Crop Science 42:348-354 (2002)
© 2002 Crop Science Society of America
CROP BREEDING, GENETICS & CYTOLOGY
A Novel Gene ef1-h Conferring an Extremely Long Basic Vegetative Growth Period in Rice
Hidetaka Nishida,
Hiromo Inoue,
Yutaka Okumoto and
Takatoshi Tanisaka*
Graduate School of Agriculture, Kyoto Univ, Kyoto 606-8502, Japan
* Corresponding author (tanisaka{at}kais.kyotou.ac.jp)
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ABSTRACT
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A late-heading mutant line, HS169, which was induced by gamma-ray irradiation to seeds of the japonica rice (Oryza sativa L.) cultivar Gimbozu, has an extremely long basic vegetative growth (BVG) period. A genetic analysis using the F2 population from the cross HS169 x Gimbozu showed that the late heading of HS169 is governed by a recessive mutant gene. The subsequent analysis of heading responses of HS169, Gimbozu, and six heading-time tester lines to five photoperiods (10, 13, 14, 15, and 16 h) revealed that the mutant gene confers an extremely long BVG period by itself. A recessive allele, ef1, at the heading-time locus Ef1 has been considered to confer an extremely long BVG period, but experimental results showed that the effect of ef1 is modified by the allelic constitution at the photoperiod sensitivity locus Se1. The allele ef1 increases the BVG period markedly only when coexisting with the nonfunctional allele Se1-e at the Se1 locus. As a result of allelism test and subsequent trisomic analysis, the mutant gene was found to be a nonfunctional allele at the Ef1 locus on chromosome 10. We designated this mutant gene ef1-h. On the basis of the results, causal genetic pathways to flowering in rice and the significance of ef1-h in recent rice breeding in the low latitudes were discussed.
Abbreviations: BVG, basic vegetative growth • DH, days from sowing to heading • GA, gibberellic acid • PS, photoperiod sensitivity • PSP, photoperiod sensitive phase • QTL, quantitative trait loci • RFLP, restriction fragment length polymorphism • RP, reproductive phase • SSLP, simple sequence length polymorphism
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INTRODUCTION
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FLOWERING TIME plays a principal role in the regional adaptability of the rice. In the long-day plant Arabidopsis thaliana (L.) Heynh., regarded as a model plant to study the genome structure of dicots, a number of genetic and physiological studies on flowering time have been made utilizing a large number of flowering-time and flower-formation mutants induced from various ecotypes. Consequently, physiological and biochemical functions of many flowering-time genes have been described, and several genetic pathways to flowering have been proposed (Levy and Dean, 1998; Simpson et al., 1999). Thus induced mutations are very useful for investigating the genetic mechanism of flowering in many plant species.
In the short-day plant rice, regarded as a model monocot species, conventional genetic analyses of flowering time (heading time) have been extensively conducted; consequently, as many as 23 heading-time loci have been identified (Yokoo and Kikuchi, 1992; Tsai 1986; Poonyarit et al., 1989; Okumoto and Tanisaka, 1997; Ichitani et al., 1998). In addition, seven quantitative trait loci (QTLs) for heading time were reported (Yano et al., 1997; Yamamoto et al., 2000). However, their physiological and biochemical functions in genetic pathways to flowering still remain unknown becaue of the lack of mutant genes available for such investigations.
According to Vergara and Chang (1985), preflowering development of rice is divided into three phases: basic vegetative phase (BVP), photoperiod sensitive phase (PSP), and reproductive phase (RP). The durations of the first two show intervarietal variation, while that of the second, insensitive to photoperiod, is almost constant among cultivars. Photoperiod sensitive phase may be completely eliminated under optimum photoperiod. On the basis of this, heading time of rice has been considered to be chiefly determined by basic vegetative growth period (BVG period, nearly equal to the duration of BVP plus that of RP) expressed by days to heading under optimum photoperiod and photoperiod sensitivity (PS) expressed by a difference of days to heading between long and optimum photoperiod (Hosoi, 1981; Tanisaka et al., 1992). Most of the 23 known heading-time loci of rice, however, control PS and a few loci responsible for the BVG period have been identified; only two loci, Ef1 and Se1, are known to control the BVG period (Yokoo and Kikuchi 1982; Tsai 1986; Sato et al., 1988). A dominant allele Ef1 at the Ef1 locus confers a short BVG period, while its recessive allele ef1 confers an extremely long BVG period. At the Se1 locus, two PS alleles, Se1-n and Se1-u, confer a short BVG period, while its photoperiod-insensitivity allele, Se1-e, confers a slightly longer BVG period. To exploit new loci for the BVG period, Tanisaka et al. (1992) induced many mutants for this trait. Among them, a late heading-time mutant line HS169 exhibited an extremely long BVG period.
In the present study, we attempted to identify the mutant gene(s) conferring the extremely long BVG period of HS169, and to investigate its physiological effect on preflowering developmental phases. As a result, we found that the mutant gene is a nonfunctional allele of the Ef1 locus.
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MATERIALS AND METHODS
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A late heading-time mutant line, HS169, with an extremely long BVG period, its original cultivar Gimbozu, and six heading-time tester lines were used in the study. HS169 was induced with gamma-ray irradiation of seeds of the japonica rice cultivar Gimbozu (Tanisaka et al., 1992). The six tester lines were developed by crossing japonica rice cultivars. Their genotypes for six major heading-time loci (E1, E2, E3, Se1, Ef1, and U) are shown together with that of the original cultivar in Table 1. For other heading-time loci, these cultivar–lines have the same allelic constitution (Yamagata et al., 1986; Yokoo and Kikuchi, 1992; Inoue et al., 1998). The E1, Se1, and Ef1 loci are located on chromosomes 7 (Okumoto and Tanisaka, 1997), 6 (Yokoo and Kikuchi, 1992), and 10 (Sato et al., 1988), respectively. The E1, E2, and E3 loci are all photoperiod sensitivity (PS) loci: their dominant alleles stimulate PS, while their recessive alleles do not have such a function (Yamagata et al., 1986). The stimulating effect of E1 on PS is fairly strong, while those of E2 and E3 are not so strong (Yamagata et al., 1986). The Se1 locus has three alleles, Se1-u, Se1-n, and Se1-e: the first two intensively stimulate PS (Se1-u has a slightly stronger effect than Se1-n; Yokoo and Kikuchi, 1992), while the second does not have such a function (Yokoo and Kikuchi, 1982). The Se1 locus also controls the BVG period: compared with Se1-u and Se1-n, Se1-e increases it by a few days (Yokoo and Kikuchi, 1982). The Ef1 locus controls the BVG period: a dominant allele Ef1 decreases it, while a recessive allele ef1 increases it markedly (Tsai, 1986). The U is a PS locus and its dominant allele reduces PS (Okumoto et al., 1992).
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Table 1. Genotypes of a late heading mutant HS169, its original cultivar Gimbozu, and six heading-time tester lines which were subjected to gene analyses and photoperiodic treatments.
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Genetic Analysis of the Mutant Gene(s) (Experiment 1)
The F2 population, comprising 216 plants, from the cross between HS169 and its original cultivar Gimbozu was subjected to a genetic analysis for heading time under natural photoperiod (Fig. 1)
in 1997. The progeny test was conducted with 100 F3 lines in 1998. Each F3 line (about 25 plants/line) was the progeny of the F2 plant randomly selected out of all the F2 plants. Germinated seeds were sown in nursery beds in a green house. Seedlings were transplanted in a paddy field in Kyoto (35°01' N) 30 d after sowing. Parental lines were planted with their F2 and F3 populations. In both years, sowing was conducted on 13 May. Fertilizers applied were 60, 90, and 90 kg/ha for N, K2O, and P2O5, respectively, and plant spacing was 10 by 30 cm. Heading date was recorded for each plant when the first panicle emerged from the sheath of the flag leaf.
Photoperiodic Response (Experiment 2)
Seeds of HS169 and the seven heading-time tester lines were disinfected by soaking in benlate—methyl-1-[(butylamino)carbonyl]-H-benzimidazol-2-ylcarbamate—solution (diluted with water to 1000-fold) at 20°C for 24 h, and were pregerminated by soaking in water at 30°C for 3 d. Ten germinated seeds per line were sown on field soil in a 3.6-L pot and covered with the granulated soil. Seedlings were thinned to four plants per pot 14 d after sowing. All the tillers except the main culm were cut off whenever they reappeared. HYPONeX solution (100 mL) at a 1.3% (w/v) concentration per pot was applied as an additional fertilizer every other week.
Five photoperiods, 10, 13, 14, 15, and 16 h, beginning at the sowing date, were used. Photoperiod treatments occurred in two growth cabinets (Shimadzu SCN401, Kyoto, Japan) with temperatures of 25°C between 0800 to 1800 h and 20°C between 1800 to 0800 h. Twelve pots for each line were placed under each photoperiod. In addition to natural daylight (0800–1800 h), supplementary artificial light from incandescent lamps (3.24 W m-2 at the surface of soil) were used for all the photoperiod treatments except 10 h. The experiment was conducted from 1 May to early October, 1998.
Allelism Test of the Mutant Gene with Se1 and Ef1 (Experiment 3)
Six F2 populations from crosses HS169 x Gimbozu, HS169 x ER, HS169 x LR, HS169 x T65, HS169 x EL30, and T65 x Gimbozu were subjected to a genetic analysis for heading time under a short photoperiod (10 h). Under a 10-h photoperiod, the effects of PS loci are negligible, and only the effects of BVG loci can be recognized. After disinfection and pregermination treatments following the procedures of Exp. 2, seeds were sown on a mixture of granulated soil and vermiculite in a 5:2 ratio in plastic trays in growth cabinets. Planting density was 3 by 3 cm. The short photoperiod treatment started from sowing day. Plants were exposed to natural daylight between 0800 to 1800 h and moved into darkrooms between 1800 to 0800 h. Other experimental procedures were similar to Exp. 2.
The Se1 locus is closely linked to the isozyme locus Pgi2, with a recombination value of 1.8 ± 0.6% (Ohshima et al., 1996). Such a linkage relationship was available for confirming the genotype for the Se1 locus, because the Pgi2 locus does not influence the heading time at all. In addition, our preliminary experiments indicated that HS169 carried a japonica type allele Pgi2-1, while LR carried an indica type allele Pgi2-2. The genotype of Pgi2 locus was determined by the methods of Glaszmann et al. (1988) with a modification of using young leaves instead of plumules. All the F2 plants from the cross of LR x HS169 were used for the isozyme analysis.
Trisomic Analysis (Experiment 4)
The above experiments showed that the late-heading of HS169 was conferred by a recessive mutant gene, tentatively designated m, allelic to ef1 on chromosome 10. To confirm this, a trisomic analysis was performed. A primary trisomic series of the japonica rice cultivar ‘Nipponbare’ (NT lines; Iwata et al., 1970) were used. The genotype of Nipponbare for heading-time loci have already been identified as E1E1e2e2e3e3Se1-nSe1-nEf1Ef1, and for other heading-time loci, Nipponbare has the same genotype as the original cultivar Gimbozu (Okumoto et al., 1991). The effect of the E2 locus is almost negligible. It was, therefore, expected to observe monogenic segregation of the mutant gene locus in all the F2 populations of the trisomic lines x HS169. In each cross, the trisomic line was used as a maternal parent. The notation of the trisomic line indicates the number of the extra chromosome: for instance, line NT10 is trisomic for chromosome 10. Not all cross combinations could be obtained, and four cross combinations (NT1, 7, 8, and 10 x HS169) that produced F1 trisomic plants were subjected to the gene analysis for heading time. F2 plants were grown together with their respective cross parents and the original cultivar Nipponbare.
When the mutant locus, tentatively designated m, is located on the disomic chromosome, the predicted F2 segregation ratio of early type [++, +m] : late type [mm] is 3:1. When the mutant locus is located on the trisomic chromosome, the genotype of the trisomic plant is expected to be ++m. The trisomic plant produces male and female gametes in the ratio of 2 [+] : 1 [m] : 1 [++] : 2 [+m], if there is no recombination between the mutant locus and centromere. However, most of the male gametes with an extra chromosome cannot take part in fertilization because of their weak viability. Consequently, for disomic plant, the ratio of 8 [early type (++, +m)] : 1 [late type (mm)] is expected. As for trisomic plants, two kinds of segregation ratios are expected: one is 44 (+++, ++m, +mm) : 1 (mmm) by chromatid segregation (Haldane, 1930) and the other is 35:1 by maximum equational segregation (Burnham, 1962, p. 375). Thus, when a mutant gene is located on the extra chromosome, the proportion of late-type plants will be far smaller than 1/4. The trisomic plants could easily be discriminated from the disomic plants by the morphological trait(s) peculiar to each trisomic (Iwata et al., 1970). Therefore, checking the chromosome number in pollen mother cells or root meristems was not required. All the materials for the trisomic analysis were sown in nursery beds and transplanted in a paddy field in Kyoto on 19 May and on 23 June 2000, respectively.
Statistical Procedure
The goodness of fit of the observed segregation ratio to the expected was examined by the chi-square test.
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RESULTS
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Genetic Analysis of the Mutant Gene(s) (Experiment 1)
The F2 population from the cross between HS169 and the original cultivar Gimbozu showed a bimodal distribution within the parental ranges with a clear breakpoint, which divided the population into early (Gimbozu type) and late (HS169 type) groups (Fig. 2) . The ratio of early type : late type fit the 3:1 ratio expected for one-locus segregation (
2 = 0.222, P = 0.637). In the progeny test, all the 100 F3 lines could easily be classified into three groups. The ratio of 26:52:22 for [Gimbozu type] : [segregating type] : [HS169 type] lines fit the 1:2:1 ratio (2 = 0.480, P = 0.787) expected for one-locus segregation. This indicates that the late heading of HS169 is conferred by a single recessive mutant gene.
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Fig. 2. Frequency distribution of days to heading in the F2 population from the cross of HS169 x Gimbozu under natural photoperiod.
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Photoperiodic Response (Experiment 2)
Heading responses of HS169, the original variety Gimbozu, and six heading-time tester lines (T65, T65Ef1, EL30, EG7, ER, and LR) to five photoperiods (10, 13, 14, 15, and 16 h) are shown in Fig. 3
. Under a 10-h photoperiod, HS169 headed 61.0 d later than Gimbozu. This suggests that the mutant gene of HS169 increased the BVG period remarkably, as the difference in days from sowing to heading (DH) under a 10-h photoperiod directly shows the difference in BVG period. The comparison of the BVG period among T65, T65Ef1, EL30, and EG7 revealed that ef1 increased the BVG period, but the effect was intensively enhanced in coexistence with Se1-e, the effect of which was estimated to be 30.7 d. The comparison between ER and LR showed that Se1-e made the BVG period slightly longer than Se1-u by 7.5 d. Thus, the increasing effect of the mutant gene on the BVG period was much greater than the single effect of ef1 or Se1-e, and even the complementary effect of these two known genes. Of the eight lines used, five (HS169, Gimbozu, EL30, EG7, and LR) with a PS allele (Se1-n or Se1-u) at the Se1 locus showed a remarkably greater DH under long photoperiods (14, 15, and 16 h), while those with allele Se1-e (T65, T65Ef1, and ER) did not show so much. This implies that the Se1 locus has an intensive effect on the degree of PS. HS169 and Gimbozu, T65 and T65Ef1, and EL30 and EG7, showed a similar response to long photoperiods (14, 15, and 16 h), respectively; although, they have a genotypic difference either at the mutant gene locus or at the Ef1 locus. However, under all photoperiods, HS169 and T65 had a longer DH than Gimbozu and T65Ef1, respectively. Therefore, these results indicate that the mutant gene and ef1 have little effect on photoperiod sensitivity and have an increasing effect on DH without regard to photoperiod.
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Fig. 3. Days to heading of HS169 and seven heading-time tester lines under five (10, 13, 14, 15, and 16 h) photoperiods.
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Allelism Test of the Mutant Gene with Se1 and Ef1 (Experiment 3)
Three F2 populations of HS169 x Gimbozu, HS169 x ER, and HS169 x LR were subjected to genetic analysis for heading time under a 10-h photoperiod. The F2 population of HS169 x Gimbozu showed a bimodal frequency distribution of DH within the parental ranges with a clear breakpoint (Fig. 4)
. The ratio of early type: late type fit the 3:1 ratio expected for one-locus segregation, as observed in Experiment 1. The mutant gene thus surely confers long BVG period. Two other F2 populations showed a bimodal distribution much similar to that of HS169 x Gimbozu. This suggests that ER and LR have no genes that intensively increase the BVG period and that the effects of E2, E3, Se1, and U loci controlling PS on the BVG period were almost negligible. ER showed a slightly longer DH than Gimbozu under a 10-h photoperiod, suggesting that Se1-e makes the BVG period slightly longer. Similarities in distribution among the three populations also show that there was no apparent interaction of the mutant locus with the E2, E3, Se1, and U loci.
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Fig. 4. Frequency distributions of days to heading in the F2 populations from crosses of HS169 x Gimbozu (A), HS169 x ER (B), and HS169 x LR (C) under short (10 h) photoperiod. In the F2 of HS169 x LR, plants with a genotype Pgi2-1Pgi2-1, Pgi2-1Pgi2-2, and Pgi2-2Pgi2-2 are indicated by black, white, and gray bars, respectively.
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The genotype for the Pgi2 locus was investigated for each F2 plant from HS169 x LR (Fig. 4C). The tight linkage of the Pgi2 locus with the Se1 locus facilitates the estimation of a genotype for the Se1 locus. The ratio of Pgi2-1Pgi2-1 : Pgi2-1Pgi2-2 : Pgi2-2Pgi2-2 fit the 1:2:1 ratio expected for one-locus segregation (2 = 4.137, P = 0.126). There was no significant difference in segregation pattern among the genotypic groups: in all the genotypes, the segregation of 3 early type and 1 late type was observed. This indicates that the mutant locus is independent of the Se1 locus and does not interact with the Se1 locus.
Using four F2 populations from crosses HS169 x T65, HS169 x EL30, T65 x Gimbozu, and HS169 x Gimbozu, an allelism test between the mutant gene and ef1 was conducted under a 10-h photoperiod (Fig. 5)
. If the mutant gene and ef1 are non-allelic to each other, a large number of early transgressive segregants with the same DH as Gimbozu (genotype : wild type-/Ef1-) ought to appear in the first two F2 populations. However, such plants did not appear. In addition, the F2 population of HS169 x EL30 showed an approximately bimodal distribution of DH without transgressive segregants, and was divided into early-type (before 70 d after sowing) and late-type groups (after 70 d after sowing). The ratio of early type : late type fit the 3:1 ratio expected for one-locus segregation (2 = 0.097, P = 0.755). These results indicate that the mutant gene is allelic to ef1 on chromosome 10 and is recessive to ef1.
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Fig. 5. Frequency distributions of days to heading in the F2 populations from crosses of HS169 x T65, HS169 x EL30, T65 x Gimbozu, HS169 x Gimbozu under short (10 h) photoperiod.
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Trisomic Analysis (Experiment 4)
Frequency distributions for DH of the trisomic plants and disomic plants in the F2 populations from crosses four NT lines x HS169 are shown in Fig. 6
. None of the trisomic plants in the F2 population of NT10 x HS169 showed the same DH as HS169, while the disomic plants were deployed continuously within the parental ranges (Fig. 6D). In other cross combinations, both of the disomic and trisomic groups showed a distribution ranging between the parental lines (Fig. 6A–C). These results support that the mutant gene of HS169 is an allele of the Ef1 locus on chromosome 10.
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Fig. 6. Frequency distributions for heading time in the F2 populations of four Nipponbare trisomic lines x HS169 under natural photoperiod.
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DISCUSSION
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In the present study, our objective was to investigate the genetic factor(s) conferring the extremely long BVG period of HS169, and to investigate its physiological effect on the preflowering developmental phases. As a result, we successfully found a single mutant gene conferring an extremely long BVG period, which proved to be a novel allele at the Ef1 locus. We designated this newly detected gene ef1-h.
It is known that the Ef1 locus has six alleles, Ef1-a, Ef1-b (identical with Ef1 in the present study), Ef1-x, Ef1-gamma, Ef1-n, and ef1. Among them, the first five are isoallelic to one another and accelerate heading by conferring a short BVG period, while the recessive allele ef1 confers an extremely long BVG period (Tsai, 1986). But, the present study showed that although ef1 increased the BVG period, its effect was enhanced by the complementary effect of Se1-e (Fig. 3). On the contrary, the mutant allele ef1-h was found to confer an extremely long BVG period by itself; the effect was not modified by alleles at other loci, including Se1. In addition, the effect of ef1-h was much greater than the complementary effect of ef1 and Se1-e. This suggests that ef1 permits some residual function accelerating heading, while ef1-h loses the function entirely.
In a long-day plant, Arabidopsis, three causal genetic pathways to flowering, i.e., photoperiodic, autonomous, and GA (gibberellic acid)-mediated pathways, have been proposed as a result of physiological and biochemical studies on many flowering mutant genes (Levy and Dean, 1998; Simpson et al., 1999). The autonomous pathway is closely related to vernalization response in Arabidopsis, but there is no finding that a short-day rice plant responds to vernalization. It is also known that exogenous GA has little effect on flowering in most short-day plants (Thomas and Vince-Prue, 1997), suggesting that the GA-mediated pathway is not present in rice. In this sense, the photoperiodic pathway plays the most crucial role in determining flowering time in rice. Under all the long photoperiods (14, 15, 16 h), however, HS169 and T65 with the recessive alleles at the Ef1 locus showed a longer DH than Gimbozu and T65Ef1 with the dominant alleles at this locus, respectively (Fig. 3). Since the Ef1 locus does not affect photoperiod sensitivity, this suggests that rice has an autonomous pathway different from vernalization response, in which the Ef1 locus is involved. The Se1 locus intensively controls photoperiod response, implying that this locus is highly associated with the photoperiodic pathway. The allelic constitution at the Se1 locus did not modify the accelerating effect of Ef1, but it influenced the effect of ef1. This suggests that the Se1 locus governs the autonomous pathway by affecting the Ef1 locus as well as the photoperiodic pathway.
The BVG period estimated in the present study does not correspond completely to the BVP (Vergara and Chang, 1985) because it comprises not only the BVP but also RP (Vergara and Chang, 1985). Nevertheless, the BVG period has been frequently used as a rough parameter of BVP in many studies (Hosoi, 1981; Tanisaka et al., 1992; Inoue et al., 1998; Ichitani et al., 1998) for the following reasons: (i) its simple experimental procedures, and (ii) RP has been considered almost constant. Collinson et al. (1992), however, suggested that there is intervarietal variation, though relatively small, both in the PSP and the subsequent photoperiod insensitive phase (almost equivalent to RP by Vergara and Chang (1985)), as well as in the BVP, even under short photoperiod. To elucidate the action of the Ef1 and Se1 loci on these phases and the interaction between these loci, reciprocal transfer treatments from short to long photoperiods and vice versa should be performed by the use of near isogenic lines with various genotypes for these loci.
Restriction fragment length polymorphism (RFLP) and simple sequence length polymorphism (SSLP) markers have been used in many species to identify the locations of various kinds of genes. It seems that they are quite helpful in the linkage analysis of heading-time genes. Actually, RFLP can be seen in large numbers between indica and japonica rices (McCouch et al., 1988; Kurata et al., 1994). But it is rarely seen among japonica cultivars (Zhang et al., 1992), comparable to the case of the present study. Recently genetically mapped SSLPs have covered almost the whole genome of rice (Temnykh et al., 2000) and the frequency of SSLP at one locus is much higher than that of RFLP (Wu and Tanksley, 1993). But SSLP is also rarely seen among genetically close japonica rices (Akagi et al., 1997). Therefore, we could not use RFLP and SSLP for the allelism test of the mutant gene.
Heading time of rice is determined chiefly by the duration of the BVG period and photoperiod sensitivity (Hosoi, 1981; Vergara and Chang, 1985; Tanisaka et al., 1992). A recently established breeding program aims to produce cultivars with a long BVG period and weak photoperiod sensitivity. Such cultivars will show almost constant vegetative growth periods under different photoperiods, and thereby permit double or triple cropping in the lower latitudes. The mutant gene ef1-h, identified in the present study, confers a long BVG period without the aid of Se1-e; therefore, this novel gene will be quite useful in rice breeding to develop suitable cultivars in the low latitudes.
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ACKNOWLEDGMENTS
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We are grateful to Dr. Masao Yokoo, Dr. Kuo-Hai Tsai, and Dr. Nobuo Iwata for kindly providing ER and LR, T65 and T65Ef1, and NT lines, respectively. This work was funded by the Ministry of Education, Science, Sports and Culture, Japan.
Received for publication March 2, 2001.
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REFERENCES
|
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- Akagi, H., Y. Yokozeki, A. Inagaki, and T. Fujimura. 1997. Highly polymorphic microsatellites of rice consist of AT repeats, and a classification of closely related cultivars with these microsatellite loci. Theor. Appl. Genet. 94:61–67.
- Burnham, C.R. 1962. Discussions in cytogenetics. Burgess, Minneapolis, MN.
- Collinson, S.T., R.H. Ellis, R.J. Summerfield, and E.H. Roberts. 1992. Durations of the photoperiod-sensitive and photoperiod-insensitive phases of development to flowering in four cultivars of rice (Oryza sativa L.). Ann. Bot. (London) 70:339–346.[Abstract/Free Full Text]
- Glaszmann, J.C., B.G. de los Reyes, and G.S. Khush. 1988. Electrophoretic variation of isozymes in plumules of rice (Oryza sativa L.) - A key to the identification of 76 alleles at 24 loci. IRRI Res. Paper Series No. 134. IRRI, Manila, the Philippines.
- Haldane, J.B.S. 1930. Theoretical genetics of autopolyploids. J. Genet. 22:359–372.
- Hosoi, N. 1981. Studies on meteorological fluctuation in the growth of rice plants. V. Regional differences of thermo-sensitivity, photo-sensitivity, basic vegetative growth and factors determining the growth duration of Japanese varieties. (In Japanese, with English abstract.) Jpn. J. Breed. 31:239–250.
- Ichitani, K., Y. Okumoto, and T. Tanisaka. 1998. Genetic analysis of low photoperiod sensitivity of rice cultivars from the northernmost regions of Japan. Plant Breed. 117:543–547.
- Inoue, H., H. Nishida, Y. Okumoto, and T. Tanisaka. 1998. Identification of an early heading time gene found in the Taiwanese rice cultivar Taichung 65. Breed. Sci. 48:103–108.
- Iwata, N., T. Omura, and M. Nakagahara. 1970. Studies on the trisomics in rice plants (Oryza sativa L.) I. Morphological classification of trisomics. Jpn. J. Breed. 20:230–236.
- Kurata, N., Y. Nagamura, K. Yamamoto, Y. Harushima, N. Sue, J. Wu, B.A. Antonio, A. Shomura, T. Shimizu, S-Y. Lin, T. Inoue, A. Fukuda, T. Shimano, Y. Kuboki, T. Toyama, Y. Miyamoto, T. Kirihara, K. Hayasaka, A. Miyao, L. Monna, H.S. Zhong, Y. Tamura, Z-X. Wang, T. Momma, Y. Umehara, M. Yano, T. Sasaki, and Y. Minobe. 1994. A 300 kilobase interval genetic map of rice including 883 expressed sequences. Nat. Genet. 8:365–372.[ISI][Medline]
- Levy, Y.Y., and C. Dean. 1998. The transition to flowering. Plant Cell 10:1973–1989.[Free Full Text]
- McCouch, S.R., G. Kochert, Z.H. Yu, Z.Y. Wang, G.S. Khush, W.R. Coffman, and S.D. Tanksley. 1988. Molecular mapping of rice chromosomes. Theor. Appl. Genet. 76:815–829.
- Ohshima, I., F. Kikuchi, K. Odaka, K. Nomura, K. Tamura, H. Kato, and R. Ikeda. 1996. Linkage analysis of a photoperiod-sensitive gene Se-1 with neighboring loci in rice. Intl. Rice Res. Notes 21:13.
- Okumoto, Y., and T. Tanisaka. 1997. Trisomic analysis of a strong photoperiod-sensitivity gene E1 in rice (Oryza sativa L.). Euphytica 95:301–307.
- Okumoto, Y., T. Tanisaka, and H. Yamagata. 1991. Heading-time genes of the rice varieties grown in south-west region in Japan. (In Japanese, with English abstract.) Jpn. J. Breed. 41:135–152.
- Okumoto, Y., T. Tanisaka, and H. Yamagata. 1992. Heading-time genes of the rice varieties grown in the Tohoku-Hokuriku region in Japan. (In Japanese, with English abstract.) Jpn. J. Breed. 42:121–135.
- Poonyarit, M., D.J. Mackill, and B.S. Vergara. 1989. Genetics of photoperiod sensitivity and critical daylength in rice. Crop Sci. 29:647–652.[Abstract/Free Full Text]
- Sato, S., I. Sakamoto, K. Shirakawa, and S. Nakasone. 1988. Chromosomal location of an earliness gene Ef1 of rice, Oryza sativa L. Jpn. J. Breed. 38:385–396.
- Simpson, G.G., A.R. Gendall, and C. Dean. 1999. When to switch to flowering. Annu. Rev. Cell Dev. Biol. 99:519–550.
- Tanisaka, T., H. Inoue, S. Uozu, and H. Yamagata. 1992. Basic vegetative growth and photoperiod sensitivity of heading-time mutants induced in rice. (In Japanese, with English abstract.) Jpn. J. Breed. 42:657–668.
- Temnykh, S., W.D. Park, N. Ayres, S. Cartinhour, N. Hauck, L. Lipovich, Y.G. Cho, T. Ishii, and S.R. McCouch. 2000. Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor. Appl. Genet. 100:697–712.[ISI]
- Thomas, B., and D. Vince-Prue. 1997. Photoperiodism in plants. Academic Press, London.
- Tsai, K.H. 1986. Gene loci and alleles controlling the duration of basic vegetative growth of rice. p. 339–349. In Rice genetics. IRRI, Manila, the Philippines.
- Vergara, B.S., and T.T. Chang. 1985. The flowering response of the rice plant to photoperiod. 4th ed. IRRI, Manila, the Philippines.
- Wu, K-S., and S.D. Tanksley. 1993. Abundance, polymorphism and genetic mapping of microsatellites in rice. Mol. Gen. Genet. 241:225–235.[ISI][Medline]
- Yamagata, H., Y. Okumoto, and T. Tanisaka. 1986. Analysis of genes controlling heading time in Japanese rice. p. 351–359. In Rice genetics. IRRI, Manila, the Philippines.
- Yamamoto, T., H. Lin, T. Sasaki, and M. Yano. 2000. Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny. Genetics 154:885–891.[Abstract/Free Full Text]
- Yano, M., Y. Harushima, Y. Nagamura, N. Kurata, Y. Minobe, and T. Sasaki. 1997. Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor. Appl. Genet. 95:1025–1032.[ISI]
- Yokoo, M., and F. Kikuchi. 1982. Monogenic control of basic vegetative phase and photoperiod-sensitive phase in rice. (In Japanese, with English abstract.) Jpn. J. Breed. 32:1–8.
- Yokoo, M., and F. Kikuchi. 1992. The Lm locus controlling photoperiod sensitivity in rice differs from E1, E2 and E3 loci. (In Japanese, with English abstract.) Jpn. J. Breed. 42:375–381.
- Zhang, Q., M.A. Saghai Maroof, T.Y. Lu, B.Z. Shen. 1992. Genetic diversity and differentiation of indica and japonica rice detected by RFLP analysis. Theor. Appl. Genet. 83:495–499.
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