Responses of earliness and lateness genes for heading to different photoperiods, and specific response of a gene or a pair of genes to short day length in rice

BackgroundHeading time is an important trait for regional and seasonal adaptabilities in rice, and is controlled by genetic factors in relation with environmental factors, mainly day length and temperature. The following genes controlling heading were examined for their responses to six different environmental conditions involving different day lengths using five early near-isogenic lines (NILs) of T65-R and three late NILs of T65wx: two earliness genes, Ef1 and Efx controlling basic vegetative phase (BVG), and m-Ef1, the enhancer to the former gene; and two lateness genes, Se1-pat(t) and se-pat controlling photo-sensitivity and BVG, respectively. T65-R and T65-T were different accessions of Taichung 65. T65wx is a NIL of T65-T carrying wx.ResultsThe five early NILs of T65-R were in the order of ER50 (Ef1, Efx, m-Ef1) < ER40 (Ef1, m-Ef1) ≤ ER20 (Ef1, Efx) < ER1 (Ef1) ≤ ER21 (Efx) < T65-R regarding days to heading (DTH) under two spring-sowing and one summer-sowing paddy field (PF) conditions. The three late NILs of T65wx were in the order of LF3 (Se1-pat(t)) ≤ LF2 (Se1-pat(t), se-pat) ≤ T65wx < LF1 (se-pat) under two short-day conditions (10-h photoperiod condition with artificial-light and natural short-day condition from autumn to winter). The NILs and T65wx were in the order of T65wx < LF3 < LF1 < LF2 under the two spring-sowing PF (long day) conditions. T65-R (Ac-ef1) was 2.8 or 5.1 days earlier in DTH than T65-T (ac-ef1) under the two spring-sowing PF conditions. However, T65-R was 19 and 10 days earlier than T65-T under the two short-day conditions.ConclusionsEarliness gene(s) and their combinations reduced DTH regardless of photoperiod lengths. Se1-pat(t) increased DTH under long-day conditions but decreased it under short-day conditions, while se-pat elongated DTH under both short-day and long-day conditions indicating that se-pat is responsible for BVG. The se-pat increased DTH by adding its effect over that of Se1-pat(t) under long-day conditions. However, this increasing effect of DTH by se-pat was almost completely masked when it coexisted with Se1-pat(t) under the short-day conditions. Notably, the response of Ac-ef1 to day length was found to delay heading under the short-day conditions.

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title: Heading-Time Genes of the Rice Varieties Grown in South-West-Warm Region in Japan
abstract: Many genetic studies have so far revealed a number of genes responsible for heading-time of rice. However, the knowledge about these respective genes has yet been of little use for actual breeding program. For saving this situation, it is necessary to detect and identify the genes controlling the heading-time of presently grown varieties, to clarify the relationships among known, detected and identified genes, and thus to systematize the information about heading-time genes. From these points of view, gene analysis of the heading time of Japanese rice varieties was undertaken with the aid of 7 tester lines named EG lines, which are different from one another in the genotype for three late-heading-time genes E1. E2 and E3.

title: The flowering response of the rice plant to photoperiod : a review of the literature
abstract: Photoperiod influences several aspects of plant growth. Some of its effects on rices have been reviewed by Best (24), Gwinner (111), Katayama (192), Morinaga (316), Sircar (439), and Wagenaar (534). This review is primarily concerned with the effect of photoperiod on the flowering of the rice plant. It includes more than 500 papers on the photoperiodism of rice, most of which are available at the 
International Rice Research Institute library. Several contributions in Japanese have been translated into English and also are available at the International Rice 
Research Institute library. A bibliography is given at the end of this review; not all papers listed were cited in this review but were nevertheless included as future 
references for interested workers

title: Developmental changes of phyllochron in near-isogenic lines of rice (Oryza sativa L.) with different growth durations
abstract: The repeated elements called phytomers, which consist of leaf, node, internode and axillary bud, play an important role in the development of modular organization in plants. Rice has the striking feature that the rate of the phytomer production is closely synchronized with the rate of leaf emergence (phyllochron). We examined developmental changes of phyllochron by using 10 near-isogenic lines (NILs) showing diversified growth durations in rice. The NILs were established by backcrosses with a strain practically insensitive to photoperiod, and they consisted of early- or late-flowering NILs whose differences of growth duration were caused by the combinations of alleles at 6 loci. The developmental patterns of phyllochron were evaluated by means of a quartic polynomial, which fitted well in most cases. The results indicated that phyllochron greatly changed during development, especially in late-flowering NILs as well as the recurrent parents, although the fluctuation of phyllochron was not so marked in the early-flowering NILs. Thus, the developmental change of phyllochron was highly dependent upon the genotypes and/or growth duration; however, it was associated with neither floral initiation nor temperature, indicating that the change of phyllochron might reflect internal or physiological changes which occur during the life cycle of rice.

title: Thermo-sensitive action of an earliness gene Ef-x in rice, Oryza sativa L.
abstract: An extremely early line of rice, T65·ER-20, was bred after 8 times of backcrossings, using two early heading lines, Kokusyokuto-2 harboring several unknown earliness genes besides the earliness gene Ef-1 as a donor parent of earliness genes, and an isogenic line of Taichung 65 (T65) harboring the Ef-1 gene (T65·ER-1) as a recurrent parent. Since extremely early and early individuals segregated in a 3:1 ratio in the B8F2 generation and in a 1:1 ratio in the B9F1, T65·ER-20 harbors a new dominant earliness gene, Ef-x, besides the Ef-1 gene. T65·ER-21 having the new earliness gene was also bred. Segregation mode for heading time in F2 plants showing disgenic segregation for two earliness genes, Ef-1 and Ef-x, was different between experiments conducted in the natural field and in the green house field. Extremely early, early and late individuals segregated in a 9:3:4 ratio in the former and in a 9:6:1 ratio in the latter. Then, the Ef-x gene was asserted to show an allele specific interaction to genes on the Ef-1 locus, and an action for earliness by itself was accelerated in the high temperature condition. A screening test surveying a chromosome carrying the Ef-x gene by the use of 40 RT-lines implied that it located on the second chromosome.

title: STUDIES ON EARLINESS GENES IN RICE, WITH SPECIAL REFERENCE TO ANALYSIS OF ISOALLELES AT THE E LOCUS
abstract: By recurrent backcrossing continued up to the B20 generation, isogenic lines with earliness genes were established. A pure line of a rice variety, Taichung 65 (abridged as T65, Japonica type, insensitive to photoperiod) was exclusively used as the recurrent parent; two early maturing cultivars from northern China (A) and northern Japan (B) and two radiation-induced early-maturing mutant lines of T65 were each used as the donor parent. The results of crossing experiments with those isogenic lines demonstrated that the earliness genes from different donor parents were at the same locus on the 8th chromosome (symbolized E), and similarly moved up the time of floral initiation about 7 days and shortened the period from floral initiation to heading by about 3 days. However, when the lines with different E alleles were compared in more detail, they showed significant differences. Evidence was produced showing that the E locus would be a region containing several recombinationary separable subloci and when the “suballeles” were combined in cis form, complementation would restore the function of an E allele. There could also be an element suppressing the function of the whole region and making the recessive allele, e, carried by T65; its mutation may result in induction of dominant E alleles. Slight but significant changes in the effect of E alleles were observed when the isogenic lines were “purified” by backcrossing. Further, isogenic lines having a modifier gene at an independent locus, m, were investigated. The m gene intensified the effect of E alleles, the magnitude of the epistatic effect differing according to E alleles. When combined with e, the m gene had no effect in summer, but promoted heading several days in the winter season. There can be other modifier genes than m exerting a buffering effect when recombined. A summary of earlier papers on these earliness genes was presented in addition.

title: Analysis of a Rice Variety Taichung 65 and its Isogenic Early-heading Lines for Late-heading Genes E1, E2and E3
abstract: The objective of this study is to systematize the information about the genes controlling heading time in rice through gene analysis using seven tester lines (EG Iines, , which differ from one another in the genotype for three late-heading genes, E1, E2 and E3. In this paper, the third report of the study, a Ponlai (or Horai) variety Taichung 65 and five derivatives which are each isogenic to the variety for one of two early-heading genes, Ef-1 and m-Ef-1, were used as the materials. These six lines (T Iines, Table 1) were crossed each with the seven EG Iines, and analyzed for the allelic relations of Ef-1 and m-Ef-1 to E1. E2 and E3 based on the segregations in the F2 and F3 generations.

title: Fine Mapping and Characterization of Quantitative Trait Loci Hd4 and Hd5 Controlling Heading Date in Rice.
abstract: Fine mapping of Hd4 and Hd5, quantitative trait loci (QTLs) for heading date in rice, was performed by using advanced backcross progeny derived from a cross between a japonica rice variety, Nipponbare, and an indica variety, Kasalath. Hd4 was mapped between restriction fragment length polymorphism (RFLP) markers R46 and C39 in the proximal region of chromosome 7, and Hd5 was mapped between C166 and R902 on the short arm of chromosome 8; both QTLs mapped as single Mendelian factors. We used marker-assisted selection to develop two nearly isogenic lines (NIL), designated NIL(Hd4) and NIL(Hd5), in which small chromosomal segments of Kasalath including Hd4 and Hd5, respectively, each were substituted into the genetic background of Nipponbare. Compared with that of Nipponbare, days-to-heading of NIL(Hd4) and NIL(Hd5) increased under long-day and natural-field conditions, but no differences were observed between those of the two NILs and Nipponbare under short-day conditions. Epistatic interaction was detected between Hd5 and Hd1, a key photoperiod sensitivity QTL, on the basis of an analysis of the F2 population derived from a cross between the NIL(Hd5) and NIL(Hd1). This result suggests that Hd5 is involved in photoperiod sensitivity and may act downstream or upstream of Hd1 in the same photoperiodic pathway. In comparison, the genetic effect of Hd5 was additive to that of Hd2, another key photoperiod-sensitivity QTL, indicating that Hd2 acts in a different photoperiodic pathway other than that of Hd1 and Hd5. The genetic effect of Hd4 was additive to those of Hd1 and Hd2; thus, epistatic interaction between these loci was not detected.

title: Dissection of a major QTL for photoperiod sensitivity in rice: its association with a gene expressed in an age-dependent manner
abstract: A proposed major quantitative trait locus (QTL) for photoperiod sensitivity on chromosome 6 in rice was examined by introducing a chromosomal segment from a sensitive line into an insensitive one. The crossing experiments showed that a range of variation in heading date occurred in the later generations and that the region might contain at least a major gene and two additional recessive genes controlling photoperiod sensitivity. Gene mapping experiments showed that the major gene was Se-1 and that a recessive gene (tentatively named se-pat) was loosely linked to it. The responses to photoperiods were examined among the different genotypes under natural and controlled conditions. The two genes acted additively on the degree of photoperiod sensitivity. However, se-pat plants showed a response to photoperiods that differed from that of the other sensitive lines; a short-day treatment at the seedling stage delayed heading in the former plants, suggesting that the manner of its expression was age-dependent. A recessive gene similar to se-pat seemed to be widely distributed in wild and cultivated rice, suggesting that the gene complex in the region plays a significant role in response to photoperiod.

title: Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars
abstract: The rice japonica cultivars Nipponbare and Koshihikari differ in heading date and response of heading to photoperiod (photoperiod sensitivity). Using simple sequence repeat (SSR) and single nucleotide polymorphism (SNP) markers, we conducted quantitative trait locus (QTL) analyses for heading date in a set of reciprocal backcross inbred lines (BILs) from crosses between Nipponbare and Koshihikari. Under natural-day conditions, transgressive segregation in days to heading (DTH) toward both early and late heading was observed in both BIL populations. QTL analyses revealed that two QTLs—on chromosomes 3 and 6—were involved in the difference in heading date between the parental cultivars. The Nipponbare allele at the QTLs on chromosomes 3 and 6 showed, respectively, increasing and decreasing effects on DTH in both BIL populations. The transgressive segregation observed in the BILs could be accounted for mainly by the complementary action of a set of alleles with opposing effects. Both QTLs were finely mapped as single Mendelian factors in secondary mapping populations (BC2F2 plants/BC2F3 lines). The QTL on chromosome 3 was mapped in the 1,140-kb interval between 94O03-4 (SSR) and OJ21G19-4 (SNP) and was designated Hd16. The QTL on chromosome 6 was mapped in the 328-kb interval between P548D347 (SSR) and 0007O20 (SSR) and was designated Hd17. Both Hd16 and Hd17 were involved in photoperiod sensitivity, as revealed by observation of the DTH of nearly isogenic lines of Nipponbare under short- and long-day conditions, suggesting that allelic differences in both Hd16 and Hd17 account for most of the difference in photoperiod sensitivity between the parental cultivars.

title: Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map
abstract: Quantitative trait locus (QTL) analysis has been carried out to identify genes conferring heading date in rice. One hundred and eighty six F2 plants derived from a cross between a japonica variety, Nipponbare, and an indica variety, Kasalath, were used as a segregating population for QTL mapping and more than 850 markers were employed to identify QTLs. Scan-analysis revealed the existence of two QTLs with large effects, Hd-1 and Hd-2, one in the middle of chromosome 6 and one at the end of chromosome 7, respectively. For both loci, the Kasalath alleles reduced days-to-heading. In addition, three QTLs with minor effects, Hd-3, Hd-4 and Hd-5, were found to be located on chromosomes 6, 7 and 8 based on a secondary scan analysis which was carried out by removing the phenotypic effects of Hd-1 and Hd-2. For the three secondary loci, the Nipponbare alleles reduced days-to-heading. The five QTLs explained 84% of the total phenotypic variation in the F2 population based on a multiple-QTL model. The presence of a digenic interaction between Hd-1 and Hd-2 was clearly suggested.

title: Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines
abstract: To characterize quantitative trait loci (QTLs), we used marker-assisted selection (MAS) to develop three nearly isogenic lines (NILs) differing only for the presence of a single, specific QTL (QTL-NILs) –Hd1, Hd2, and Hd3 – for heading date in rice. The three lines contained the chromosomal region of the target QTL from donor variety Kasalath(indica) in the genetic background of var. Nipponbare (japonica). To analyze epistatic interactions in pairs of these QTLs, we also used MAS to develop four combined QTL-NILs with 2 of the 3 QTLs or with all 3. Different daylength treatment testing of the QTL-NILs revealed that the three QTLs control photoperiod sensitivity. Genetic analysis of F2 populations derived from crosses between the three QTL-NILs with a single QTL using molecular markers revealed the existence of epistatic interactions between Hd1 and Hd2, and Hd2 and Hd3. These interactions were also confirmed by the analysis of combined QTL-NILs under different daylength conditions. The existence of an epistatic interaction between Hd1 and Hd3 was also clarified. Based on these results, we suggest that the Kasalath allele of Hd3 does not affect photoperiod sensitivity by itself but that it is involved in enhancement of the expression of the Nipponbare alleles of Hd1 and Hd2.

title: Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions
abstract: Heading date is the one of the most important traits in rice breeding, because it defines where rice can be cultivated and influences the expression of various agronomic traits. To examine the inhibition of heading by Heading date 2 (Hd2), previously detected on the distal end of chromosome 7’s long arm by quantitative trait locus (QTL) analysis, we developed backcross inbred lines (BILs) from Koshihikari, a leading Japanese cultivar, and Hayamasari, an extremely early heading cultivar. The BILs were cultivated under natural field conditions in Tsukuba Japan, and under long-day (14.5 h), extremely long-day (18 h), and short-day (10 h) conditions. Combinations of several QTLs near Hd1, Hd2, Ghd7, Hd5, and Hd16 were detected under these four conditions. Analysis of advanced backcross progenies revealed genetic interactions between Hd2 and Hd16 and between Hd2 and Ghd7. In the homozygous Koshihikari genetic background at Hd16, inhibition of heading by the Koshihikari allele at Hd2 was smaller than that with the Hayamasari Hd16 allele. Similarly, in the homozygous Koshihikari genetic background at Ghd7, the difference in heading date caused by different alleles at Hd2 was smaller than in plants homozygous for the Hayamasari Ghd7 allele. Based on these results, we conclude that Hd2 and its genetic interactions play an important role in controlling heading under long-day conditions. In addition, QTLs near Hd2, Hd16, and Ghd7, which are involved in inhibition of heading under long-day conditions, function in the same pathway that controls heading date.

title: Tight Linkage of Blast-Resistance with Late Maturity Observed in Different Indica Varieties of Rice
abstract: A tight linkage between blast-resistance and late maturity with a recombination value of 3.5±0.5% was observed in the progenies of several different japonica ×indica crosses in rice. The blast-resistance in the sixcrosses was controlled by the identical gene Pi-zt and the lateness in maturity was due to a photoperiod-sensitive gene. These two genes were linked with the genes for apiculus color and for digestibility of milled rice in dilute alkali, and were located in the linkage group I in rice. The significance of the tight linkage in practical rice breeding was discussed.

title: Multiple Allelism of the Locus Controlling Heading Time of Rice, Detected Using the Close Linkage with Blast-Resistance
abstract: A genetic experiment was conducted to detect the multiple allelism of the locus controlling heading time in rice, with the aid of the close linkage with resistance to blast disease. Frve vaneties were used as parents "Fujisaka 5" was early-maturing, "Norin 8" "Toride 1" and "J 287" were medium and "J 315" was late FuJisaka 5 and Norin 8 are Japanese vaneties. The last three lines were developed from the cross between Norin 8 and an Indian variety "TKM.1" by the backcross breedmg program, and they had the Pi-zt gene for blast resistance that was derived from TKM. 1 (NAGAI et al. 1970). Nine crosses were made between the parents, and the heading date of F1 and F2 plants was recorded in the field. The F3 family of each F2 plant was tested for resistance to the Ken 53-33 strain of blast fungus to estimate the F2 genotype for the Pi-zt gene, , In the six crosses segregating for resistance to Ken 53-33, the Pi-zt gene was confirmed to control resistance of the hybrid populations (Table 1).

title: Hd1, a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS
abstract: A major quantitative trait locus (QTL) controlling response to photoperiod, Hd1, was identified by means of a map-based cloning strategy. High-resolution mapping using 1505 segregants enabled us to define a genomic region of ∼12 kb as a candidate for Hd1. Further analysis revealed that the Hd1 QTL corresponds to a gene that is a homolog of CONSTANS in Arabidopsis. Sequencing analysis revealed a 43-bp deletion in the first exon of the photoperiod sensitivity 1 (se1) mutant HS66 and a 433-bp insertion in the intron in mutant HS110. Se1 is allelic to the Hd1 QTL, as determined by analysis of two se1 mutants, HS66 and HS110. Genetic complementation analysis proved the function of the candidate gene. The amount of Hd1 mRNA was not greatly affected by a change in length of the photoperiod. We suggest that Hd1 functions in the promotion of heading under short-day conditions and in inhibition under long-day conditions.

title: Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice
abstract: Rice is a facultative short-day plant, and molecular genetic studies have identified the major genes involved in short-day flowering. However, the molecular mechanisms promoting the diversity of flowering time in cultivated rice are not known. We used a core collection of 64 rice cultivars that represent the genetic diversity of 332 accessions from around the world and studied the expression levels and polymorphisms of 6 genes in the short-day flowering pathway. The RNA levels of Heading date 3a (Hd3a), encoding a floral activator, are highly correlated with flowering time, and there is a high degree of polymorphism in the Heading date 1 (Hd1) protein, which is a major regulator of Hd3a expression. Functional and nonfunctional alleles of Hd1 are associated with early and late flowering, respectively, suggesting that Hd1 is a major determinant of variation in flowering time of cultivated rice. We also found that the type of Hd3a promoter and the level of Ehd1 expression contribute to the diversity in flowering time and Hd3a expression level. We evaluated the contributions of these 3 factors by a statistical analysis using a simple linear model, and the results supported our experimental observations.

title: Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars
abstract: To dissect the genetic factors controlling naturally occurring variation of heading date in Asian rice cultivars, we performed QTL analyses using F2 populations derived from crosses between a japonica cultivar, Koshihikari, and each of 12 cultivars originating from various regions in Asia. These 12 diverse cultivars varied in heading date under natural field conditions in Tsukuba, Japan. Transgressive segregation was observed in 10 F2 combinations. QTL analyses using multiple crosses revealed a comprehensive series of loci involved in natural variation in flowering time. One to four QTLs were detected in each cross combination, and some QTLs were shared among combinations. The chromosomal locations of these QTLs corresponded well with those detected in other studies. The allelic effects of the QTLs varied among the cross combinations. Sequence analysis of several previously cloned genes controlling heading date, including Hd1, Hd3a, Hd6, RFT1, and Ghd7, identified several functional polymorphisms, indicating that allelic variation at these loci probably contributes to variation in heading date. Taken together, the QTL and sequencing results indicate that a large portion of the phenotypic variation in heading date in Asian rice cultivars could be generated by combinations of different alleles (possibly both loss- and gain-of-function) of the QTLs detected in this study.

title: Diversification in flowering time due to tandem FT‐like gene duplication, generating novel Mendelian factors in wild and cultivated rice
abstract: The complex structure of a single Mendelian factor widespread in the Asian cultivated rice (Oryza sativa) and its wild progenitor (Oryza rufipogon) that caused diverse phenotypes in the timing of flowering under natural field conditions was investigated in near isogenic lines. These near isogenic lines showed differences in flowering time despite all eight accessions collected from tropical regions possessing a recessive gene allelic to the se‐pat gene. Fine mapping in two of these near‐isogenic lines revealed that cultivated (Patpaku) and wild (W593) accessions had three and two linked quantitative trait loci (QTL) in the candidate regions, respectively, showing that Patpaku and W593 possessed linked QTLs with different effects in addition to the commonly‐observed recessive gene (se‐pat). Molecular dissection suggested that the tandemly duplicated FT‐like genes (Hd3a and RFT1) could be the candidate genes for these QTLs. Interestingly, the linked QTLs differed in their epistases, degree of dominance, and genotype × environment interactions. The nucleotide sequences showed that RFT1 has diverged more rapidly than Hd3a during rice evolution, suggesting phenotypic diversification of the two genes. Phylogenetic analysis implied that the se‐pat+ alleles might have emerged in different lineages within O. sativa. The present results strongly suggest that nucleotide divergence and shuffling of the linked QTLs by recombination might have created novel Mendelian factors that probably contribute to responding to local environments.

title: Monogenic Control of Basic Vegetative Phase and Photoperiod-sensitive Phase in Rice
abstract: Lm which belongs to the linkage group I is one of the primary loci controlling heading time of cultivated rice and is also associated with photoperiod sensitivity. The effects of alleles of the Lm locus on two phases of the vegetative growth duration, the basic vegetative phase and the photoperiod-sensitive phase, were analysed by growing two isogenic lines with Lme and Lmu allelles under natural and controlled daylengths. Heterozygotes (Lme/Lmu) were maintained during 15 generations Lrom F1 through BC4F11 in the cross between the Malaysian cultivar Morak Sepilai and the Japanese cultivar Fujisaka 5, which was used as the recurrent parent for the successive four backcrosses. Fujisaka 5 and Morak Sepilai transmitted the early-maturing allele Lme and the late-maturing allele Lmu to their hybrid progenies, respectively.

title: Epistasis among the three major flowering time genes in rice: coordinate changes of photoperiod sensitivity, basic vegetative growth and optimum photoperiod
abstract: Flowering time is affected not only by photoperiod sensitivity (PS) but also by basic vegetative growth (BVG) and optimum photoperiod (OP), although their developmental and genetic relationships are not well understood. The present study was carried out in rice to examine to what extent these three developmental components are modified by the three flowering time genes, Se1 (= Hd1), Ef1 and e1 (= m-Ef1), which are known to contribute to flowering time in temperate and tropical regions of rice cultivation. Photoperiodic response curves were estimated under controlled conditions of different growth regimes, using eight near-isogenic lines possessing different combinations of the alleles at the three loci. The results showed that each of the components is greatly affected by the main effect of the genes, temperature and their epistasis, indicating that none of the three genes controls flowering time by altering any single component in PS, BVG or OP. Epistasis was detected more frequently among the three genes than reported before, suggesting that epistasis contributes to flowering time by changing PS, BVG and OP differently. The comparison of the nucleotide sequences suggested that Ef1 is the same as Early heading date 1 (Ehd1). Since the two genes Se1 (= Hd1) and Ef1 (= Ehd1) are known to up-regulate the rice homolog of ArabidopsisFT, it is suggested that the detected epistasis may respond to diverse environments by modulating the CO/FT system conserved in flowering plants.

title: Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes.
abstract: Heading date and photoperiod sensitivity are fundamental traits that determine rice adaptation to a wide range of geographic environments. By quantitative trait locus (QTL) mapping and candidate gene analysis using whole-genome re-sequencing, we found that Oryza sativa Pseudo-Response Regulator37 (OsPRR37; hereafter PRR37) is responsible for the Early heading7-2 (EH7-2)/Heading date2 (Hd2) QTL which was identified from a cross of late-heading rice 'Milyang23 (M23)' and early-heading rice 'H143'. H143 contains a missense mutation of an invariantly conserved amino acid in the CCT (CONSTANS, CO-like, and TOC1) domain of PRR37 protein. In the world rice collection, different types of nonfunctional PRR37 alleles were found in many European and Asian rice cultivars. Notably, the japonica varieties harboring nonfunctional alleles of both Ghd7/Hd4 and PRR37/Hd2 flower extremely early under natural long-day conditions, and are adapted to the northernmost regions of rice cultivation, up to 53° N latitude. Genetic analysis revealed that the effects of PRR37 and Ghd7 alleles on heading date are additive, and PRR37 down-regulates Hd3a expression to suppress flowering under long-day conditions. Our results demonstrate that natural variations in PRR37/Hd2 and Ghd7/Hd4 have contributed to the expansion of rice cultivation to temperate and cooler regions.

title: Hd3a and RFT1 are essential for flowering in rice
abstract: RICE FLOWERING LOCUS T 1 (RFT1/FT-L3) is the closest homologue of Heading date 3a (Hd3a), which is thought to encode a mobile flowering signal and promote floral transition under short-day (SD) conditions. RFT1 is located only 11.5 kb from Hd3a on chromosome 6. Although RFT1 RNAi plants flowered normally, double RFT1-Hd3a RNAi plants did not flower up to 300 days after sowing (DAS), indicating that Hd3a and RFT1 are essential for flowering in rice. RFT1 expression was very low in wild-type plants, but there was a marked increase in RFT1 expression by 70 DAS in Hd3a RNAi plants, which flowered 90 DAS. H3K9 acetylation around the transcription initiation site of the RFT1 locus had increased by 70 DAS but not at 35 DAS. In the absence of Hd3a and RFT1 expression, transcription of OsMADS14 and OsMADS15, two rice orthologues of Arabidopsis APETALA1, was strongly reduced, suggesting that they act downstream of Hd3a and RFT1. These results indicate that Hd3a and RFT1 act as floral activators under SD conditions, and that RFT1 expression is partly regulated by chromatin modification.

title: A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice
abstract: Although some genes that encode sensory or regulatory elements for photoperiodic flowering are conserved between the long-day (LD) plant Arabidopsis thaliana and the short-day (SD) plant rice, the gene networks that control rice flowering, and particularly flowering under LD conditions, are not well understood. We show here that RICE FLOWERING LOCUS T 1 (RFT1), the closest homolog to Heading date 3a (Hd3a), is a major floral activator under LD conditions. An RFT1:GFP fusion protein localized in the shoot apical meristem (SAM) under LD conditions, suggesting that RFT1 is a florigen gene in rice. Furthermore, mutants in OsMADS50, a rice ortholog of Arabidopsis SUPPRESOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) did not flower up to 300 days after sowing under LD conditions, indicating that OsMADS50, which acts upstream of RFT1, promotes flowering under LD conditions. We propose that both positive (OsMADS50 and Ehd1) and negative (Hd1, phyB and Ghd7) regulators of RFT1 form a gene network that regulates LD flowering in rice. Among these regulators, Ehd1, a rice-specific floral inducer, integrates multiple pathways to regulate RFT1, leading to flowering under appropriate photoperiod conditions. A rice ortholog of Arabidopsis APETALA1, OsMADS14, was expressed in the floral meristem in wild-type but not in RFT1 RNAi plants, suggesting that OsMADS14 is activated by RFT1 protein in the SAM after the transition to flowering. We have thus exposed a network of genes that regulate LD flowering in rice.

title: Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions.
abstract: Heading date 3a (Hd3a) has been detected as a heading-date-related quantitative trait locus in a cross between rice cultivars Nipponbare and Kasalath. A previous study revealed that the Kasalath allele of Hd3a promotes heading under short-day (SD) conditions. High-resolution linkage mapping located the Hd3a locus in a approximately 20-kb genomic region. In this region, we found a candidate gene that shows high similarity to the FLOWERING LOCUS T (FT) gene, which promotes flowering in Arabidopsis: Introduction of the gene caused an early-heading phenotype in rice. The transcript levels of Hd3a were increased under SD conditions. The rice Heading date 1 (Hd1) gene, a homolog of CONSTANS (CO), has been shown to promote heading under SD conditions. By expression analysis, we showed that the amount of Hd3a mRNA is up-regulated by Hd1 under SD conditions, suggesting that Hd3a promotes heading under the control of Hd1. These results indicate that Hd3a encodes a protein closely related to Arabidopsis FT and that the function and regulatory relationship with Hd1 and CO, respectively, of Hd3a and FT are conserved between rice (an SD plant) and Arabidopsis (a long-day plant).

title: Natural Variation of the RICE FLOWERING LOCUS T 1 Contributes to Flowering Time Divergence in Rice
abstract: In rice (Oryza sativa L.), there is a diversity in flowering time that is strictly genetically regulated. Some indica cultivars show extremely late flowering under long-day conditions, but little is known about the gene(s) involved. Here, we demonstrate that functional defects in the florigen gene RFT1 are the main cause of late flowering in an indica cultivar, Nona Bokra. Mapping and complementation studies revealed that sequence polymorphisms in the RFT1 regulatory and coding regions are likely to cause late flowering under long-day conditions. We detected polymorphisms in the promoter region that lead to reduced expression levels of RFT1. We also identified an amino acid substitution (E105K) that leads to a functional defect in Nona Bokra RFT1. Sequencing of the RFT1 region in rice accessions from a global collection showed that the E105K mutation is found only in indica, and indicated a strong association between the RFT1 haplotype and extremely late flowering in a functional Hd1 background. Furthermore, SNPs in the regulatory region of RFT1 and the E105K substitution in 1,397 accessions show strong linkage disequilibrium with a flowering time–associated SNP. Although the defective E105K allele of RFT1 (but not of another florigen gene, Hd3a) is found in many cultivars, relative rate tests revealed no evidence for differential rate of evolution of these genes. The ratios of nonsynonymous to synonymous substitutions suggest that the E105K mutation resulting in the defect in RFT1 occurred relatively recently. These findings indicate that natural mutations in RFT1 provide flowering time divergence under long-day conditions.

title: Two Distinct Growth Types for Number of Developed Leaves, Heading Time, Culm and Panicle Lengths, and Internode Length within Near-isogenic Lines of Rice
abstract: There are two growth types of plants for the number of developed leaves, heading time, and culm and panicle lengths within a population of a homozygous rice cultivar. However, this phenomenon has not been deeply investigated, because of lack of concrete data. Rice breeders and physiologists have paid little attention to it, regarding it as a genetically uncontrollable environmental variation. To study more details of the phenomenon, we grew two near-isogenic lines of rice with each one of the alleles for the Sel locus conferring photoperiod sensitivity on chromosome 6 under natural long and short day-length conditions. In the line ER homozygous for the earliness allele Sel-e, and the line LR with the lateness allele Sel-u, N-leaf plants headed several days earlier than N+1-leaf plants. The N-leaf plants had shorter culms and longer panicles and were the upper-intemode elongation type, whereas the N+1-leaf plants had opposite values of these characters. The proportion of these two kinds of plants changed in lines, plots and experiments. We discuss the meanings of this phenomenon from the viewpoints of rice cultivation to attain the uniform growth of plants, breeding to select individual plants with environmental variation, and fixation test to evaluate the uniformity needed as a cultivar.