Journal of Heredity Advance Access originally published online on March 2, 2008
Journal of Heredity 2008 99(3):283-291; doi:10.1093/jhered/esn005
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Mapping Homologous Sequences for Determinacy and Photoperiod Sensitivity in Common Bean (Phaseolus vulgaris)
From the Department of Plant Sciences/MS1, Section of Crop and Ecosystem Sciences, University of California, 1 Shields Avenue, Davis, CA 95616-8780
Address correspondence to Paul Gepts at the address above, or e-mail: plgepts{at}ucdavis.edu.
Determinacy and photoperiod insensitivity are agronomically important traits, selected during or after domestication in common bean. Determinacy reduces aboveground plant biomass and accelerates and synchronizes flowering. Photoperiod insensitivity allows common bean to be grown at higher latitudes under long days. In this study, we attempted to identify Phaseolus vulgaris homologues of 12 Arabidopsis genes that are involved in meristem identity determination and the photoperiod-dependent and autonomous flowering pathways. Amplification products with homology to the original Arabidopsis gene were obtained for 8 genes, 7 of which could be mapped onto the common bean-linkage map using the BAT93 x Jalo EEP 558 and Midas x G12873 [GenBank] recombinant inbred populations. Three Terminal Flower 1 homologues (PvTFL1x, PvTFL1y, and PvTFL1z) were mapped to B4, B1, and B7, respectively. PvTFL1y cosegregated with the determinacy locus, fin. In addition, PvTFL1z mapped near or at a second determinacy locus on B7. A Zeitlupe homologue mapped near a quantitative trait locus (QTL) for flowering time on linkage group B9. Constans, FCA, Flowering locus D, Gigantea, and Leafy homologues did not cosegregate with currently mapped flowering time QTLs and photoperiod insensitivity loci in common bean. Further studies are needed to confirm the role of these homologues as potential candidate genes.
Wild common bean is indeterminate and flowers under short-day conditions. Plants are typically viny and grow on other plants that act as physical support. In addition, they require nights of at least 11–12 h for flowering induction. During common bean domestication and dissemination from its centers of domestication, selection for photoperiod insensitivity allowed common bean to spread to higher latitudes (Gepts and Debouck 1991). Also, the determinate growth habit (GH) has been exploited in crop breeding to accelerate flowering and shorten the flowering period (Cober and Tanner 1995). In indeterminate cultivars, the terminal meristem remains in a vegetative state during which it controls the production of stems and leaves. In determinate cultivars, the terminal meristem switches from a vegetative to a reproductive state, that is, it produces a terminal inflorescence. Thus, photoperiod-insensitive, determinate common bean cultivars generally flower and mature early, allowing a shortening of the time to harvest (Koinange et al. 1996). Because common bean in the Andean region may have been domesticated without maize, which is used as a physical support for climbing bean in traditional agriculture, determinate genotypes would have been favored in that domestication region (Koinange et al. 1996).
In common bean, several major loci and quantitative trait loci (QTLs) have been reported for GH, photoperiod sensitivity, and flowering time (Norton 1915; Wallace et al. 1993; Jung et al. 1996; Bassett 1997; McClean et al. 2002; Tar'an et al. 2002; Kolkman and Kelly 2003). Among them, the recessive fin (determinacy) and the dominant Ppd (photoperiod sensitivity) loci are located on the B1 linkage group (Norton 1915; Koinange et al. 1996; Freyre et al. 1998). Isolation of these genes would allow us to better understand how selection for determinacy and photoperiod insensitivity has shaped, if at all, genetic diversity in the fin–Ppd region relative to other regions of the bean genome. It will also allow us to get a better understanding of their function for further utilization and improvement of these traits in bean breeding.
As a first step toward isolating these genes in common bean, we sought to use information obtained in model species such as Arabidopsis through a candidate gene approach. Genetic regulation of flowering induced by light has been studied most intensively in model species, especially in Arabidopsis (Hayama and Coupland 2003; Komeda 2004; Corbesier and Coupland 2005). Photoperiodism involves regulation of flowering time through a circadian clock (Ratcliffe and Riechmann 2002; Komeda 2004). Thus, identification of candidate genes for photoperiod sensitivity in target species can be initiated with testing genes of the light-dependent flowering pathway from Arabidopsis. For example, in rice, heading date is controlled by photoperiod. One of the major QTL for heading date, Hd1, is a homologue of the Arabidopsis Constans (CO) gene. This gene codes for a zinc finger–containing protein, which interacts between circadian rhythms and the flowering signaling pathway (Yano et al. 2000; Hayama and Coupland 2004).
Determinacy and photoperiod sensitivity traits play an important role in common bean evolution and breeding, but the actual genes have not yet been isolated in this species. In this study, several common bean homologues related to floral transition and photoperiod sensitivity mainly from Arabidopsis were isolated and mapped onto the consensus common bean-linkage map. This work will provide genetic background information to manipulate GH and photoperiod sensitivity for future common bean breeding as well as identifying candidate genes for those traits in other legume species.
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Polymerase Chain Reaction Primers
Table 1 shows the Arabidopsis genes included in this study. Amplifications of LFY and TFL1 homologues were performed with degenerate primers developed prior to this study by Frohlich and Meyerositz (1997) and Foucher et al. (2003), respectively. To identify other homologous genes in common bean, degenerate primers were developed in this study (Table 2). Using Arabidopsis sequences, the corresponding homologues of soybean, peanut, Medicago, or/and lotus sequences were obtained by BLAST searches in GenBank. The sequences were aligned with ClustalX (Thompson et al. 1997). The degenerate primers were developed based on conserved motifs among the sequences from those species.
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Amplification of Homologous Sequences
Genomic DNA was extracted from young leaves using the Cetyl TrimethylAmmonium Bromide method (Doyle and Doyle 1987). The target fragments in BAT93, G12873 [GenBank] , Jalo EEP558, and Midas (parents of the mapping populations used in this study) were amplified using polymerase chain reaction (PCR) with Taq DNA polymerase (New England Biolabs, Ipswich, MA). PCR reaction mixtures contained approximately 100 ng of total DNA, 0.2 mM of dNTP, 0.2 µM of forward and reverse primers, standard Taq buffer with 1.5 mM MgCl2, and 1 unit of Taq polymerase in a total volume 50 µl reaction. The PCR cycle consisted of 2 min at 95 °C and 35 cycles of 1 min at 95 °C, 1 min at 48 °C (PvLFY), 54°C (PvFKF1 and PvZTL), 55 °C (PvTFL1x, PvTFL1y, and PvTFL1z), 56 °C (PvFCA), 57 °C (ELF3), 58 °C (PvGI), or 60 °C (PvCO and PvFLD), and lastly 1–3 min at 72 °C followed by a 7 min extension at 72 °C. For amplification of AP1, AG, and TFL2 fragments, various annealing temperatures from 50 °C to 62 °C were tested. For amplification of a PHYB fragment, the PCR cycle consisted of 35 cycles of 1 min at 92 °C, 1.5 min at 53 °C, and 4.5 min at 68 °C. The fragments obtained were sequenced at the sequencing facility in the Division of Biological Sciences at University of California, Davis. For TFL1 homologues, fragments of approximately 360 bp, 520 bp, and 800 bp were cloned using the TOPO TA Cloning Kit for Sequencing (Invitrogen, Carlsbad, CA). Transformation and analysis were done following manufacturer's instructions. Sequencing of inserted fragments was performed with SP6 and T7 universal primers. The identity of the sequences was confirmed with a tBLASTx search. Sequence polymorphisms between parental lines were searched for restriction enzyme cleavage sites. For PvFCA, PvFLD, PvGI, PvTFL1x, PvTFL1y, and PvTFL1z, nested primers to improve amplification quality were designed and used for the genotyping and mapping experiment (Table 2).
Mapping Populations
The BAT93 x Jalo EEP 558 (BJ, n = 80) and Midas x G12873
[GenBank]
F8 (MG, n = 58) recombinant inbred (RI) populations were used to integrate the homologous sequences into the common bean molecular linkage map. The BJ RI population is the common bean core mapping population (Freyre et al. 1998; Blair et al. 2003). BAT93 is a multiple disease–resistant breeding line belonging to the Mesoamerican gene pool, whereas Jalo EEP558 is a Brazilian cultivar from the Andean gene pool. The MG RI population was used to investigate the inheritance of domestication syndrome traits in common bean (Koinange et al. 1996). Midas is a domesticated Andean accession, and G12873
[GenBank]
is a wild Mesoamerican accession. This MG population shows several segregating traits related to domestication, including determinacy (fin) and photoperiod sensitivity (Ppd), which do not segregate in the BJ population. However, because the map of MG is a low-density map, homologous sequences were mapped in both the BJ and MG populations. Huron and Newport (HN), the parental lines of the HN population used for mapping an additional determinacy locus on B7 (Kolkman and Kelly 2003), were used to sequence PvTFL1z, an additional homologous sequence.
Genotyping Amplified Fragments
To genotype fragments in the 2 RI populations, PvCO, PvFLD, PvFKF1, PvLFY, and PvTFL1y sequences were amplified and digested with TaqI, BsmAI, BsssSI, CviJI, and MseI, respectively (Table 3). For PvZTL sequences, amplified fragments in the BJ population were digested with Taq
I and the fragments of the MG population were digested with Hpy188I. Digestions followed the manufacturer's instructions. Digested fragments were separated by 1.5% agarose gel or 6% polyacrylamide gel electrophoresis depending on their size and size differences. To genotype PvFCA, PvGI, and PvTFL1x, the fragments of the RI populations were amplified and genotyped directly in a 6% polyacrylamide gel according to their size difference. PvTFL1z was genotyped by sequencing.
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Genetic Mapping of Homologous Sequences
Homologous sequences were mapped with MAPMAKEWR/EXP 3.0 (Lander et al. 1987; Lincoln et al. 1992; Freyre et al. 1998) using a minimum LOD score of 3.0 and a maximum distance of 50 cM. The markers were ordered using the "Sequence" command and the new homologous sequences in this study were placed using the "Try" and "Compare" commands into their respective linkage group. The likelihood of their placement was tested using the "Ripple" command to find the most likely order. The linkage maps obtained are represented using the MapChart program (Voorrips 2002).
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Results |
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The PCR amplifications using degenerate primers designed in this study were successful in identifying homologous sequences potentially coding for determinacy and photoperiod sensitivity in common bean, except for homologues of AP1 and TFL2 (Table 3). BLAST searches of GenBank revealed that the sequences obtained in this study are very similar to reproductive transition and photoperiod sensitivity genes, mostly of Medicago truncatula, considered a legume model plant (Table 4). For amplification of ELF3, a fragment of approximately 1200 bp was obtained from the 4 parental lines. However, the sequencing of this fragment was not successful and ELF3 was excluded from further analyses. For amplification of homologous sequences of PHYB, fragments of approximately 2 kb, 1 kb, 750 bp, and 400 bp were obtained with PHYB-F1 and PHYB-R2 primers and of approximately 1.4 kb, 700 bp, 600 bp, and 300 bp were obtained with PHYB-F3 and PHYB-R4 primers. However, tBlastx searches did not identify any sequences homologous to flowering time or GH genes. Thus, PHYB was excluded from further analysis as well. Using the primers developed by Foucher et al. (2003), an approximately 800-bp PvTFL1y fragment was not amplified from Midas as expected. However, because a 251-bp PvTFL1y fragment could be amplified using nested primers for PvTFL1y, genotyping in the MG population was successful (Table 3).
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The polymorphisms in the PvCO, PvFCA, PvFLD, PvLFY, PvTFL1x, PvTFL1y, and PvTFL1z sequences among parents of the 2 RI populations reflected generally the origin of bean accessions. Midas and Jalo EEP558 represent accessions of Andean origin, whereas G12873 [GenBank] and BAT93 originated in the Mesoamerica gene pool. Four SNPs were found in PvZTL sequences. Whereas 1 SNP distinguished G12873 [GenBank] from the 3 other genotypes in PvZTL sequences, 3 SNPs distinguish BAT93 from the other 3 sequences. Three SNPs and a 24-bp tandem repeat were found in PvGI sequences. These SNPs in PvGI sequences distinguished the G12873 [GenBank] sequence from the others. Because we could not find any polymorphism between BAT93 and Jalo EEP 558 for the PvGI sequence, the BJ population was not genotyped for PvGI sequences. Likewise, because a PvFCA sequence could not be amplified in G12873 [GenBank] , PvFCA was not genotyped in the MG population. The enzymes and genotyping methods are summarized in Table 3. The segregations of these alleles in the RI populations are summarized in Tables 5 and 6.
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The distribution of flowering and GH homologues in the common bean-linkage map is shown in Figure 1. TFL1 sequences mapped to 3 different linkage groups: B1, B4, and B7. The PvTFL1y, PvTFL1z, and PvFLD loci had similar map positions in the MG and BJ maps. PvTFL1y cosegregated with the fin locus in the MG RI population. PvTFL1z mapped to linkage group B7. Although there was no segregating locus for GH trait located on B7 in the MG and BJ populations, a determinate morphology in the HN population had been mapped to the B7 linkage group in a similar location (Kolkman and Kelly 2003). In addition, Tar'an et al. (2002) mapped a plant height (PH) QTL on B7 in the OAC Seaforth x OAC 95-4 cross. However, the absence of polymorphism between the Huron and Newport PvTFL1z sequences precluded comparative mapping of the PvTFL1z and determinacy loci on B7 in the HN population. We could not find any morphological marker cosegregating with PvTFL1x on linkage group 4.
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A PvZTL fragment mapped to the B9 linkage group in population BJ (Figure 1). The position of PvZTL was similar to that of a GH gene identified by Tar'an et al. (2002). This GH locus is correlated with the number of days to flowering and maturity (Tar'an et al. 2002). The PvCO, PvLFY, PvZTL, and PvTFL1x could not be assigned in the MG population with a LOD score of at least 3.0. The PvFKF1 sequence could not be assigned in either population.
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Discussion |
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Gene discovery using public sequence databases of model plants is useful especially for specialty crops that do not have this type of information yet (Mahalakshmi and Ortiz 2001). The strategy to identify certain homologous genes with degenerate primers designed from sequence information in model plants databases was partially useful in this study. The sequences obtained in this study had a high BLAST match with corresponding sequences in M. truncatula or other species (Table 5). Considerable progress has been made in legume genomics with large genomic or EST sequencing efforts in soybean (Glycine max), M. truncatula, and Lotus japonicus (Gepts et al. 2005). The availability of these resources made the design of degenerate primers considerably easier than it was 5 years ago when degenerate primers for Phaseolus vulgaris had to be established based on homologies with nonlegume sequences (Sambatti J. and Gepts P., unpublished data: e.g., TFL1 homologues: AY028710 [GenBank] and AY028711 [GenBank] ). However, of the 12 Arabidopsis genes included in this study, homologous P. vulgaris sequences could be amplified for only 8 of them. No amplified product could be obtained for 2 genes (AP1 and TFL2). Predicted sequences could not be obtained for 2 other genes (ELF3 and PHYB). The lack of success can be attributed to at least 2 causes. First, and most likely, sequence divergence within the legume family may make the design of primers more difficult. Further attempts at designing primers could ultimately yield sequenceable amplicons. Second, the specific homologues may not exist in common bean. However, given the ubiquitousness of these sequences, this possibility seems unlikely although not impossible in individual cases. Sequences homologous to AP1 have been identified in other legumes (Berbel et al. 2001; Hecht et al. 2005). Through a BLAST search using an Arabidopsis TFL2 sequence (AB073490 [GenBank] ), a similar sequence was identified in soybean (TC230509; e value 2.1 x 10–23).
An indeterminate common bean plant produces stem nodes until maturity and senescence take over the growth processes. After floral initiation, each node consists of an internode with above it, 1 compound leaf and a compound raceme inflorescence in its axil. However, a determinate common bean plants ceases producing stem nodes well before the onset of maturity and senescence because the terminal meristem of stems produces a terminal inflorescence. The growth pattern through successive series of modular units is similar to that of tomato (Sage and Webster 1987; Schmitz and Theres 1999). In tomato, Self-Pruning (SP) and Falsiflora (FA) control meristem identity. SP gene suppresses the transition of vegetative to reproductive state, keeping a plant indeterminate (Pnueli et al. 1998). FA is responsible for floral meristem identity and promotes flowering (Molinero-Rosales et al. 1999). SP is a member of the CETS family (Centroradialis [CEN] in Antirrhinum, TFL1 in Arabidopsis, and FT in Arabidopsis [Pnueli et al. 2001]). FA is an orthologue of Arabidopsis LFY and Antirrhinum Floricaula (FLO). LFY in Arabidopsis activates directly AP1, causing flowering (Komeda 2004; Saddic et al. 2006). Recently, a pea homologue of TFL1, PsTFL1a, has been found to correspond to the determinacy locus (Determinate; DET) in that species (Foucher et al. 2003). Another pea TFL1 homologue, PsTFL1c, is a homologue of Late Flowering, a repressor of flowering. In common bean, cosegregation between the PvTFL1y and fin loci in the MG population suggests that PvTFL1y may be a candidate gene for the fin locus. Further data are needed to confirm this finding. Furthermore, because amplification using Foucher et al. (2003) was not successful in Midas, it implies that Midas might possess a mutation in primer site on the putative forth exon of PvTFL1y. Thus, further research to investigate relationship of this mutation in Midas PvTFLly and determinacy should be pursued.
PvLFY mapped to the B9 linkage group in this study, but we could not find any morphological trait associated with it. However, because a large single leaf mutation (Unifoliata-2), similar to pea uni has been reported in common bean (Garrido et al. 1991), the role of PvLFY as a potential candidate gene for Uni-2 should be analyzed further. LFY homologues have been isolated from many species and their function is well conserved in angiosperms. Unifoliata (UNI) in pea is a LFY homologue and regulates indeterminacy of leaf and flower morphogenesis (Hofer et al. 1997).
The map position of PvTFL1z on B7 is similar to that of another possible determinacy locus (Tar'an et al. 2002; Kolkman and Kelly 2003). This determinacy may correspond to the determinate mutant generated by artificial mutagenesis in navy bean (Kelly 2000; Kolkman and Kelly 2003). Because we obtained a partial sequence of the putative first and second exons and first intron of Huron and Newport, it may be possible to find polymorphisms outside of the sequences obtained. Thus, a further linkage experiment between PvTFL1z and determinacy locus on B7 as well as morphological characterization of determinate phenotypes and possible epistatic interactions between PvTFL1y and PvTFL1z should be performed. This work may be helpful in manipulating plant architecture to improve common bean.
Among economic plants in the legume family, soybean, pea, and common bean have several genotypes or mutant lines with a determinate GH. The phenotype of 2 determinate soybean mutants (dt-1 and Dt-2) is identical to the determinacy phenotype of common bean. Although genetic and physical maps for soybean have been constructed, the actual determinacy genes have not yet been identified in that species (Tasma and Shoemaker 2003; Wu et al. 2004). TFL1 homologues in soybean should be tested as candidate genes to elucidate the nature of soybean determinacy genes. In pea, it has been shown recently that the determinate mutant (det) is caused by mutations in a homologue of the Arabidopsis TFL1 gene. These mutations are synonymous or nonsynonymous substitutions at the junction between an exon and an intron resulting in splicing failure (Foucher et al. 2003).
In this study, we found that the map position of the PvZTL on B9 is similar to that of a GH locus in common bean. Because determinacy causes an early flowering, there is a positive correlation between earliness and PH. Tar'an et al. (2002) reported correlation of days to flowering and days to maturity to this locus. This raises the question whether the PvZTL locus could be a candidate gene for this locus.
With the exception of the PvTFL1y, PvTFL1z, and PvZTL sequences, we could not find any further sequences associated with a morphological trait associated in this study. In particular, we have not been able so far to identify a potential candidate gene for the Ppd locus. Therefore, of the 8 Arabidopsis sequences mapped, only 2 are currently associated with a mapped flowering-related gene in common bean. However, this study is based on segregation of photoperiod and GH traits that are present in only 3 study populations. It is possible that additional morphological traits will be identified that segregate in other populations and will cosegregate with homologous sequences mapped in this study. Also, the genetic mapping of potential candidate genes will provide a database for their potential role in photoperiod and reproductive transition pathways. Further isolation of mapping of flowering and GH genes is warranted to obtain a more complete picture of the genes involved in this important developmental stage of the bean plant.
In summary, our study was able to identify homologous sequences that either cosegregate with or map in the vicinity of known major genes controlling flowering. The case of the PvTFL1y homologue, which cosegregates with the fin gene is tantalizing given the similarity in phenotype action (if not the phenotype). However, the segregating population is small (n 
65). Thus, this cosegregation will have to be confirmed in a larger population if PvTFL1y is to be considered as a candidate gene for the fin locus. In addition, polymorphisms at this locus should correlate with the determinacy/indeterminacy phenotype. Ultimately, transformation and complementation tests will determine if fin is coded by PvTFL1y.
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National Research Initiative Plant Genome Program of the United States Department of Agriculture Cooperative State Research, Education and Extension Service Grant no. 03-35300-13287 (to P.G.); Department of Plant Sciences at the University of California, Davis, student fellowship (to M.K.).
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Corresponding Editor: William Tracy
Received June 21, 2007
Accepted November 30, 2007
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