JXB Advance Access published online on August 9, 2007
Journal of Experimental Botany, doi:10.1093/jxb/erm159
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
FOCUS PAPER |
Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice
National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan
* E-mail: tizawa{at}nias.affrc.go.jp
Received 23 April 2007; Revised 5 June 2007 Accepted 18 June 2007
 |
Abstract |
|---|
 Top Abstract IntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
The adaptation of plants to natural environments depends on the adaptation of flowering-time control at the appropriate season to set seeds. Possible molecular mechanisms underlying this adaptation have recently been revealed. In Arabidopsis thaliana, a model long-day plant, control of floral transition by vernalization and long-day floral promotion pathways is a key regulator in adaptation to different regions. A floral repressor termed FLC and a floral promoter termed CONSTANS (CO), which control FT, a florigen gene, are key transcriptional regulators of these pathways. Recent analyses of haplotypes in accessions of A. thaliana revealed that FLC regulation by an activator termed FRIGIDA (FRI) had been a target for natural selection. By contrast, in rice (Oryza sativa), a model short-day plant, two independent floral pathways—Heading date 1 (Hd1, a CO orthologue)-dependent and Early heading date 1 (Ehd1)-dependent pathways—control Hd3a (an FT orthologue) and flowering time. Interestingly, there is an antagonistic action between Hd1 and Ehd1 in the control of flowering time under long-day conditions, because Hd1 represses floral transition whereas Ehd1 promotes it. A wild rice species, Oryza rufipogon, has common ancestry with cultivated rice and grows wild in the tropics, yet cultivated rice is grown even in the cold regions of northern latitudes. During domestication, the adaptation of O. sativa to northern regions by artificial selection may have become possible through interactions of the two pathways. These suggest that the domestication process of rice will provide novel insights into the adaptation of plants in evolution.
Key words: Arabidopsis thaliana, Ehd1, Hd1, photoperiodic flowering, rice, vernalization
|
Introduction |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
The ability to find ecological niches and adapt to natural environments is a key strategy for the ecological prosperity of plants. Regulation of flowering time under given environments has long been understood to be involved in this adaptation. Molecular genetic analysis of floral regulation in Arabidopsis thaliana has provided critical clues to what kinds of genes have been the targets for natural selection in evolution. It is, however, noteworthy that the long history of plant species may make it difficult to get clear conclusions from analysis using Arabidopsis accessions, since the natural variations at DNA levels showed their complex nature.
The domestication of crops through adaptation under artificial selection during the last 10 000 years is a good example of evolutionary processes (Darwin, 1868). With the increasing availability of genome-wide information, the domestication of crops is becoming a good model for elucidating the elements of evolution, because changes in DNA among populations can be examined, and as they cannot be enormous its coalescent processes can be inferred. Recent molecular genetic studies and quantitative trait locus (QTL) analyses of flowering-time genes in rice have revealed several key genes involved in floral transition in the field and under laboratory conditions, and have provided enough information to allow the study of adaptation during the domestication of rice. The tremendous expansion in growing regions of cultivated rice to the north during the last several thousand years implies a strong impact of artificial selection during the domestication of rice. Analyses of flowering-time genes have given several hints to explain local adaptations in rice. There is no doubt that the study of rice domestication will provide many novel insights into the adaptation of plants in the near future.
|
Molecular mechanisms of flowering-time regulation of A. thaliana |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
A. thaliana has two forms of ecotype, winter-annual and summer-annual (or rapid cycler) ecotypes (Simpson and Dean, 2002; Henderson et al., 2003). Winter-annual plants flower in early spring after a long, cold winter, whereas summer-annual plants flower throughout spring and summer. Molecular genetics revealed that a transcriptional activator termed CONSTANS (CO) is a key regulator of floral promotion under long-day conditions (Putterill et al., 1995). CO functions as a transcriptional activator and promotes the expression of FT, an Arabidopsis florigen gene (Kardailsky et al., 1999; Kobayashi et al., 1999; Corbesier et al., 2007). Transcription of CO is regulated by both circadian clocks and acute light signals. GIGANTEA (GI) functions as both a component of circadian clocks and a mediator between CO and the circadian clocks in A. thaliana, and CO mRNA is transcribed mainly during the night (Suarez-Lopez et al., 2001; Mizoguchi et al., 2005). CO transcription is repressed by transcription factors such as CYCLING DOF FACTOR 1 (CDF1) (Imaizumi et al., 2005). CDF1 protein is degraded at dusk only under long-day conditions through an F-box gene termed FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) (Imaizumi et al., 2003). FKF1 is expressed by circadian clocks around dusk. FKF1 protein is believed to be a blue-light photoreceptor and to be activated by blue light signals. Therefore, FKF1 can activate CO transcription at dusk through CDF1 degradation only under long-day conditions. These transcription mechanisms can lead to a significant amount of CO mRNA accumulation at dusk under long-day conditions (Imaizumi et al., 2005). CO protein stability is also regulated by photoperiod (Valverde et al., 2004). Light signal transduction of blue and far-red light mediated by cryptochrome 2 and phytochrome A photoreceptors, respectively, stabilizes CO protein before dusk only under long-day conditions, in addition to preferred expression of CO at dusk regulated by GI and FKF1. Futhermore rapid degradation of CO protein is regulated by SPA under darkness and by PHYB in the morning (Valverde et al., 2004; Laubinger et al., 2006). These redundant regulations of CO activity make CO activate FT at dusk only under long-day conditions (Imaizumi and Kay, 2006). This mechanism may explain why summer-annual ecotypes of A. thaliana grow and flower throughout spring and summer under long-day conditions.
These mechanisms appear to be insufficient to explain the habit of winter-annual ecotypes, however. To explain this requires the introduction of molecular mechanisms for vernalization into floral regulation (Mylne et al., 2004; Sung and Amasino, 2005). A MADS box transcription factor termed FLC has been shown to be a key floral repressor of FT, which is responsible for vernalization response (Michaels and Amasino, 2001). FLC transcription is epigenetically repressed through a Polycomb complex including VERNALIZATION 2 protein after vernalization treatment (Gendall et al., 2001). By this mechanism, winter-annual plants germinate and grow in autumn but do not flower, owing to floral repression by FLC expression until a long, cold winter has passed. During winter, FLC is epigenetically repressed. In spring, when the photoperiod is lengthening, CO starts to activate FT, and winter-annual plants flower. This sequential regulation of FLC repression and CO activation of FT expression explains the winter-annual ecotype.
|
Natural variations associated with geographic distribution of Arabidopsis |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
The association of A. thaliana accessions with natural variations in flowering-time genes suggests that several such natural variations underlie ecological distribution (Alonso-Blanco et al., 2005; Ehrenreich and Purugganan, 2006). Extensive molecular analyses suggest that non-functional alleles of both FLC and FRIGIDA (FRI), an activator of FLC, underlie some summer-annual ecotypes (Johanson et al., 2000; Michaels et al., 2003). Several non-functional alleles of FRI are distributed widely among Arabidopsis accessions, suggesting that FRI has been a target of natural selection (Stinchcombe et al., 2004; Shindo et al., 2005). However, they are not associated with the latitudinal distribution of the accessions. Toomajian et al. (2006) suggested that two major non-functional alleles of FRI, FRICol and FRILer, were selected during the last few thousand years in association with the domestication of crops, perhaps by conferring weediness. This relatively recent spreading of these non-functional alleles and the possible dispersal of Arabidopsis genotypes with human migration could be the reason for the lack of clear association with the latitudinal distribution of the accessions.
By contrast, only the presence of functional alleles of FRI, two major FLC alleles, FLCA and FLCB, can explain some of the latitudinal distribution in Eurasia and North Africa. This offers very strong evidence that natural selection against natural variations in FLC produced the latitudinal cline. Therefore, the recent non-functionalization of FRI might result in rapid disturbance of the FLC-dependent latitudinal cline (Caicedo et al., 2004; Shindo et al., 2005, 2006). Therefore, some epistatic relationships between FRI and FLC can be speculated from the geographical distribution of Arabidopsis accessions, and these were consistent with analysis of flowering-time phenotypes of fri and flc mutants in the laboratory. These results suggest that diversification of FLC, but not FRI, is a major reason for adaptation to local areas (Fig. 1). There is still no good explanation for why non-functional alleles of FRI have not contributed to a latitudinal cline in Arabidopsis accessions. Loss of function of FRI may result in broader adaptability of A. thaliana than that permitted by FLC variations. Further study is required. The complex nature of natural selection for different flowering-time genes in Arabidopsis accessions along the latitudinal cline provides an example of evolution in plants. The evidence clearly indicates that the winter-annual ecotype is the default in A. thaliana. Therefore, it is possible that the emergence of summer-annual ecotypes has occurred repeatedly in the history of A. thaliana, and some ancient summer-annuals may have gone extinct.
|
In addition, natural variations in photoreceptor genes, such as CRYPTOCHROME 2 and PHYTOCHROME C (PHYC), are also involved in adaptation to local areas among Arabidopsis accessions (Olsen et al., 2004; Balasubramanian et al., 2006). In particular, natural variations in PHYC may partly explain the latitudinal cline. It is noteworthy that phyC is not required for long-day promotion of flowering in A. thaliana in the laboratory. Therefore, biological functions of phyC other than floral transition, such as growth control, may be involved in this adaptation. So far, there is no evidence that the long-day promotion pathway mediated by CO and GI has been a target for natural selection (Alonso-Blanco et al., 2005). Taken together, these results suggest that long-day floral promotion is not a critical factor in the adaptation of A. thaliana to local areas. Deficiencies in this long-day promotion pathway may cause mutations that are deleterious to the propagation of Arabidopsis, although it is noteworthy that the long-day floral pathway may not be essential for survival, because late-flowering mutants of gi are a kind of vital mutant in A. thaliana. Therefore, the role of natural variations in this pathway in Arabidopsis adaptation is still an open question.
|
Molecular mechanisms of flowering-time regulation in rice |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
Heading date 1 (Hd1) is one of the first flowering-time genes cloned from rice (Yano et al., 2000). Hd1 was originally identified as a QTL in crosses between two cultivars in different subspecies of cultivated rice, Kasalath (ssp. indica) and Nipponbare (ssp. japonica) (Yano and Sasaki, 1997; Yano et al., 2000, 2001). Recent works have revealed that these subspecies are likely to have evolved in at least two independent domestication processes (Vitte et al., 2004; Londo et al., 2006). Here, the Kasalath allele of Hd1 contains some null mutations in the coding region (Yano et al., 2000). Phylogenetic analysis revealed that Hd1 is a CO orthologue (Izawa et al., 2003). But, whereas CO promotes flowering under long-day conditions, Hd1 promotes it under short-day conditions and represses it under long-day conditions (Yano et al., 2000; Izawa et al., 2002, 2003). Hd3a, another QTL of flowering-time in rice is an FT orthologue and is regulated by Hd1 (Izawa et al., 2002; Kojima et al., 2002), and Hd3a protein functions as a florigen (Tamaki et al., 2007). These clues clearly indicate that the evolutionally conserved floral induction mechanism is involved in photoperiodic control of flowering in plants and has diversified among long-day and short-day species. Because CDF1 and FKF1 have homologues in rice, it is possible that Hd1 stability is regulated similarly as in A. thaliana. However, the activation of Hd3a by Hd1 around dawn (Izawa et al., 2002) cannot be explained by mimicking of the rapid degradation of CO protein under darkness. Thus, the genetic modification of this conserved pathway in rice must be elucidated in order to explain the diversification of flowering-time genes in plants.
Another flowering-time gene of rice, termed Early heading date 1 (Ehd1), encodes a B-type response regulator, with possibly no orthologue in A. thaliana (Doi et al., 2004). Ehd1 promotes floral transition preferentially under short-day conditions even in the absence of functional alleles of Hd1. Therefore, Hd1 and Ehd1 function redundantly under short-day conditions but antagonistically under long-day conditions (Fig. 2). This antagonistic action makes it possible for rice to flower even under long-day conditions. In fact, under long-day conditions, rice plants carrying a functional Hd1 and a non-functional Ehd1 did not flower even after 180 d (Doi et al., 2004). Extensive expression analysis revealed that Ehd1 is preferentially expressed under short-day conditions and acts upstream of FT orthologues such as Hd3a (Doi et al., 2004).
|
These results clearly indicate that two independent floral pathways, the evolutionally conserved Hd1 pathway and the unique Ehd1 pathway, integrate environmental photoperiod signals into the expression of FT orthologues such as Hd3a and make rice a short-day plant (Izawa et al., 2003; Izawa, 2007).
|
North by north-east: the adaptation of rice by artificial selection during domestication |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
Rice is a major crop and a staple food. Cultivated rice, O. sativa, and a wild rice, Oryza rufipogon, are believed to be derived from the same common ancestor (Khush, 1997; Vitte et al., 2004). Oryza rufipogon is broadly distributed around Indochina, from southern China to eastern India, mainly at tropical latitudes (Londo et al., 2006). Its northern limit is currently around 28° N (Fig. 3). Palaeobotanical studies revealed that the northern limit of the ancestral wild rice was near the Yangtze River basin in China at around 31° N several thousand years ago (Cao et al., 2006; Lee et al., 2007). By contrast, cultivated rice is distributed widely, and its northern limit is currently around 45° N (Fig. 3). This expansion has been made possible by domestication and breeding during the past several thousand years. It is apparent that strong artificial selection by humans has adapted rice to these broader areas.
|
This northward expansion of rice into cold regions is largely due to changes in the flowering time of cultivars, in addition to the acquisition of cold-tolerance traits. At higher latitudes, early flowering and reduced photoperiod-sensitive traits are essential to producing a harvest before approaching cold weather makes plants sterile. There is likely to be an association between the northward expansion of rice and natural variations in flowering-time genes. In fact, it is well known that many rice cultivars exhibit a latitudinal cline in flowering time. This cline has a simple explanation. Because at higher latitudes the periods for flower formation, meiosis in pollen development, and embryogenesis become limited, critical control of flowering time is essential for rice cultivation. The domestication and breeding of rice for northern regions might have included steps that changed flowering time.
|
A possible molecular mechanism involved in the adaptation of rice to the north |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
Several nearly isogenic lines (NILs) containing a genome fragment from Kasalath with a defective Hd1 allele flowered earlier than the background cultivars (such as Nipponbare and Koshihikari) in Ibaraki prefecture (
36° N), in mainland Japan [Ebitani et al., 2005; Takeuchi et al., 2006; http://ineweb.narcc.affrc.go.jp/search/inedata_top.html?ineCode=KANI0010 (in Japanese)] (Fig. 3). As described earlier, Hd1 promotes flowering under short-day conditions and represses it under long-day conditions in the laboratory. Therefore, the early-flowering traits of the NILs in the field indicate that the background cultivar flowered under a natural environment mimicking long-day conditions in the laboratory. Based on dates of flowering time in the field, the photoperiod at the floral transition was calculated and it was confirmed that the floral transition occurred under long-day conditions. In paddies at lower latitudes, the early-flowering phenotypes of the NIL became less clear. In the paddy at around 31° N in Miyazaki prefecture (Fig. 3), there was virtually no flowering-time difference between the NIL and their parent cultivars, indicating that the long-day Hd1 repressor activity was cancelled under the natural conditions in the Miyazaki paddy [http://ineweb.narcc.affrc.go.jp/search/inedata_top.html?ineCode=KANI0010 (in Japanese)]. Estimated dates of floral transition were just after the summer solstice in the paddy at 36° N and much earlier at 31° N. Therefore, short-day induction by decreasing day-length after the solstice was not involved in the flowering of rice in these paddies. These flowering-time phenotypes also clearly suggest that Ehd1 plays a critical role in flowering in the field at temperate latitudes, because functional alleles of Hd1 in the presence of a non-functional Ehd1 allele almost suppressed flowering under long-day conditions (Doi et al., 2004). In paddies at temperate latitudes (above 31° N), the balance between Hd1 repression and Ehd1 promotion could be critical to determining the appropriate flowering time in certain rice cultivars (Fig. 2). In fact, there are at least two major functional alleles of Hd1, one of which contains a 36 bp deletion in the conserved B-box zinc finger domain; these may have different effects on flowering time of cultivars grown in Japan (Griffiths et al., 2003; Nakazaki et al., 2003).
By contrast, on tropical Okinawa (24° N; Fig. 3), the same NIL with the defective Hd1 flowered a little later than the background cultivar (I Ando, NICS, personal communication), suggesting that the flowering was due to floral promotion by Hd1 at this latitude. It is likely that rice grows and flowers in Okinawa under a natural environment mimicking short-day conditions in the laboratory. In the tropics, the maximum photoperiod is shorter and the warm season is longer than those at temperate latitudes, and rice farmers in the tropics sometimes raise three crops a year. Therefore, at the lower latitudes, floral transition under short-day conditions plays a more important role than at higher latitudes. In addition, because Kasalath contains a defective allele of Hd1 (Yano et al., 2000), the mutation, which may have occurred during the domestication of Kasalath-type indica rice (sometimes called ‘aus’) (Garris et al., 2005), may have been favoured due to the longer vegetative phase and higher yield conferred in the tropics. Therefore, this allele may have underlain the cultivation of rice in Indochina (Londo et al., 2006). These examples clearly suggest that the short-day promotion of rice by Hd1 plays a role in the field at tropical latitudes.
In addition, Taichung 65 (T65), which is a cultivar grown in Taiwan (24° N; Fig. 3), contains non-functional alleles of both Hd1 and Ehd1, as identified previously by Doi et al. (2004). This non-functional allele of Ehd1 was the allele present when Ehd1 was identified as a QTL. It was further demonstrated that the non-functional allele of Hd1 is due to the insertion of a retro-element. Both non-functional alleles are naturally occurring and are thought to have been selected during breeding (Doi et al., 2004). T65 is a late-flowering cultivar and does not flower early even under short-day conditions in the laboratory, because both Hd1 and Ehd1 floral promotion pathways are defective. Under long-day conditions in the laboratory, the loss of both Hd1 inhibition and Ehd1 promotion makes T65 flower relatively late. Thus, the combination of loss-of-function alleles of Hd1 and Ehd1 may increase yield in the tropics, because cultivars with both non-functional alleles would grow longer before flowering in warm climates regardless of the natural photoperiod.
These examples demonstrate how the combination of Hd1 and Ehd1 alleles is important for flowering-time traits in rice. Thus, the identification of novel alleles with distinct biological functions would provide clues to the domestication of rice cultivars and would have an agronomic impact on future breeding. The association of flowering-time traits with Hd1 and Ehd1 haplotypes in rice cultivars awaits study.
Compared with these examples of adaptations in rice, there does not yet seem to be any good explanation at the molecular level for flowering-time traits of some rice cultivars grown at the northern limit, such as Sapporo, Japan (43° N). The flowering time of these cultivars is very early compared with those of typical cultivars at temperate latitudes, and these cultivars exhibit little photoperiod response in the laboratory. Preliminary data suggest that Hd3a is up-regulated in seedlings of these cultivars, which may be a major reason for their very early flowering and photoperiod-insensitivity. However, because this de-repression of Hd3a has not been observed in some hd1-defective lines (Izawa et al., 2002), the early flowering in the northern cultivars is not due simply to hd1 mutations. This ectopic expression of Hd3a is reminiscent of the phytochrome-deficient mutant se5 (Izawa et al., 2000, 2002), indicating that an unknown strong repressor of Hd3a expression may be regulated by phytochromes and may be defective in these northern cultivars. These clues suggest that the northern rice cultivars have distinct mechanisms regulating their early flowering.
Thus, the adaptation of rice cultivars to local regions at distinct latitudes can be partly explained by three types of photoperiodic control of flowering: short-day floral promotion with redundant actions of two promotion pathways by Hd1 and Ehd1; long-day floral repression with antagonistic actions by Hd1 and Ehd1; and early flowering due to de-repression of Hd3a expression by unknown mechanisms (Table 1). These variations in flowering-time regulation among rice cultivars at least partly allowed rice to adapt to the tremendously broad range of environments by artificial selection during domestication and breeding.
|
|
Perspectives |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
Strong artificial selection during the domestication of cultivated rice drew on the potential for adaptation present in ancient wild rice. Further association studies in cultivars and accessions will be needed to confirm this. Arabidopsis accessions have provided enough clues to study this genus, although its evolution processes would reflect its long life history and may be more complicated than that of domesticated crops.
Similar dramatic changes of agronomic traits during plant domestication are often apparent. Loss of seed-shattering traits in rice grains, morphological changes in plant architecture in maize, size changes of tomato fruits, changes in panicle morphology in barley, and flowering-time in barley and wheat are well-known examples analysed by molecular genetics (Frary et al., 2000; Doebley et al., 2006; Konishi et al., 2006; Li et al., 2006; Cockram et al., 2007; Komatsuda et al., 2007). Molecular genetic analysis of crops has made it possible to identify genes and functional nucleotide polymorphisms (FNPs) targeted by artificial selection. Furthermore, it is apparent that these FNPs have served as a foundation of agriculture and have thus contributed to the establishment of civilization and human culture. The identification of such FNPs will provide genetic resources for future breeding of crops and novel insights for new applications in different crops, in addition to novel findings of molecular mechanisms in plant biology and molecular evolution of plants.
|
Acknowledgements |
|---|
Work in my laboratory has been funded by the Program for Promotion of Basic Research Activities for Innovative Biosciences, Grants-in-Aid for Scientific Research in Priority Areas, and projects of the Ministry of Agriculture, Forestry, and Fisheries of Japan (IP1001, GD2003, GD2008).
|
References |
|---|
|
TopAbstractIntroductionMolecular mechanisms of...Natural variations associated...Molecular mechanisms of...North by north-east: the...A possible molecular mechanism...PerspectivesReferences |
|---|
Alonso-Blanco C, Mendez-Vigo B, Koornneef M. From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. International Journal of Developmental Biology (2005) 49:717–732.[CrossRef][Web of Science][Medline]
Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, Maloof JN, Clark R, Warthmann N, Chory J, Weigel D. The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nature Genetics (2006) 38:711–715.[CrossRef][Web of Science][Medline]
Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences, USA (2004) 101:15670–15675.
Cao ZH, Ding JL, Hu ZY, Knicker H, Kogel-Knabner I, Yang LZ, Yin R, Lin XG, Dong YH. Ancient paddy soils from the Neolithic age in China's Yangtze River delta. Naturwissenschaften (2006) 93:232–236.[CrossRef][Web of Science][Medline]
Cockram J, Jones H, Leigh FJ, O'Sullivan D, Powell W, Laurie DA, Greenland AJ. Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. Journal of Experimental Botany (2007) 58:1231–1244.
Corbesier L, Vincent C, Jang S, et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science (2007) doi: 10.1126/science.1141752.
Darwin C. The variation of plants and animals under domestication (1868) London: John Murray.
Doebley JF, Gaut BS, Smith BD. The molecular genetics of crop domestication. Cell (2006) 127:1309–1321.[CrossRef][Web of Science][Medline]
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes and Development (2004) 18:926–936.
Ebitani T, Takeuchi Y, Nonoue Y, Yamamoto T, Takeuchi K, Yano M. Construction and evaluation of chromosome segment substitution lines carrying overlapping chromosome segments of indica rice cultivar ‘Kasalath’ in a genetic background of japonica elite cultivar ‘Koshihikari’. Breeding Science (2005) 55:65–73.[CrossRef][Web of Science]
Ehrenreich IM, Purugganan MD. The molecular genetic basis on plant adaptation. American Journal of Botany (2006) 93:953–962.
Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science (2000) 289:85–88.
Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S. Genetic structure and diversity in Oryza sativa L. Genetics (2005) 169:1631–1638.
Gendall AR, Levy YY, Wilson A, Dean C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell (2001) 107:525–535.[CrossRef][Web of Science][Medline]
Griffiths S, Dunford RP, Coupland G, Laurie DA. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiology (2003) 131:1855–1867.
Henderson IR, Shindo C, Dean C. The need for winter in the switch to flowering. Annual Review of Genetics (2003) 37:371–392.[CrossRef][Web of Science][Medline]
Imaizumi T, Kay SA. Photoperiodic control of flowering: not only by coincidence. Trends in Plant Science (2006) 11:550–558.[CrossRef][Web of Science][Medline]
Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science (2005) 309:293–297.
Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature (2003) 426:302–306.[CrossRef][Medline]
Izawa T. Daylength measurements by rice plants in photoperiodic short-day flowering. International Review of Cytology (2007) 256:191–222.[Web of Science][Medline]
Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes and Development (2002) 16:2006–2020.
Izawa T, Oikawa T, Tokutomi S, Okuno K, Shimamoto K. Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). The Plant Journal (2000) 22:391–399.[CrossRef][Web of Science][Medline]
Izawa T, Takahashi Y, Yano M. Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Current Opinion in Plant Biology (2003) 6:113–120.[CrossRef][Web of Science][Medline]
Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science (2000) 290:344–347.
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D. Activation tagging of the floral inducer FT. Science (1999) 286:1962–1965.
Khush GS. Origin, dispersal, cultivation and variation of rice. Plant Molecular Biology (1997) 35:25–34.[CrossRef][Web of Science][Medline]
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. A pair of related genes with antagonistic roles in mediating flowering signals. Science (1999) 286:1960–1962.
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiology (2002) 43:1096–1105.
Komatsuda T, Pourkheirandish M, He C, et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proceedings of the National Academy of Sciences, USA (2007) 104:1424–1429.
Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M. An SNP caused loss of seed shattering during rice domestication. Science (2006) 312:1392–1396.
Laubinger S, Marchal V, Le Gourrierec J, Wenkel S, Adrian J, Jang S, Kulajta C, Braun H, Coupland G, Hoecker U. Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development (2006) 133:3213–3222.
Lee GA, Crawford GW, Liu L, Chen X. Plants and people from the Early Neolithic to Shang periods in North China. Proceedings of the National Academy of Sciences, USA (2007) 104:1087–1092.
Li C, Zhou A, Sang T. Rice domestication by reducing Shattering. Science (2006) 311:1936–1939.
Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proceedings of the National Academy of Sciences, USA (2006) 103:9578–9583.
Michaels SD, Amasino RM. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell (2001) 13:935–941.
Michaels SD, He Y, Scortecci KC, Amasino RM. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences, USA (2003) 100:10102–10107.
Mizoguchi T, Wright L, Fujiwara S, et al. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. The Plant Cell (2005) 17:2255–2270.
Mylne J, Greb T, Lister C, Dean C. Epigenetic regulation in the control of flowering. Cold Spring Harbor Symposia on Quantitative Biology (2004) 69:457–464.[CrossRef][Web of Science][Medline]
Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T. Mobilization of a transposon in the rice genome. Nature (2003) 421:170–172.[CrossRef][Medline]
Olsen KM, Halldorsdottir SS, Stinchcombe JR, Weinig C, Schmitt J, Purugganan MD. Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics (2004) 167:1361–1369.
Putterill J, Robson F, Lee K, Simon R, Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell (1995) 80:847–857.[CrossRef][Web of Science][Medline]
Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology (2005) 138:1163–1173.
Shindo C, Lister C, Crevillen P, Nordorg M, Dean C. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes and Development (2006) 20:3079–3083.
Simpson GG, Dean C. Arabidopsis, the Rosetta stone of flowering time? Science (2002) 296:285–289.
Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences, USA (2004) 101:4712–4717.
Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature (2001) 410:1116–1120.[CrossRef][Medline]
Sung S, Amasino RM. Remembering winter: toward a molecular understanding of vernalization. Annual Review of Plant Biology (2005) 56:491–508.[CrossRef][Medline]
Takeuchi Y, Ebitani T, Yamamoto T, et al. Development of isogenic lines of rice cultivar Koshihikari with early and late heading by marker-assisted selection. Breeding Science (2006) 56:405–413.[CrossRef][Web of Science]
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. Hd3a protein is a mobile flowering signal in rice. Science (2007) doi: 10.1126/science.1141753.
Toomajian C, Hu TT, Aranzana MJ, Lister C, Tang C, Zheng H, Zhao K, Calabrese P, Dean C, Nordborg M. A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biology (2006) 4:e137.[CrossRef][Medline]
Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science (2004) 303:1003–1006.
Vitte C, Ishii T, Lamy F, Brar D, Panaud O. Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L). Molecular Genetics and Genomics (2004) 272:504–511.[CrossRef][Web of Science][Medline]
Yano M, Katayose Y, Ashikari M, et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. The Plant Cell (2000) 12:2473–2484.
Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T. Genetic control of flowering time in rice, a short-day plant. Plant Physiology (2001) 127:1425–1429.
Yano M, Sasaki T. Genetic and molecular dissection of quantitative traits in rice. Plant Molecular Biology (1997) 35:145–153.[CrossRef][Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  R. Komiya, S. Yokoi, and K. Shimamoto A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice Development, October 15, 2009; 136(20): 3443 - 3450. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Alonso-Blanco, M. G.M. Aarts, L. Bentsink, J. J.B. Keurentjes, M. Reymond, D. Vreugdenhil, and M. Koornneef What Has Natural Variation Taught Us about Plant Development, Physiology, and Adaptation? PLANT CELL, July 1, 2009; 21(7): 1877 - 1896. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Takahashi, K. M. Teshima, S. Yokoi, H. Innan, and K. Shimamoto Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice PNAS, March 17, 2009; 106(11): 4555 - 4560. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Siefers, K. K. Dang, R. W. Kumimoto, W. E. Bynum IV, G. Tayrose, and B. F. Holt III Tissue-Specific Expression Patterns of Arabidopsis NF-Y Transcription Factors Suggest Potential for Extensive Combinatorial Complexity Plant Physiology, February 1, 2009; 149(2): 625 - 641. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Matsubara, U. Yamanouchi, Z.-X. Wang, Y. Minobe, T. Izawa, and M. Yano Ehd2, a Rice Ortholog of the Maize INDETERMINATE1 Gene, Promotes Flowering by Up-Regulating Ehd1 Plant Physiology, November 1, 2008; 148(3): 1425 - 1435. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Wu, C. You, C. Li, T. Long, G. Chen, M. E. Byrne, and Q. Zhang RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice PNAS, September 2, 2008; 105(35): 12915 - 12920. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Compiled by, F. Tooke, T. Chiurugwi, and N. Battey Flowering Newsletter bibliography for 2007 J. Exp. Bot., July 18, 2008; (2008) ern109v1. [Full Text] [PDF]
|
|
|
|
|
|
M. E. Vega-Sanchez, L. Zeng, S. Chen, H. Leung, and G.-L. Wang SPIN1, a K Homology Domain Protein Negatively Regulated and Ubiquitinated by the E3 Ubiquitin Ligase SPL11, Is Involved in Flowering Time Control in Rice PLANT CELL, June 1, 2008; 20(6): 1456 - 1469. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||