Annals of Botany 110: 1573– 1580, 2012

doi:10.1093/aob/mcs207, available online at www.aob.oxfordjournals.org

Multiple origins of the determinate growth habit in domesticated common bean

(Phaseolus vulgaris)
Myounghai Kwak1,†, Orlando Toro2, Daniel G. Debouck2 and Paul Gepts1,*
1
Department of Plant Sciences/MS1, Section of Crop and Ecosystem Sciences, University of California, Davis, CA 95616-8780,
USA and 2Unidad de Recursos Genéticos, CIAT, Apartado Aéreo 6713, Cali, Colombia
†
Present address: National Institute of Biological Resources, Environmental Research Complex, Incheon, 404-708, South Korea.
* For correspondence. E-mail [email protected]

Received: 3 June 2012 Returned for revision: 9 July 2012 Accepted: 7 August 2012 Published electronically: 27 September 2012

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† Background and Aims The actual number of domestications of a crop is one of the key questions in domesti-
cation studies. Answers to this question have generally been based on relationships between wild progenitors and
domesticated descendants determined with anonymous molecular markers. In this study, this question was inves-
tigated by determining the number of instances a domestication phenotype had been selected in a crop species.
One of the traits that appeared during domestication of common bean (Phaseolus vulgaris) is determinacy, in
which stems end with a terminal inflorescence. It has been shown earlier that a homologue of the arabidopsis
TFL1 gene – PvTFL1y – controls determinacy in a naturally occurring variation of common bean.
† Methods Sequence variation was analysed for PvTFL1y in a sample of 46 wild and domesticated accessions that
included determinate and indeterminate accessions.
† Key Results Indeterminate types – wild and domesticated – showed only synonymous nucleotide substitutions.
Determinate types – observed only among domesticated accessions – showed, in addition to synonymous sub-
stitutions, non-synonymous substitutions, indels, a putative intron-splicing failure, a retrotransposon insertion and
a deletion of the entire locus. The retrotransposon insertion was observed in 70 % of determinate cultivars, in the
Americas and elsewhere. Other determinate mutants had a more restricted distribution in the Americas only,
either in the Andean or in the Mesoamerican gene pool of common bean.
† Conclusions Although each of the determinacy haplotypes probably does not represent distinct domestication
events, they are consistent with the multiple (seven) domestication pattern in the genus Phaseolus. The predom-
inance of determinacy in the Andean gene pool may reflect domestication of common bean prior to maize intro-
duction in the Andes.

Key words: Determinate growth habit, mutability, TFL1y, centroradialis, domestication, common bean,
Phaseolus vulgaris.

IN T RO DU C T IO N unlikely to survive. Determinacy is, therefore, a trait selected

during or after domestication.
Domestication is a selection process conducted by humans – The growth habit of legumes, such as common bean, is con-
either consciously or unconsciously – among wild plants for structed in modular fashion (e.g. Tanaka and Fujita, 1979).
adaptation to human cultivation and consumption. This selec- Individual modules consist of a subtending internode, a leaf
tion process has brought about marked changes in the morph- and, in later stages of growth, an inflorescence in the axil of
ology and physiology of crop plants (Evans, 1993). Indeed one the leaf. In plants with an indeterminate growth habit, the pro-
of the hallmarks of full domestication among crop plants is duction of new modules continues until senescence. Wild
their inability to survive without human intervention common beans are all indeterminate, as is a sizable fraction
(Darwin, 1859). One of the traits selected during crop domes- of domesticated beans. In determinate domesticated types,
tication is a more compact growth habit, manifested, for the production of modules is interrupted by the appearance
example in the legumes, by a series of traits such as reduced of a terminal inflorescence in the early stages of plant develop-
branching, shorter internodes, fewer nodes, reduced twining ment, e.g. around the time of production of the fifth trifoliolate
and, in some cases, a determinate stem ending (Smartt, node (Debouck, 1991). Thus, stems have a finite length, and
1990). The wild relatives of food legumes are generally flowering occurs earlier than in indeterminate types. In
viny, herbaceous plants, with a high level of branching, Phaseolus, a determinate growth habit exists not only in
many nodes, long and twining internodes, and diageotropic domesticated common bean (P. vulgaris), but also in domesti-
branch growth. The vininess allows plants to compete with sur- cated runner bean (P. coccineus) and lima bean (P. lunatus).
rounding plants for light in the shrubby or arboreal vegetation The determinate growth habit has been exploited for crop
in which these wild plants grow naturally (e.g. Debouck et al., breeding to decrease plant biomass and to optimize allocation
1993; Freyre et al., 1996). Under these conditions, a non-viny, between vegetative and reproductive growth (Cober and
determinate plant is presumably at a severe disadvantage and is Tanner, 1995). Since the determinate growth habit allows

# The Author 2012. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [email protected]
1574 Kwak et al. — Origins of determinate growth habit in common bean

mechanical harvesting with a shorter growing cycle, cultivars accessions. Wild common bean consists of two geographic
with the determinacy trait have been preferred in several crop gene pools, Mesoamerican and Andean, which had already
species, such as tomato, soybean and common bean (Pnueli diverged prior to domestication (Gepts and Debouck, 1991;
et al., 1998; Kelly, 2001; Boote et al., 2003). In common Kwak and Gepts, 2009). Domesticated common bean origi-
bean, determinacy has been adopted at higher latitudes or in nated from those two gene pools through independent domes-
cooler climates to select earlier varieties adapted to shorter tication events (Gepts and Debouck, 1991; Kwak and Gepts,
growing seasons. Many bush snap bean varieties are determin- 2009; Kwak et al., 2009). Thus, we examine whether this es-
ate because the trait shortens the period of pod production and sential feature of bean domestication originated in one of the
leads to a more homogeneous harvest. gene pools or both of them, and whether it originated from a
Two phenotypic loci have been reported that control deter- single mutation or multiple mutations at the PvTFL1y locus.
minacy in common bean. The fin locus was first identified in
1915 (Norton, 1915) and has since been mapped to chromo-
some Pv01 (Koinange et al., 1996). This locus appears to be M AT E R I A L S A N D M E T H O D S
responsible for determinacy in most varieties with a determin- Plant materials
ate growth habit, most of whom have an origin in the Andean

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gene pool of common bean (Singh et al., 1991). A second, as The sequence of PvTFL1y was determined in a sub-sample
yet unnamed locus, was mapped on chromosome Pv07 of 47 accessions of common bean (Phaseolus vulgaris;
(Kolkman and Kelly, 2003) and may be responsible for deter- Supplementary Data Table S1) taken from a larger sample of
minacy observed in some Michigan navy bean cultivars, which 349 accessions that represented the entire P. vulgaris germplasm
arose from an artificial mutagenesis programme in the 1950s and whose genetic structure has been characterized with micro-
(Kelly, 2001). satellites (Kwak and Gepts, 2009). The 47 accessions included a
We have reported that one of the arabidopsis Terminal sample of wild and domesticated entries from the Andean and
Flower 1 (TFL1) homologues in common bean, PvTFL1y, Mesoamerican gene pools. All determinate accessions belonged
co-segregated with the fin locus on Pv01 in a recombinant to the type I growth habit as defined by Singh (1982); the number
inbred line population resulting from a cross between an indeter- of nodes bearing trifololiate leaves on the main stem varies from
minate, wild and a determinate, domesticated genotype (Kwak four to seven (D.G. Debouck and O. Toro, pers. obs.).
et al., 2008). The arabidopsis TFL1 gene is a member of the
CETS family (TFL1, Flowering Locus T, Mother of FT and High-throughput genomic DNA extraction
TFL1, Arabidopsis thaliana centroradialis homologue, Twin
sister of ft and brother of ft and tfl; Kobayashi et al., 1999). The plant tissue samples were freeze-dried in a lyophilizer
Centroradialis (CEN) from Antirrhinum and Self-pruning (sp) for 2 d. Genomic DNA was extracted using a modified
from tomato are also homologous to TFL1. This family has an high-throughput cetyltrimethylammonium bromide (CTAB)
important role in controlling the switch from a vegetative to a re- method with stainless steel beads (Chen and Ronald, 1999).
productive phase and inflorescence morphology (Pnueli et al., Two stainless steel beads were put into each well and the
1998; Ratcliffe and Riechmann, 2002; Carmel-Goren et al., block was sealed with a sealing mat. The block was placed
2003). TFL1 homologues have been identified in some legume under the grinder and the dried plant tissue samples were pow-
species (Bennloch et al., 2007). In pea, two homologous loci dered for 6 min. Then, 800 mL of lysis buffer [2 % CTAB, 1.4
were identified: PsTFL1a as the Determinate (DET) gene and M NaCl, 20 mM EDTA ( pH 8.0), 100 mM Tris base, 1 %
PsTFL1c as the Late Flowering (LF) gene (Foucher et al., b-mercaptoethanol, 5 % polyvinylpolypyrrolidone (PVPP),
2003). Ljcen1, the Lotus japonicus TFL1 homologue, is and RNase A] was added. Samples were sealed with adhesive
expressed in the inflorescence meristem; its ectopic expression foil sealer tape and then incubated at 65 8C in a hybridization
in arabidopsis delays flowering (Guo et al., 2006). In soybean, oven for 20 min. After incubation, 800 mL of sample solutions
a homologue of TFL1 is responsible for the determinate were transferred to a new 96 deep-well block and 800 mL of
growth habit controlled by the Dt1 locus (Tian et al., 2010) chloroform:isoamylalcohol (24:1) was added. After mixing
and the region including the Dt1 locus on soybean chromosome by inverting five times, samples were centrifuged for 10 min
19 is collinear to the part of common bean chromosome Pv01 at 4000 g at room temperature. The upper aqueous layers
harbouring the fin locus (S. Repinski and P. Gepts, unpubl. were transferred into another 96-well block and DNA was pre-
results). In addition, co-segregation between the fin locus and cipitated by the addition of the same volume of isopropanol.
determinacy is maintained in a much larger (n approx. 1470) After centrifugation for 10 min at 4000 g at room temperature,
population, expression of PvTFL1y determinate mutants is DNA was washed twice with 70 % ethanol and dissolved in
sharply reduced, and complementation in A. thaliana of the 100 mL of TE (10 mM Tris – HCl, 0.1 mM EDTA, pH 8.0).
mutant tfl1 phenotype with the wild-type PvTFL1 gene has
been demonstrated (Repinski et al., 2012). Thus, PvTFL1y is
Association study
the gene that underlies the determinacy locus fin at the phenotyp-
ic level on chromosome Pv01 (Kwak et al., 2008). To test the association of the retrotransposon insertion in
Here we address the origin and diversity of the mutation(s) PvTFL1y and determinacy, a sample of 349 accessions compris-
in the PvTFL1y gene leading to the determinacy phenotype in ing 100 wild and 249 domesticated accessions; 194 Andean and
the domesticated gene pool by analysing the geographic and 155 Mesoamerican accessions) was genotyped using the
gene pool distribution of mutations and haplotypes in a TFL1-la and TFL1-F4 primers (Repinski et al., 2012). PCR
sample of 349 wild and domesticated common bean mixtures contained approx. 45 ng of total genomic DNA,
 Kwak et al. — Origins of determinate growth habit in common bean 1575

200 mM dNTP, 0.2 mM TFL1y-la and TFL1-F4 primers, Expand insertion (in an Andean background; mutation IR,
long template buffer with 1.75 mM MgCl2, and 0.5 U of expand Supplementary Data Table S2) and the putative splicing
long template PCR Taq polymerase (Roche Applied Science) in mutant (in a Mesoamerican background; mutation NS10,
a 30 mL total reaction volume. The PCR cycle consisted of Supplementary Data Table S2).
2 min at 94 8C and ten cycles of 10 s at 94 8C, 30 s at 56 8C A haplotype network illustrates the relationships among the
and then 4 min at 68 8C, followed by 25 cycles of 15 s at 94 different haplotypes at the PvTFL1y locus (Fig. 2). The genetic
8C, 30 s at 56 8C and then 4 min at 68 8C with a 20 s increase background (Andean or Mesoamerican) of individual acces-
every cycle with a PTC-220 thermocycler (MJ Research). sions was determined by microsatellite fingerprinting (Kwak
Accessions whose DNA was not amplified with the TFL1-la and Gepts, 2009). Two haplotypes in PvTFL1y were correlated
and TFL1-F4 primer pair were tested with the TFL1-R7 with determinate phenotypes in the Mesoamerican gene pool
(5′ -GAGCTCACACTCCTTTTCTC-3′ ) and TFL1-F12(5′ - (M2ns and M2fs) and five haplotypes in the Andean gene
CAAACCAACAGTAAAAACCA-3′ ) primer pair, with the pool (A3fs, A2, A2ts, A2tsns and A1fs). Initially, the A4d
same PCR cycles. A 5 mL aliquot of amplified product with haplotype could not be assigned to the Andean or
1 mL of loading buffer were loaded in a 1.5 % agarose gel in Mesoamerican gene pool since the entire coding sequence
0.5× TBE and genotyped for their size. was deleted. However, the adjacent 5′ upstream and 3′ down-

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Individual sequences have been deposited in GenBank (ac- stream sequences showed that the A4d haplotype could clearly
cession nos JN418219 – 418266) be assigned to the Andean gene pool (Fig. 1). Some determin-
ate accessions shared their haplotype with indeterminate acces-
sions (M1, M2 and M3), implying the existence of unidentified
Analysis of genetic and geographic relationships of PvTFL1y
mutations in PvTFL1y or other determinacy genes.
Using primers designed based on G12873 and Midas The association test revealed that determinate types were dis-
sequences, the sequences of PvTFL1y from 47 accessions tributed mainly in Andean subpopulations, as determined by a
were determined; haplotypes were identified based on the pres- STRUCTURE analysis: K2, K4, K7 and K8 (Fig. 3; Kwak and
ence or absence of specific polymorphisms (Supplementary Gepts, 2009). Among the 160 determinate accessions included
Data Table S2). A haplotype network of PvTFL1y coding in this study, 73 % showed the retrotransposon insertion in
sequences including three introns was generated using TCS PvTFL1y. Conversely, all accessions with the retrotransposon
ver. 1.21 (Clement et al., 2000) after gap coding (Simmons insertion in PvTFLly were determinate and Andean, except ac-
and Ochoterena, 2000). Since the A4d haplotype (observed in cession G03807 (Brasil2), which has a Mesoamerican back-
accessions G02686, G04647, G24705 and G24800) does not ground (Fig. 3, Group K6, and Supplementary Table S3).
contain coding sequences of PvTFL1y, it was excluded from Although the determinate accessions with retrotransposon inser-
the haplotype network. The presence/absence of the retrotrans- tion were closely related genetically, they were distributed
poson insertion haplotype among domesticated types was dis- broadly in South and North America, Europe, Africa and Asia.
played in the previously published Neighbor – Joining tree and All determinate types originating outside the American contin-
STRUCTURE bar plot (Kwak and Gepts, 2009). ent (23 accessions from Europe, seven from Africa and four from
Asia) showed the haplotype with the retrotransposon insertion
(A2ts and A2tsns). Determinate accessions without retrotrans-
R E S U LT S
poson insertion in PvTFL1y were distributed in both Andean
The polymorphic sites in PvTFL1y sequences from 47 (K2, K4 and K8) and Mesoamerican (K6 and K9) subpopula-
common bean accessions are shown in Fig. 1. At this locus, tions (Fig. 3), further underscoring the diversity of mutations
we identified 47 nucleotide substitutions and 14 insertions or leading to the determinacy phenotype. Also, four accessions
deletions (Supplementary Data Tables S1 and S2). Among with haplotype A4d, characterized by a deletion of the entire
them, eight mutations are expected to lead to a marked PvTFL1y sequence, were found only in the Andean region, spe-
change in gene function. Most strikingly, a 4171 bp insertion cifically on the eastern slope of the Andes in Colombia and Peru,
was observed in the fourth exon (mutation IR; Fig. 1 and in sub-population K2 (Fig. 3, Supplementary Data Table S3).
Supplementary Data Table S2; Repinski et al., 2012). This
mutation is expected to lead to a frameshift, with a change
DISCUSSION
in amino acid sequence and a lengthening of the protein
coded at the 3′ end of the fourth exon. The other mutations Independent data based on co-segregation (Kwak et al., 2009;
(Fig. 1 and Supplementary Table S2) included four frameshift Repinski et al., 2012), gene expression and complementation
mutations: two with a 2 bp insertion in exons (IN1 and IN3), (Repinski et al., 2012) show that PvTFL1y is the molecular
one with a 2 bp deletion (DE3) and one exon– intron boundary locus underlying the phenotypic locus fin (Repinski et al.,
mutation (NS10) leading to a putative splicing failure and 2012), the recessive allele of which controls determinacy. Our
altered gene structure. In addition, there was a deletion of present results provide additional information supporting the
the entire coding region (DE2), and two non-synonymous role of PvTFL1y. All the variation observed among indetermin-
mutations (NS9 and NS18; Supplementary Data Table S2). ate entries involved synonymous substitutions (Fig. 1) that prob-
Interestingly, all mutations expected to lead to a marked ably did not affect the expression of PvTFL1y in these entries. In
change in gene function were found only among determinate contrast, among determinate entries, several mutation types
(domesticated) accessions. The marked loss of expression (Fig. 1 and Supplementary Data Table S2) were observed that
expected from these mutations has been confirmed by quanti- potentially cause reduction or elimination of gene expression.
tative PCR for two of the mutations, the retrotransposon These types include deletion of the entire locus (haplotype
1576 Kwak et al. — Origins of determinate growth habit in common bean

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M Dd M1
M Dd
M Dd
M W
M W
M W
M Dd M3
M W
A Dd
M W PE
M W
A W A1
M W
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A Dd

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1 kb

F I G . 1. Haplotype diversity in the PvTFL1y region. Each row is a different accession, presented in the same order as in Supplementary Tables S1 and S3. Gene pool:
assignment for each accession – M, Mesoamerican; A, Andean. Accession type – domestication status of accessions: W, wild (all indeterminate); D, domesticated in-
determinate; Dd, domesticated determinate. STRUCTURE membership coefficient – ancestry of accessions in nine STRUCTURE clusters (Kwak et al., 2009) as indicated
by the length of each coloured segments: pink, races Jalisco and Durango; red, race Mesoamerica; grey, Mesoamerican wild; brown, Mesoamerican and Colombian wild;
dark blue, ancestral Peru and Ecuador wild; purple, Andean wild; green, race Peru; light blue, race Chile; orange, race Nueva Granada. Polymorphisms in the PvTFL1y
region – light blue, coding region; grey, untranslated region; horizontal bar, nucleotide substitution; open triangle, deletion; filled triangle, insertion; black vertical bar,
4171 bp retrotransposon insertion, not to scale. Polymorphisms expected to affect gene expression are indicated as red-coloured symbols. Information about each poly-
morphism is given in Supplementary Data Table S2. Haplotype – haplotype of PvTFL1y. Black bar, wild type; coloured bar, mutations with severe structural changes
expected: d, deletion of the entire coding region; fs, frameshift; ns, non-synonymous substitution; ts, transposon insertion. Structural changes – the expected structural
changes are depicted and the mutations leading to changes are shown. DE, deletion; IN, insertion; IR, insertion of retrotransposon; NS, non-synonymous substitution.
 Kwak et al. — Origins of determinate growth habit in common bean 1577

re-structuring of certain domesticated Gossypium species

M2ns M2fs (Palmer et al., 2012), and render certain genes more inducible
by external stresses such as cold (Naito et al., 2009).
NS10 IN3 Secondly, it may be more than a coincidence that the insertion
occurred in the fourth exon of the PvTFL1y gene. In
M2 A. thaliana, experiments show that the fourth exon is crucial
for the full inhibitory effect of the TFL1 gene to be expressed
(Ahn et al., 2006). Assuming that the mechanism of action is
similar in P. vulgaris, natural insertional mutagenesis in the
M1 fourth exon may ensure strong inactivation of PvTFL1y and a
stable and highly heritable expression of the determinacy pheno-
type. Thirdly, of all the PvTFL1y haplotypes, the retrotrans-
PE M3 poson insertion is the most frequent one. It occurs in 73 % of
the determinate accessions. Outside of the Americas, it is the
only PvTFL1y haplotype among determinates. The predomin-

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A3fs
IN1 ance of this haplotype among determinate domesticated types
DE3 A1
could be attributed to several, non-mutually exclusive reasons.
Indeterminate domesticated The A2ts haplotype may have achieved its predominance by
A2 A1fs Determinate domesticated – virtue of being the earliest haplotype to appear in the Andean
retrotransposon domesticated gene pool. Other haplotypes would have appeared
IR Determinate domesticated + later and achieved a more limited geographic distribution.
retrotransposon
A2fs
Alternatively, the A2ts haplotype is linked to a factor promoting
Wild
A4d domestication in addition to determinacy. Selection for this add-
Mutation in exon
itional factor combined with hitchhiking could speed up the
Mutation in intron spread of the A2ts haplotype. A quantitative trait locus (QTL)
A2tsns analysis of the domestication syndrome of common bean has
shown that the fin locus is linked to both the Ppd ( photoperiod
F I G . 2. Haplotype network of PvTFL1y. The frequency of determinate, retro-
sensitivity) locus and a QTL for internode length (L5) on
transposon insertion and domesticated accessions for each haplotype is shown chromosome Pv01 (Koinange et al., 1996). Further research is
as a proportion of colour in the node circle. Yellow, indeterminate domesti- needed to isolate the genes involved and determine the geno-
cated; green, determinate domesticated without retrotransposon insertion; types at these linked loci in the domesticated sample involved.
blue, determinate domesticated with retrotransposon insertion; brown, wild. Further research is needed to determine the specific phenotypic
For haplotype abbreviations, see text. Mutations in exon and intron are as indi-
cated in the key. Nodes without circles were not sampled in this study. effects (in addition to determinacy) especially on growth habit
of the different PvTFL1y haplotypes.
A4d), non-synonymous mutation (haplotype M2ns), indels The haplotype tree of PvTFL1y sequence variation (Fig. 2) is
(haplotype M2fs, A1fs and A3fs), a potential splicing site alter- consistent with the overall genealogy of common bean, as deter-
ation (haplotype M2ns) and a retrotransposon insertion in the mined through numerous studies (e.g. Kwak and Gepts, 2009;
fourth exon (haplotypes A2ts and A2tsns). The predicted Kwak et al., 2009). Wild types (all of which are indeterminate)
elimination of gene expression in two of these haplotypes as well as indeterminate domesticated types are located in the
(M2ns and A2ts) was verified experimentally (Repinski et al., centre of the tree, whereas determinate domesticated types
2012). These expression-disrupting mutations were only were located at the end of branches. This topology confirms
observed among determinate types and are consistent with the the derived nature of determinacy. Furthermore, there are two
recessiveness of the trait. major branches, one including Andean accessions and the
Three haplotypes (M1, M2 and M3) included both deter- other Mesoamerican accessions (as determined by independent,
minate and indeterminate types (Fig. 2), suggesting that neutral microsatellite markers), confirming that determinacy has
sequences responsible for determinacy in these accessions been selected independently in the two major geographic gene
are not situated within the sequence covered by the current pools. With two exceptions (Suppelementary Data Fig. S1 and
analysis. These sequences could be located immediately adja- Table S1), there is congruity between haplotypes and gene
cent to the PvTFL1y sequence, perhaps in a regulatory se- pool assignments, i.e. all the haplotypes were observed in a
quence 5′ upstream of PvTFL1y, or at other determinacy loci single gene pool. The first exception was haplotype A2ts, the
in the genome, such as the PvTFL1x and PvTFL1z loci. major Andean PvTFL1y haplotype, which was also represented
Haplotypes involving the retrotransposon insertion deserve in a single determinate Mesoamerican accession, G03807 or
more scrutiny. First, this type of mutation confirms the import- Brasil2. Microsatellite diversity analyses show that Brasil2
ance of transposons in general as a factor shaping evolution has the characteristic microsatellite complement of a
(Barabaschi et al., 2012; Kejnovsky et al., 2012; Leitch and Mesoamerican accession (Kwak and Gepts, 2009). Our observa-
Leitch, 2012; Slotkin et al., 2012). Evidence is growing that tions therefore suggest that Brasil2 acquired the determinacy
transposons have influenced the crop domestication process. trait from an Andean accession by an initial hybridization fol-
For example, they have increased the expression of genes lowed by multiple backcrosses to one or more Mesoamerican
involved in morphological development, such as the Tb1 locus parents. This somewhat unlikely scenario would account for
in maize (Studer et al., 2011), have been involved in the the existence of an Andean PvTFL1y allele in a predominantly
1578 Kwak et al. — Origins of determinate growth habit in common bean

DM
DS
DG
IG
W

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K9 K6 K5 K3 K1 K7 K2 K4 K8
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F I G . 3. The distribution of determinacy in each sub-population (K1– K9) as identified by STRUCTURE (Kwak and Gepts, 2009). The lower part of the figure
represents a STRUCTURE bar graph of wild and domesticated bean simple sequence repeat diversity according to Kwak and Gepts (2009). The upper part of the
figure represents the proportion of four classes of bean accessions based on status (wild vs. domesticated), growth habit (determinate vs. indeterminate) and pres-
ence or absence of a retrotransposon insertion in the PvTFL1y locus: DM, domesticated, determinate, retrotransposon insertion into PvTFL1y region; DS, domes-
ticated, determinate, deletion of whole PvTFL1y region; DG, domesticated, determinate, wild-type PvTFL1y region; IG, domesticated, indeterminate, wild-type
PvTFL1y region; W, wild, indeterminate, wild-type PvTFL1y region.

Mesoamerican background. The second exception is G24999, varieties, a plant that could fulfil a similar function was not
which carries a Mesoamerican PvTFL1y haplotype (M3) in an domesticated in the Andes as most crop plants in the Andes
Andean microsatellite background and probably arose through are of lesser stature or stem strength compared with maize
a similar introgression procedure to that of Brasil2. The exist- (e.g. root crops, tarwi or lupine, and quinoa). Common bean
ence of these two exceptions is important because it shows the remnants in the Andes have been retrieved in contexts associated
high level of congruence between haplotypes, and gene pool with charcoal, the latter dated to 7700 calibrated years BP
membership is not due to reproductive isolation between the (Kaplan and Lynch, 1999). The dissemination of maize from
two gene pools, but presumably through the limited opportun- its centre of domestication in Mexico into Panama and
ities for hybridization between these geographically isolated Ecuador has been dated to 7800 – 7000 calibrated years BP
gene pools. Genes causing F1 Andean × Mesoamerican dwarf (Dickau et al., 2007) and 5300 – 4950 calibrated years BP
lethality – located on the linkage groups Pv02 and Pv11 (Zarrillo et al., 2008), respectively. In Peru, the oldest maize
(Hannah et al., 2007) – are also unlinked to the fin-PvTFL1 remains documented so far were dated to 3600– 4000 calibrated
loci (located on linkage group Pv01). years BP (Perry et al., 2006). Plant starch grains embedded in
The higher frequency of determinacy in the Andean domesti- tooth calculus have been retrieved from an early archaeological
cated gene pool can be traced back to the early stages of agricul- site in northern Peru. These starch grains, dated to 5500 – 9000
ture in the Andean domestication centre. Whereas in the BP, originated from three legume species (common bean,
Mesoamerican domestication centre, farmers could use maize peanut and Inga sp.) and squash (Piperno et al., 2008). No
(domesticated in Mesoamerica, presumably in the Balsas maize was described at this site. Thus, there may have been an
River basin) as a physical support for viny common bean incipient agricultural period in which maize had not yet been
 Kwak et al. — Origins of determinate growth habit in common bean 1579

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