sorghum, maize, rice, wheat, and barley: Across 15 maize populations studied by seven groups of researchers, 55 QTLs or mutations affecting flowering time were reported (Table 3). A total of 26 (47%) are clustered in five regions that span 12.1% of the maize genome, on chromosomes I , 5, 8, 9, and 1 0 . One flowering QTL reported in an intraspecific sorghum population was included (PEREIRA P/ nl. 1994), as well as three QTLs in an intersubspecific rice population (LI e/ al. 1995), three discrete mutants in wheat (HART et nl. 1993), and one in barley (LAURIE et al. 1994).

Chromosome I: Based on study of four different maize populations, two different groups (KOESTER et nl. 1993; VELDBOOM et nl. 1994) reported significant effects on flowering time associated with interval 1.08-1.10. Fur- ther one maize flowering mutant, i d l , was associated with this region. By mapping maize DNA probes umc83 and csu77, we found that this region corresponds to sorghum LGs C (umc83) and I (csu77) (Table 3, Figure 4). Neither QTLs nor conversion were found in this region of sorghum (Figure 4).

In addition, a rice flowering QTL, QHd9a (LI et al. 1995), corresponded to maize interval 1.08-1.10 and sorghum LC C , based on mapping of rg463b and umc83 (Figure 4).

Chromosome 5: Based on study of four different maize populations, two groups (ABLER et al. 1991; VELDBOOM et al. 1994) reported significant effects on flowering time associated with interval 5.06-5.08 of the maize RFLP map. By mapping maize, rice, and oat DNA probes umc126, umc54, csul73, umc156, cd01380, n166, and n476, we found that this region corresponds to sorghum LC F (Table 3, Figure 4). No QTL associated with flowering time was found in this region of sorghum, but conversion was found in one accession of race caudatum (Figure 4).

Chromosom 8: Based on study of nine different maize populations, five groups (ABLER et nl. 1991; BEAVIS et al. 1991; STUBER et al. 1992; ZEHR ~t al. 1992; KOESTER et al. 1993) reported significant effect5 on flowering time associated with interval 8.05-8.07 of the maize RFLP map. By mapping rice DNA probes n244, 7~776, and maize probes c.w3l, e.~ullO, umc12, umc89, and csu142, we found that this region corresponds to sorghum LGs A (n244, n776, csu31, csullOn), C (umcl2, umc89), and C (csu142 Table 4, Figure 4). No QTLs associated with flowering time were found in any of these regions in


Linkage Group I Linkage Group J D D C C C G G B K 1 2 1 2 3 1 2 1 1

6 ch344a (M1.3.4R12WS~)

a Height of main culm only Average days to anthesis of main culm plus the fmt four tillers

a Polymorphism. no conversion 0 No polymorphism = Conversion

FIGYRE 4.-Conlin1c~d

Distance CM

1

!O

10

50

90

100

1 20

140

160

180

sorghum, but conversion was associated with height QTLs on LG A in one accession of race kafir, and LG G in one accession of race bicolor (Figure 4).

Chromosome 9: Based on study of four different maize populations, two groups (ABLER et al. 1991; BFAVIS et al. 1994) reported significant effects on flowering time associated with interval 9.03-9.04 of the maize RFLP map. By mapping maize and rice DNA probes csu158, csu147, umcl14, umc81, n612, cdol7, and cd078, we found that this region corresponds to sorghum LGs I and C (umc81 only; Table 3, Figure 4). Neither QTLs

nor conversion were found in this region of sorghum (Figure 4).

In a S. bicolor X S. bicolor cross (PEREIRA et al. 1994), a QTL affecting flowering time corresponding to the maize interval 9.03-9.04 was reported (Table 3). Fur- ther, QHd3a affecting flowering time in rice (Lr et al. 1995) corresponds to this region of sorghum LG C (Fig- ure 4) based on mapping of cd020, rg348, rg944, and n329.

Chromosome 10: Based on study of three different maize populations, one group (KOESTER et al. 1993)

Correspondence Among Poaceae QTLs 40 1

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reported significant effects on flowering time associated with interval 10.08 of the maize RFLP map. All three populations were generated from the same cross, NC264 X SC76, and were three of only four temperate X tropical maize crosses found. By mapping maize and rice DNA probes umc44, bnllO. l?, and n l 7 , we found that this region corresponds to sorghum LG D (Table 3, Figure 4). We did detect a QTL associated with flowering time in this region, FIrAvgDl (putatively Mal of QUINBY and KARPER 1945) (see below), and found conversion in all nine sorghum accessions examined (Fig- ure 4).

Maize chromosome 10 corresponds to homoeologous group 2 chromosomes of wheat (AHN et al. 1993), and several markers of wheat group 2 chromosomes, rz69, n l 7 , and cdo1328, map to this region of sorghum. The photoperiodic genes of wheat, p p d l , ppd2, and ppd?, are located on homoeologous group 2 chromosomes (WOIUAND and LAW 1986; HART et al. 1993). In barley, a major photoperiod response gene, PPD-HI, was mapped on the short arm of chromosome 2 (2H) and is orthologous to wheat ppdl (LAURIE et al. 1994). This correspondence is described in more detail else- where (A. H. PATERSON, Y. LIN, Z. LI, K. F. SCHERTZ, J. F. DOEBLEY, S. R. M. PINSON, S. C. LIU, J. W. STANSEL and J. E. IRVINE, unpublished data).

QTLs or mutations affecting plant height in maize, rice, sorghum, and wheat: Across 22 maize populations studied by 10 groups of researchers, 105 QTLs or mutations affecting plant height have been reported (Table 4). A total of 54 (51 %) of those are clustered in seven regions that span 16.0% of the maize genome, on chromosomes 1, 3 (two regions), 4, 8, 9, and 10. In an intraspecific sorghum population, four height QTLs were found ( PEREIRA et al. 1994). In an intersubspecific rice population, four QTLs affecting plant height were reported with 90% likelihood intervals spanning 3.3% of the genome (LI et al. 1995). Three height mutants on the linkage maps of rice and wheat were also included.

Chromosome 1: Based on study of seven different maize populations, four different groups (BEAVIS et al. 1991; KOESTER et al. 1993; SCHON et al. 1994; VELDBOOM et al. 1994) reported significant effects on plant height in the interval 1.08-1.10. Further, three height mutants, br2, an l , and brl, were associated with interval 1.08-1.10 of the maize RFLP map (COE and NEUFFER 1993). As shown above, this regon corresponds to sorghum LGs C and I (Table 4, Figure 4). Neither QTLs nor conversion was found in this region of sorghum (Figure 4).

In a S. bicolor X S. bicolor cross (PEREIRA et al. 1994), one height QTL that the authors tentatively identified as Du, (of QUINBY and KARPER 1945) corresponded to maize interval 1.08-1.10. In addition, a rice height QTL, QPh9a (LI et al. 1995), corresponded to this region, as we revealed by mapping rg463 in sorghum. This interval corresponded to sorghum LG C (Table 4,

Figure 4), where neither height QTLs nor conversion were found (Figure 4).

Chromosome 3: Based on study of four different maize populations (but only two different pedigrees, and all involving inbred B73), three studies (BEAMS et al. 1991, 1994; ZEHR et al. 1992) reported significant QTLs for plant height in maize interval 3.03. For all cases in which allele effects were reported (BEAVIS et al. 1991, 1994), B73 alleles were associated with increased height. Further, three height mutants, d l , d2, and crl, were associated with maize interval 3.03 (COE and NEUF- FER 1993). By mapping rice DNA probe 7x543, we determined that this region corresponds to sorghum LG A (Table 4, Figure 4). Neither QTLs nor conversion were found in this region of sorghum.

Based on study of four different maize populations, three groups (BEAVIS et al. 1991; STUBER et al. 1992; SCHON et al. 1994) reported significant effects on plant height in maize interval 3.05-3.07. Further, four height mutants, rd3, yd2, nul , and sdw2, were associated with maize interval 3.05-3.07 (COE and NEUFFER 1993). By mapping maize DNA probes csu30, umc60, and rice probe n244, it was determined that this region corresponds to sorghum LGs A, E ( c s u ~ O ) , and G( umc606) (Table 4, Figure 4). We did detect both plant height QTLs and conversion, on both LGs A and G in this region (Figure 4).

Chromosome 4: Based on study of five different maize populations (three different pedigrees, and two involving inbred Mo17), five different studies (BEAMS et al. 1991; D O E B L E Y ~ ~ ~ STEC 1991; STUBER et al. 1992; ZEHR et al. 1992; VELDBOOM et al. 1994) reported significant effects on plant height in maize interval 4.05-4.06 (COE and NEUFFER 1993). One height mutant, stl, was associated with interval 4.05-4.06 (COE and NEUFFER 1993). By mapping maize, rice and oat probes, umc156, rz567, cd0400, cdo507, and cdo1380, we determined that this region corresponds to sorghum LG F (Table 4, Figure 4). No height QTLs were found in this region, but conversion was found in one accession of race caudatum (Figure 4).

The five different maize studies include only three different pedigrees, two involving inbred Moly. One of the two pedigrees was the cross Mol7 X B73, which showed overdominance ( d / a > 0) in two different populations (BFAVIS et al. 1991, 1994; VELDBOOM et al. 1994).

Chromosome 8: Based on study of nine different maize populations, five different groups (ABLER et al. 1991; DOEBLEY and STEC 1991; STUBER et al. 1992; KOESTER et al. 1993; BEAVIS et al. 1994) reported significant effects on plant height, and three height mutants, ctl, des1 7, and sdwl, were associated with maize interval 8.05-8.07 (COE and NEUFFER 1993). As shown above, this region corresponds to LGs A, G, and C of sorghum. We did detect both conversion and QTLs associated with plant height in each of these three regions (Figure 4). In a S. bicolor X S. bicolor cross (PEREIRA et al. 1994), a QTL


affecting plant height in this region was also reported (Table 4, Figure 4).

Chromosome 9: Based on study of seven different maize populations, four reports (ABLER et al. 1991; BEAVIS et al. 1991; DOEBLEY and STEC 1991; STUBER et al. 1992) described significant effects on plant height. Further, one height mutant, d?, was associated with maize interval 9.03-9.04 (COE and NEUFFER 1993). As shown above, this region corresponds to sorghum LGs I and C (umc81; Table 4, Figure 4). We did detect both a QTL and conversion on LG C, associated with plant height in this region (Figure 4).

In a S. bicolor X S. bicolor cross (PEREIRA et al. 1994), a QTL affecting plant height corresponded to maize interval 9.03-9.04 was reported (Table 4, Figure 4). The report’s authors tentatively designated this Dw, of QUINBY and KARPER (1945), but see DISCUSSION.

One QTL affecting plant height of rice, QPh3a (LI et al. 1995), corresponds to this region of sorghum LG C based on mapping of cdo20, rg348, rg944, and a329 (Figure 4).

Chromosome 10: Based on study of four different maize populations, three different groups (DOEBLEY and STEC 1991; ZEHR et al. 1992; KOESTER et al. 1993) reported significant effects on plant height associated with maize interval 10.08. As shown above, this region corresponds to sorghum LG D (Table 4, Figure 4). We did detect a QTL associated with plant height in this region (LG D), tentatively Dw, of QUINBY and KARPER

(1945) and did find conversion in all sorghum accessions, in this region (Figure 4).

Homoeologous chromosomal regions that influence common phenotypes within taxa: Maize is well-known to be paleopolyploid, and many homoeologous chromosome segments can be identified by mapping of genetic markers to duplicated sites (HELENTJARIS et 01. 1988; WHITKUS et al. 1992; A H N and TANKSLEY 1993). We have been able to infer homoeology for 21 (66%) of the 32 chromosomal regions summarized in Tables 3 and 4 (Figure 5). Among the 28 regions affecting height of maize, 14 (50%) tentatively fall into seven homoeologous regions. Among a total of 25 regions affecting flowering of maize, eight (32%) tentatively fall into four homoeologous regions. The most striking case is in maize interval 3.08-3.09, which harbors four height and two flowering QTLs: the corresponding interval 8.05-8.07 was associated with nine height and nine flowering QTLs, as well as three discrete height mutants (Tables 3 and 4). Homoeologous maize intervals 1.03-1.04 and 9.05-9.07 each showed two height and three flowering QTLs (Tables 3 and 4). Several additional intervals show corresponding effects on either height or flowering (Figure 5).

DNA markers detect duplicate loci in sorghum (WHITKUS et al. 1992) and rice (GAUSSE et al. 1994) less frequently than in maize, making it more difficult to assess possible homoeology among QTLs in these taxa.

However, we (CHITTENDEN et al. 1994) and others (PER- EIRA et al. 1994) have shown that (at least) segmental chromosome duplication has occurred in sorghum.

One possible case of homoeologous QTLs in sorghum was found. Markers cdol l60 and umc60 mapped to linked duplicated sites on sorghum LGs A and G, in regions that were each associated with height QTLs, HtAvgAl and HtAvgGl (Figure 4). Mapping of additional duplicated markers will be necessary to permit comprehensive assessment of homoeology among sorghum QTLs.

The duplicated region of FlrAvgDl, on sorghum LG I, was not associated with flowering time in the interspecific sorghum population, and no conversion was found in this region. One flowering QTL was detected in an intraspecific sorghum population (PEREIRA et al. 1994), which appeared to correspond to LG I based on mapping of a single maize DNA probe (Table 3) -however, the maize probe detected a second faint restriction fragment that we could not map. Duplication of the relevant DNA probe (umcl14) on sorghum LGs D and I (in our nomenclature) would resolve incongruity between our data and that of PEREIRA et al. (1994) in assignment of Mal and Dw2.

Transgression of parental height phenotypes in sorghum and maize may be partly due to corresponding genetic loci: Transgressant interspecific progenies were found for both flowering time and plant height. FlrAvgBl ( d / a = -1.61; Table 2), partly accounts for heterozygous individuals that flowered earlier than S. bicolor. HtMG2 ( a = 0, d / a = -18.74; Table 2), partly accounts for height exceeding that of S. propinquum. Three of the five remaining height QTLs showed d > 0 but a = 0 and may have contributed to height exceeding that of S. popinquum.

Height QTLs reported herein which tentatively show “overdominance” ( d > a - 0) correspond to previously reported loci that tentatively showed overdominance in both sorghum and maize. Among four height QTLs identified in the intraspecific sorghum population CK60 X PI229828, only one showed evidence of overdominance (PEREIRA et al. 1994). This QTL corresponded to both HtAvgAl and HtMG2 herein (see homoeology, above), both showing d > a. Finally, these QTLs also correspond to overdominant height QTLs on chromosome 8 in maize (STUBER et al. 1992). While the correspondence among these loci is striking, we ac- knowledge that evidence of overdominance from QTL mapping must be interpreted with caution, as it is s u b ject to variation in estimating both a and d.

DISCUSSION

Comparative mapping yields a more comprehensive “catalog” of QTLs than can be obtained from any individual population. It is virtually inconceivable to iden- tify, or create, a single population that segregates for


Maize Maize Chromosome I Chromosome 5

I

cdo200

bn15.62

Maize Chromosome 9

Maize Maize Chromosome 2 Chromosome IO

mc163

cdo1328b

cdo348b cab456b

Maize Chromosome 7

FIGURE 5.-Homoeologous genomic regions affecting height and flowering in maize and sorghum. For most maize probes, duplicated loci are as reported by COE and NEUFFER (1993). For most rice, oat, and barley probes, duplicated markers are as reported by AHN and TANGLEY (1993), and locations on the COE and NEUFFER (1993) map are inferred relative to linked DNA markers. All sorghum DNA markers are as reported herein, or in CHITTENDEN et nl. (1994).

allelic variants at all genetic loci potentially influencing a complex phenotype. Even if such a population could be created, QTLs with relatively large effects would tend to obscure those with smaller effects (6 PATERSON el al. 1988, 1990; LANDER and BOTSTEIN 1989). Comparative analysis of disparate taxa and pedigrees permits one to catalog allelic variants at a maximal number of potential “traitdetermining” loci.

Interspecific (or other “wide”) crosses are especially

useful in comparative QTL mapping, being rich in allelic variants. The minimum of 78% correspondence of conversion in s. bicolor with QTLS from S. pqbinquum suggests that many such variants are relevant to the primary gene pool, at least in sorghum. Moreover, the prepon- derance of dominant alleles associated with tall stature and late flowering suggests that alteration of these traits in cultivated sorghums has proceeded largely by selection for recessive “loss-of-function” mutations.


Maize Maize Chromosome 3 Chromosome 8

npi220

pi0200042

wncl03a r2244a wncl24

rz244b bnll3.05~

m 3 2 b

bn11024b npi268

wnc164a

npi414

wnc7

Maize Maize Chromosome 4 Chromosome 5

The utility of a comparative approach to genetic analysis of complex traits is exemplified not only by correspondence of QTLs in different taxa but also by correspondence of at least some QTLs on homoeologous chromosomal segments within maize and perhaps also in sorghum. Correspondence in the mode of gene action for height QTLs in sorghum and maize further supports the possibility of independent, but conver- gent, mutations in common genes.

Comparative mapping of height and flowering QTLS in the Poaceae: QTLs affecting height and flowering of sorghum correspond to those in maize and rice, at levels explicable by chance in only 0.5-10.5% of cases (Table 5). Among the eight genomic regions asociated with sorghum height QTLs herein and in PEREIM et al. (1994), five were associated with height variation in maize, and two with height variation in rice. Among

the five genomic regions most commonly associated with variation in flowering time of maize, two were associated with flowering variation in sorghum and two with flowering variation in rice.

Conservation of the genomic region associated with short-day flowering in the Poaceae appears to transcend ancient chromosomal duplication in the genomes of sorghum and rice, respectively (A. H. PATERSOX, Y. LIN,

S. C. LIU,J . W. STANSEL and J. E. IRVIXE, unpublished data). The maize interval 8.05-8.07 and its homoeolog 3.08-3.09 are the genomic regions most commonly associated with nine height QTLs and also harbors three discrete height mutants, c t l , ck.717, and sd~ul , in interval 8.05-8.07 and four height QTLs in interval 3.08-3.09. The corresponding regions in sorghum affect plant height in both intraspecific (PEREIM ~t al. 1994) and

z. LI, K. F. SCHERTZ, J . F. DOERLEY, s. R. M. PINSON,

Correspondence Among Poaceae QTIs 407

Maize Chromosome 6 Chromosome 9

Maize Sorghum Linkage Group A Linkage Group c

Sorghum

7 b

H Intervals for QTLs affecting plan! height a Intervals for QTLs affecting flowering 0 Probable location of relomere

pSB I2 9

pSB443a

pSB350 pSB379

pSB614

pSB613

pSB289 , f q $ h umc a

1otrc6Oo pSBO79

pSB443c

pSBlO9

pSB333h pSB243

P I

interspecific populations (HtAugA I , HtAvgC1, and/or H M G 2 ) and in an intersubspecific rice population ( QPh2n and QPh3n).

Relationship between height and flowering: In most Poaceae, flowering terminates apical growth (increase in height). Increased plant height is often correlated with late flowering. Is this correlation caused by pleiotropic effects of the same genes or different closely linked genes with independent effects on plant height or flowering time?

A small region on sorghum LC D explained 54.8% of variation in height and 85.7% of variation in flowering time. A small region of LG G explained 6.7% of height variation and 4.2% of flowering time variation. Linkage of these QTLs largely explained the correlation ( r = 0.79) between height and maturity observed herein. Sim- ilarly high phenotypic correlations of plant height and flowering time were previously reported in sorghum ( r = 0.5: WENZEL. 1990; r = 0.76: b o and Goun 1979), rice ( r = 0.51 : LI d nl. 1995) and maize ( r = 0.4: KOESTER ~t nl. 1993; r = 0.69, 0.55: BF>\VIS pt nl. 1994). However,

VEL~DROOM et nl. (1994) found no si<gnificant correlation of height and flowering in maize. All mapping studies which showed correlations also showed specific QTL regions that influenced both traits.

The finding, in a companion study (A. H. PATERSON, Y. LIN, Z. Lr, K. F. SCI-IERTZ, J . F. DOERLEY, S. R. M. PINSON, S. C . LIU,J. W . STANSEI. andJ. E. IRVINE, unpublished data), that the gene(s) determining short-day flowering occur in corresponding locations across many Poaceae is paralleled herein by correspondence of nearby genes affecting plant height. It is unlikely to be happenstance that corresponding regions of LG D in sorghum, chromosome IO (interval 10.08) in maize, chromosome 4 in rice, and group 2 homoeologs in wheat all harbor height genes or mutants, e . g , d l I and d8 in rice (KINOSHITA and TAKAHASHI 1991; TANKSLEY d nl. 1993), Rlzt8 in wheat (GALE 1985; WOUND and LAW 1986; HART Pt 01. 1993), f i o 2 in sorghum, and height QTLs in four maize crosses (Table 4).

Comparative data support the possibility that independent, closely linked genes, rather than a single gene,


TABLE 5

Likelihood that coincidence among QTLs/mutants in different taxa would occur by chance

Height“ Floweringb

Sorghum Rice Sorghum Rice

Maize 0.0005 0.082 0.043 0.043 Sorghum - 0.105 - 0.027

‘ Comparisons were based on seven genomic regions most commonly associated with height QTLs (mutants) across 22 maize populations (Table 4), as described in text; four height QTLs reported in LI et al. (1995) study of rice; and six height QTLs reported herein and four height QTLs reported in PER- EIRA et al. (1994) in sorghum.

*Five genomic regions most commonly associated with flowering QTLs across 15 maize populations (Table 3); three flowering QTLs reported herein and one flowering QTL reported in PEREIRA et al. (1994) in sorghum; and three flowering QTLs reported in LI et al. (1995) and the only mapped photoperiodic genes (Se-I and Se-3) in rice (CAUSSE et al. 1994).

account for increased height and short-day flowering, respectively. Many pairs of independent discrete mutations affecting height and flowering, respectively, are closely linked in corresponding locations of other species. In wheat, Ppdl and Rht8 are linked on chromosome 20 (WORLAND and LAW 1986; HART et al. 1993). In rice, Se1 and Se-3 on chromosome 6 are closely linked with d-4 and d-9 (KINOSHITA and TAKAHASHI 1991; CAUSSE et al. 1994). QUINBY and KARPER (1945) reported that Mar and h2 were closely linked, with ca. 8% crossing over in 47 F3 families evaluated (based on phenotype) -however, the extent of variation we observed within geno- typic classes for these loci suggests that this estimate may be somewhat imprecise. In other species such as wheat (WORLAND and LAW 1986), detailed study of homozygous recombinant stocks has more clearly demonstrated that coupled effects on plant height and flowering in the corresponding chromosomal region are due to close linkage between different genes, rather than pleiotropic effects of a single gene.

The general conservation of gene order across di- verse Poaceae ($ HULBERT et al. 1990; WHITKUS et al. 1992; A H N and TANKSLEY 1993; A H N et al. 1993; BENNET- ZEN and FREELING 1993; HELENTJARIS 1993; SHIELDS 1993; KURATA et al. 1994) may partly account for the widespread association of increased height and late flowering. Close linkage between ancestral Mal and Dw2 genes in the prototypic grass may have persisted either by chance or due to a selective advantage. It is curious that in a genome of ca. 1100 cM (based on the conservative recombinational estimates herein), the two loci with largest effects on height and flowering time are linked at a distance of ca. 8 cM, an event which would only be expected by chance in 0.72% of cases. Virtually all of the 65 million years of Poaceae evolution occurred in the wild, where increased height affords a competi-

tive advantage in light interception and seed dispersal, and short-day flowering synchronizes seed development with water availability in the semiarid centers of origin of most Poaceae (HARPER 1977). Dominant “function” alleles at different genes that conferred both optimal height and flowering time to the same progenies by virtue of close linkage might have become fixed more quickly than those at independently segregating loci conferring only one of these attributes.

Genetic control of flowering in temperate us. tropical environments: Photoperiod sensitivity is a common phenomenon in the Poaceae. In this study, only the QTL on LG D (FlrAvgDl) shows a phenotypic effect large enough to account for the shortday/longday flowering dichotomy (Figure 3)-we infer that this is Mal ( QUINBY and KARPER 1945). This locus has an es- sentially discrete effect, although the influence of other genetic loci precluded mapping as a discrete character (this was attempted, but the gene mapped distal to the end of LG D, at a distance that was unrealistic in view of the marker density of the sorghum map). Moreover, the corresponding locus appears to be partly if not solely responsible for short-day flowering in sugarcane, maize, wheat, barley, and perhaps rice (A. H. PATERSON, Y. LIN, Z. Lr, K. F. SCHERTZ, J. F. DOEBLEY, S. R. M. PINSON, S. C. LIU, J. W. STANSEL and J. E. IRVINE, unpublished data).

Temperate adaptation of sorghum (and other grasses) has largely involved selection for recessive mutants that result in earlier flowering, and the discovery of a dominant allele for early flowering (nrAvgBI) was unex- pected. Only one sorghum flowering gene, Ma4, has previously been associated with dominance of early flowering. Ma4, discovered in Hegari and existing as a dominant allele in Milo, is influenced more by temperature than recessive mal, maz, and maq from Milo. At high temperatures, recessive ma4 behaves like dominant Ma4 (QUINBY 1966). In a tropical environment, there would thus be no phenotypic consequences of mutation (loss of function) at Ma4, but in adaptation to temperate cultivation the dominant allele would quickly become fixed in heterogeneous populations. Thus, it is plausible that S. propinquum possesses a recessive ma4 allele that delays flowering only under temperate conditions. Alternatively, the dominant allele for early flowering may be at a new locus not previously described.

Relationship of height and flowering QTLs to phytochrome: The phytochrome gene family is perhaps the beststudied regulator of photomorphogenesis in plants. Mutations in phyb have a pronounced phenotypic effect on flowering and other traits of Arabidopsis (REED et al. 1993), eliciting a phenotype that bears a striking resemblance to the ma3R allele of sorghum (CHILDS et al. 1992).

Our data show minimal association between phytochrome and flowering QTLs but stronger association between phytochrome and height QTLs. Mal , on LG


D, does not correspond to any phytochrome gene cloned to date ”phya, phyb, and phyc all map to sorghum LG C, and corresponding regions of other Poaceae chromosomes (M. M. CORDONNIER-PUTT, G. KOCHERT, Y.-R. LIN, A. H. PATERSON, L. H. PUTT, unpublished data). In our tropical X temperate sorghum cross, no flowering QTLs are found on LG C. In maize, phyal and phya2, homoeologous loci on intervals 1.11 -1.12 and 5.02-5.03, are both closely associated with height mutants. Phyb in maize, mapped at interval 9.05-9.06, was associated with height QTLs in both maize and sorghum (Table 4, Figure 4). The region of rice chromosome 3 near phyb, between markers rglO4 and rg944, is associated with QTLs for both height and flowering in an intersubspecific rice population (LI et al. 1995). Finally, the same region in a different rice population accounts for one of two genes regulating photoperiodic male-sterility (ZHANG et al. 1994).

Homoeolog among height and flowering QTLs: The suggestion that segregation at homoeologous loci may account for some cases of “polygenic” variation in seed characteristics (A. H. PATERSON, Y. LIN, Z. LI, K. F. SCHERTZ, J. F. DOEBLEY, S. R. M. PINSON, S. C. LIU, J. W. STANSEL and J. E. IRVINE, unpublished data), is reinforced herein by correspondence of QTLs affecting plant height both in maize and sorghum and by QTLs affecting flowering of maize. It is intuitive that in a polyploid of recent origin such as wheat, height and flowering genes frequently map to homoeologous chromosomes (cf : group 2: WORLAND and LAW 1986; HART et al. 1993). It is noteworthy that in a “weakly diploidized” genome such as maize (HELENTJARIS et al. 1988; WHIT- KUS et al., 1992; & I N and TANKSLEY 1993), 50% of intervals affecting height fall into seven pairs of homoeologous regions. It is curious that in a highly diploidized genome such as sorghum (WHITKUS et al. 1992; CHIT- TENDEN et al. 1994), closely linked duplicated loci detected by DNA probes umc60 and cdol160 (LGs A and G), flanked height QTLs in each (putatively) duplicated chromosome segment.

Homoeology among QTLs would facilitate molecular cloning of this class of genetic loci, which has not been cloned to date. Specifically, by first isolating QTL alleles of relatively large phenotypic effect, one could simply isolate corresponding homoeologous alleles of smaller effect, an approach exemplified in extremis for cases where a discrete mutation appears to correspond to a QTL (see below). Moreover, by “parallel walks” in different homoeologous chromosomal regions, obsta- cles such as repetitive DNA arrays, and bias in represen- tativeness of megabase DNA libraries might be obviated (A. H. PATERSON, Y. LIN, Z. LI, K. F. SCHERTZ, J. F. DOEBLEY, S. R. M. PINSON, S. C. LIU, J. W. STANSEL and J. E. IRVINE, unpublished data).

The role of qualitative genes in quantitative traits: Al- leles with qualitative effects are more readily cloned than alleles with quantitative effects-identification of

qualitative alleles at multiallelic loci may greatly facilitate cloning of QTLs (ROBERTSON 1985).

Our results support a prior study (BEAVIS et al. 1991) in finding associations between qualitative mutants and QTLs more often than would be expected by chance. In maize, 75% of intervals harboring discrete height mutants also harbored height QTLs ( c t l , h2, rd2, and 0-4 are not listed on Table 4), and 43% of intervals harboring QTLs also harbored mutants (Table 4). The only flowering mutant of maize reported, id l , is associated with one maize QTL and one rice QTL (QHd9a). The clearest example is maize interval 8.05-8.07, which harbors the ctl , des1 7, and sdwl height mutants, and is associated with height QTLs in nine maize populations, as well as both interspecific and intraspecific sorghum populations (Table 4).

However, the association between QTLs and qualitative mutants is by no means absolute. Maize intervals 3.08-3.09 and 10.08, which show height QTLs in many populations, are not associated with discrete mutants (Table 4). Further, four height mutants, gll7, na2, td l , and bvl, in the interval 5.06-5.08 are associated only with one QTL (Table 4).

Correspondence of introgressed chromosome segments in conversion lines with height and flowering QTLs in the interspecific cross: At least seven of nine QTLs influencing height and/or flowering time of the interspecific sorghum population corresponded to regions of conversion (introgression), and the magnitude of QTL effects was closely correlated with the frequency of conversion. The region of the QTLs with largest effects on height and flowering (LG D) has been “converted” in all nine accessions. The regions with the second largest effects on height and flowering, respectively, have been converted in two accessions (HtAvgJI) and three accessions (RrAvgB1). All other QTL regions are converted in only one accession (Figure 4), based on present data-although there exists the possibility of additional conversion not yet detected. Moreover, five regions (on three chromosomes) not associated with QTLs were converted-we are evaluating crosses between exotic and “converted” types to determine whether these regions harbor additional QTLs, or were simply converted by chance.

DNA markers flanking the mapped loci are of consid- erable utility for sorghum improvement. Many of the 12 generations of the sorghum conversion program are done for phenotypic testing of heterozygosity and might be eliminated by using codominant DNA markers to detect genotypes heterozygous for recessive alleles imparting reduced height and/or early flowering. By converting RFLPs to cleaved amplified polypmor- phic sequences ( JARVIS et al. 1994), simplified PCR- based assays for the most prominent height and maturity loci in sorghum can be conducted quickly and effi- ciently. Moreover, integration of these results (Figure 4) with widely used markers in maize (COE and NEUFFER


1993) and rice (CAUSSE et al. 1994) broaden the utility of this comparative “cataloging” of genes influencing height and/or flowering.

The sorghum conversion program as a model for “pedigreebreeding”: Molecular analysis of the sorghum conversion program (CJ: ROSENOW and CLARK 1987), a highly focused classical plant breeding project, serves as an example of a generally applicable approach to capturing genetic information accumulated over de- cades, or even centuries, of breeding progress. Levels and patterns of “conversion” (introgression) implicate one particular chromosomal region as the primary de- terminant of the traits under selection, and suggest sup- porting roles of several other genomic locations. Similar patterns have recently been reported in derivatives of historical introgression events in another crop, cotton (Gossypium hirsutum) ( W ~ G et al. 1995). In the present study, however, the inference is supported, and the underlying trait(s) identified, by QTL mapping.

Conceptually, mainstream plant breeding programs differ from the sorghum conversion program primarily in two ways selection for a wider range of traits is prac- ticed in mainstream breeding programs and genetic exchange is less-easily monitored in mainstream breeding programs, as elite germplasm affords less DNA polymorphism than the exotic germplasm used in the sorghum conversion program. In our experiments, specific chromatin segments have been associated with phenotypes peculiar to one progenitor. In principle, such an approach might well be extrapolated to the more complex array of traits and progenitors which comprise a classical plant breeding program. Use of many DNA markers, or highly polymorphic DNA marker systems, to evaluate the genome-wide consequences of more complex long-term breeding programs, may point to genomic regions that confer particular attributes of elite germplasm.

Prospects. Comparative QTL maps find potential ap- plication in many aspects of the life sciences especially breeding and genetics, physiology, and molecular cloning. A comparative QTL map might be used to predict the locations of new reduced height mutants in which allelic variation has not yet been found and perhaps even to guide a search for such new variants in breeding programs. By establishing correspondence between well-defined mutations in different taxa, the physiolo- gist might focus on orthologous genes (via pairs of near- isogenic lines) and maximize the validity of comparative studies. Through unification across taxa of the repertoire of genes influencing complex traits, genes of interest in a large, highly duplicated genome such as maize might be more simply cloned based upon allelic variants in more facile genomes such as sorghum ( CHIITEN- DEN et al. 1994) or rice (CAUSSE et al. 1994). “Parallel walks” in multiple species (A. H. PATERSON, Y. LIN, Z. LI, K. F. SCHERTZ, J. F. DOEBLEY, S. R. M. PINSON, S. C. LIU, J. W. STANSEL and J. E. IRVINE, unpublished data)

may obviate problems such as species-specific repetitive DNA arrays (X. ZHAO and A. H. PATERSON, unpublished data), or bias in megabase DNA libraries. Comparative mapping, based upon persistence of large tracts of chromatin only rarely interrupted by rearrangements across millions of years of evolution, provides a means to unify, and thereby simplify, molecular analysis of complex phenotypes.

We thank J. TAYLOR, M. HUSSEY, S. KRESOVICH, J. PEDERSON, and the anonymous reviewers for valuable suggestions, Z. LI, S . PINSON, J. STANSEL and W. PARK for providing data prior to publication, D. ROSENOW for germplasm, E. COE, J. GARDINER, S. MCCOUCH, M. SORRELLS, and S. TANKSLEY for DNA probes, and J.-L. CHANG, Y.-L. CHANG, J.-M. DONG, T-H. LAN, and S.-C. LIU for technical help. As- pects of this work were supported by the USDA Plant Genome Pro- gram (92-37300-7654 to A.H.P., K.F.S., and R. A. WING), USDA-ARS (KFS), Pioneer Hibred Competitive Grants Program (A.H.P., K.F.S.), and Texas Agricultural Experiment Station (A.H.P.).

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Comparative Analysis of QTLs Affecting Plant Height and ... · Poaceae, more frequently than would be expected by chance. Possible homoeologous QTLs were found within both the maize