Construction of a potato consensus map and QTL meta-

analysis offer new insights into the genetic architecture of

late blight resistance and plant maturity traits
Danan et al.

Danan et al. BMC Plant Biology 2011, 11:16

http://www.biomedcentral.com/1471-2229/11/16 (19 January 2011)
Danan et al. BMC Plant Biology 2011, 11:16
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RESEARCH ARTICLE Open Access

Construction of a potato consensus map and QTL

meta-analysis offer new insights into the genetic
architecture of late blight resistance and plant
maturity traits
Sarah Danan1, Jean-Baptiste Veyrieras2, Véronique Lefebvre1*

Abstract
Background: Integrating QTL results from independent experiments performed on related species helps to survey
the genetic diversity of loci/alleles underlying complex traits, and to highlight potential targets for breeding or QTL
cloning. Potato (Solanum tuberosum L.) late blight resistance has been thoroughly studied, generating mapping
data for many Rpi-genes (R-genes to Phytophthora infestans) and QTLs (quantitative trait loci). Moreover, late blight
resistance was often associated with plant maturity. To get insight into the genomic organization of late blight
resistance loci as compared to maturity QTLs, a QTL meta-analysis was performed for both traits.
Results: Nineteen QTL publications for late blight resistance were considered, seven of them reported maturity
QTLs. Twenty-one QTL maps and eight reference maps were compiled to construct a 2,141-marker consensus map
on which QTLs were projected and clustered into meta-QTLs. The whole-genome QTL meta-analysis reduced by
six-fold late blight resistance QTLs (by clustering 144 QTLs into 24 meta-QTLs), by ca. five-fold maturity QTLs (by
clustering 42 QTLs into eight meta-QTLs), and by ca. two-fold QTL confidence interval mean. Late blight resistance
meta-QTLs were observed on every chromosome and maturity meta-QTLs on only six chromosomes.
Conclusions: Meta-analysis helped to refine the genomic regions of interest frequently described, and provided
the closest flanking markers. Meta-QTLs of late blight resistance and maturity juxtaposed along chromosomes IV, V
and VIII, and overlapped on chromosomes VI and XI. The distribution of late blight resistance meta-QTLs is
significantly independent from those of Rpi-genes, resistance gene analogs and defence-related loci. The
anchorage of meta-QTLs to the potato genome sequence, recently publicly released, will especially improve the
candidate gene selection to determine the genes underlying meta-QTLs. All mapping data are available from the
Sol Genomics Network (SGN) database.

Background mapping results from independent experiments (e.g.

The number of publications reporting the mapping of Gramene for maize and rice). But for most species, QTL
QTLs (quantitative trait locus) in plants has exponen- data accumulates in bibliography until the coming out
tially increased since the Eighties, reaching a total of of hot-spot genomic regions that become targets for
about 34,300 papers in 2010 (source: Google Scholar introgression into breeding material or for cloning. To
with key words “QTL” and “plant”). For a few species get a comprehensive understanding of the genetic con-
only, this huge amount of QTL data has been recorded trol of a polygenic trait and to optimize its use in breed-
in databases that enable quick comparison of QTL ing, it is needed to get a complete view of the genetic
architecture of the trait with the distribution of the
* Correspondence: [email protected] involved loci along the genome. This synthesis can be
1
Institut National de la Recherche Agronomique (INRA), UR 1052 Génétique greatly facilitated by achieving a QTL meta-analysis.
et Amélioration des Fruits et Légumes (GAFL), BP94, 84140 Montfavet, The general principle of a meta-analysis is to pool the
France
Full list of author information is available at the end of the article results of several studies that address the same issue to

© 2011 Danan et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Danan et al. BMC Plant Biology 2011, 11:16 Page 2 of 16
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improve the estimate of targeted parameters. Meta- food crop in the world after rice and wheat. Almost all
analysis was first used in social and medical sciences, Rpi-genes (R-genes to P. infestans) deployed in the potato
like epidemiology. More recently, it was applied in plant fields have been rapidly overcome, while polygenic resis-
genetics to combine on a single map the genetic marker tance appears to be a fairly efficient and durable alterna-
data and the QTL characteristics (location, confidence tive. However, it has been observed that this kind of
interval, effect and trait used for QTL detection) from resistance in potato is often associated with plant matur-
independent QTL mapping experiments to finally esti- ity, as most resistant plants are also the ones that mature
mate the optimal set of distinct consensus QTLs, called the latest. This is a handicap for breeders and growers
meta-QTLs. The positions of those meta-QTLs are esti- who aim to get early maturing plants to shorten the time
mated with a higher accuracy as compared to the indivi- of tuber production.
dual QTLs in the original experiments [1]. To date, Attempts to get a synthetic view of the loci controlling
QTL meta-analyses have been achieved for traits related polygenic late blight resistance in potato with compari-
to plant development and plant response to environ- son of their positions with maturity QTLs have already
ment (nutrients, abiotic and biotic stresses) in maize, been published [21,22]. However, because of a lack of
wheat, rice, rapeseed, cotton, soybean, cocoa and apricot common markers, the comparison of QTLs was
[2-18]. achieved at a half-chromosome scale, which made the
Statistical methods have been proposed for the meta- compilation imprecise. Consequently, to enhance the
analysis of QTLs from several experiments. The method comparison of QTL positions coming from different
proposed by Goffinet and Gerber (2000) was implemen- mapping studies and also to refine the localization of
ted in the Biomercator software [1,19]. It compiles the hot-spot genomic regions, the mapping of common
QTLs that have been projected on an existing reference markers between maps is crucial.
map and uses the transformed Akaike classification cri- Reference dense maps constructed with transferable
terion to determine the best model between one QTL, markers are privileged sources of common markers.
two QTLs, three QTLs etc. until the maximum number A UHD potato map containing 10,000 AFLP markers
of QTLs mapped in the same region. This method was has been designed to become a reference map [23,24].
first used by Chardon et al. (2004) and by most authors However, the anchorage of AFLP markers is restricted
until recently [2,3,6,8-10,15,16]. Then Veyrieras et al. to closely-related species. In addition, as the comparison
(2007) have extended the statistical method and imple- is based on the comigration of the marker bands on the
mented the new algorithms in the MetaQTL software gel, AFLP gels are required, which does not make the
[20]. MetaQTL notably uses a weighted least squares comparison easy to achieve [25]. Other reference maps
strategy to build the consensus map from the maps of containing SSR and RFLP markers have been developed
individual studies and offers a new clustering approach in potato (SSR maps [26-28]; RFLP map [29]). These
based on a Gaussian mixture model to define the optimal markers are well defined by specific primers or a probe
number of QTL clusters or meta-QTLs on each chromo- sequence, which makes them easily transferable from
some that best explain the observed distribution of the one cross to another, even between distantly related spe-
individual projected QTLs. The Gaussian mixture model cies; they are thus handy tools for map comparison.
has shown to be flexible and robust to the non-indepen- A functional map for pathogen resistance, enriched
dence of the experiments [4]. Moreover, simulations with RGA (resistance gene analog) and DRL (defence-
demonstrated that the number of meta-QTLs selected by related locus) sequences, SNPs and InDels tightly linked
the Akaike criterion is lower than the expected number or located within NBS-LRR-like genes, has been devel-
with random distributions of QTLs and that it has a very oped on the basis of two potato populations (BC9162
low probability to happen by chance [4]. The MetaQTL and F1840 [30-33]; PoMaMo database [34]). This func-
software has successfully been used in wheat, maize, rice tional map also contains CAPS, SSR and RFLP litera-
and apricot [4,5,12,13,17]. ture-derived markers, which enables the comparison
Potato (Solanum tuberosum L.) late blight resistance is with other QTL maps. However, it remains difficult to
typically a trait for which meta-analysis can be applied. infer precisely functional locus information to QTL
From 1994 to 2009, 19 studies have been published on mapping results as QTLs often have large confidence
QTL mapping in different crosses and with different intervals.
related species, generating a significant amount of QTL QTL meta-analysis thus appears here to be an ade-
data. All these publications reflect the interest of the quate tool i) to narrow-down the confidence intervals of
potato scientific community towards polygenic partial hot-spot loci where congruent late blight resistance
resistance to late blight. Late blight, caused by the oomy- QTLs of multiple origins map, and ii) to investigate
cete Phytophthora infestans, is one of the most serious colocalization of these loci with Rpi-genes, RGAs, DRLs
diseases in potato, which is the third most important and maturity QTLs as well. In this paper, we present a
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three-step meta-analysis process achieved with the transformed data (non-parametric statistical tests or
MetaQTL software. First, we built a consensus potato ANOVA, Interval Mapping, Composite Interval Map-
map by compiling 21 QTL maps and eight reference ping or Multiple QTL Mapping with permutation tests).
maps. This consensus map includes common markers Most of the P. infestans isolates used for late blight
and specific markers tagging Rpi-genes, as well as RGA resistance assessments were of A1 mating type and viru-
and DRL markers. Second, individual QTLs for late lent towards the 11 S. demissum Rpi-genes. However, it
blight resistance and maturity were projected onto the was difficult to say whether some of the isolates used in
consensus map. Third, for each trait, QTLs were clus- the different studies were the same or not. As wild
tered into meta-QTLs on the basis of the distribution of tuber-bearing relatives of potato have proven to be
their projected positions on the consensus potato map. high-potential sources of resistance, most mapping
populations derived from a cross between a dihaploid
Results S. tuberosum clone (the susceptible parent) and a clone
Bibliographic review of QTL mapping studies derived from a diploid relative (the resistant parent).
The initial map set comprised a total of 37 maps divided Two mapping populations even derived from crosses
into i) 29 QTL maps from 19 publications related to between two potato relatives (without S. tuberosum,
QTL detection of late blight resistance and maturity Table 2). The parental pedigrees were sometimes quite
type, and ii) eight independent reference maps (without complex. Nevertheless, the marker order in all maps
any QTL) (Table 1). Reference maps were included was well conserved and aligned with the S. tuberosum
because they provided numerous pivotal markers, which map [35,36]. If all known species of the parent pedigrees
improved connections between maps. Because of a lack are taken into account, a total of 13 potato-related spe-
of shared markers, the initial 29 QTL map set was cies were involved in the meta-analysis.
refined to a core subset of 21 “connected” QTL maps
coming from 14 publications that were included in the Consensus potato map
meta-analysis (Table 1). Common markers between the 21 “connected” QTL
The 21 “connected” QTL maps were representative of maps and eight reference maps (Table 3) made it possi-
the diversity of assessments for late blight resistance and ble the construction of a consensus map for the 12
maturity, the QTL detection methods and the sources potato chromosomes. The number of maps used to con-
of resistance (Table 2). Resistance tests were based on struct each consensus chromosome varied between 20
disease spread on foliage in the field (FF) or in the and 25 (Figure 1). The consensus potato map had a
greenhouse (FG), sporulation or necrosis spots on total length of 1,260 cM (Haldane) and contained a total
in vitro detached leaflets or leaf discs (LT), necrosis pro- of 2,141 markers (SSR, SSCP, CAPS, RFLP, AFLP, SNP,
gression on stems (ST) and disease damage on tuber InDels and STS markers). Among them, 514 markers
slices (TS) or whole tubers (T% or WT) in controlled were shared by at least two different maps. There were
conditions. Maturity type was evaluated by the number between 28 and 58 common markers per chromosome,
of days before flowering or senescence (MT), plant corresponding to 16% up to 29% of the total number of
height (PH) and plant vigour (PV). QTLs were detected markers per chromosome. The name, map position and
with different statistical detection methods according to occurrence of each marker are given in Additional file 1
the number of available markers, the size of the progeny and on the SGN database [37].
and the frequency distribution profile of the raw or
QTL dataset for meta-analysis
On the basis of the 19 publications of QTL studies, a
Table 1 Number of publications, maps and QTLs total of 211 late blight resistance QTLs and 64 matur-
collected to perform meta-analysis ity QTLs were collected (Table 1). However, some
No. of No. of maps No. of QTL intervals did not include the minimum of two
publications QTLs anchor markers, which were required for their projec-
Available published data 19 (7)† 29 (8) 211 (64) tion onto the consensus map. Thus, the QTL dataset
Data included in meta- 14 (4) 21 (5) + 8††† 144 (42) for meta-analysis was reduced down to 144 late blight
analysis††
resistance QTLs and 42 maturity QTLs, coming from
First number: for late blight resistance traits; second number within brackets:
14 publications. The excluded QTLs, which harboured
for maturity traits.
† Table 2 lists all the concerned publications. a single common marker with the consensus map,
†† Only QTL maps that had a minimum of two common markers with at least were referred to “anchored QTLs” and indicated at
a chromosome of another map were included into the meta-analysis. this marker position in Additional file 1 but their
††† 8 reference potato maps without QTLs (listed in Table 3) were added to
meta-analysis to increase connections between maps through common
orientation and projected confidence interval could not
markers and to improve consensus map accuracy. be determined.
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Table 2 Published potato QTL mapping studies included in the QTL meta-analysis
Reference Cross Pop. No. of Resistance Maturity QTL
sizea maps assayc traitd detection
b
considered methode
[39] Bormann et al., -S. tuberosum Leyla x S. tuberosum Escort 84 1c FF MT LR
2004
-S. tuberosum Leyla x S. tuberosum Nikita 95
[55] Bradshaw et al., -S. tuberosum 12601ab1 x S. tuberosum Stirling 200- / FF, FG, T% MT, PH LR
2004 226
[68] Bradshaw et al., -HB193 = HB171 (S. tuberosum PDH247 x S. phureja DB226) x S. 87- / FF, FG, T% / IM
2006 phureja DB226 120
[42] Collins et al., -GDE = G87D2.4.1[(DH Flora x PI 458.388) x (DH Dani x PI 113 2 FF, TS MT, PV LR
1999 230468)] x I88.55.6 {[DH (Belle de Fontenay x Kathadin) x PI
238141]x [DH Jose x (PI 195304 x WRF 380)]} †
[35] Costanzo et al., -BD410 = BD142-1 (S. phureja x S. stenotomum) x BD172-1 (S. 132 1c FF / IM
2005 phureja x S. stenotomum)
[38] Danan et al., -96D31 = S. tuberosum CasparH3 x S. sparsipilum PI 310984 93 4 FF, ST / CIM
2009
-96D32 = S. tuberosum RosaH1 x S. spegazzinii PI 208876 116
[54] Ewing et al., 2000 -BCT = M200-30 (S. tuberosum USW2230 x S. berthaultii PI 146 1c FF / LR
473331) x S. tuberosum HH1-9
[69] Ghislain et al., -PD = S. phureja CHS-625 x S. tuberosum PS-3 92 2 FF / IM
2001
[41] Leonards- -P49xP40 = H82.368/3 (P49) x H80.696/4 (P40) †† 197 2 LT / LR
Schippers et al., 1994
[70] Meyer et al., 1998 -S. tuberosum 12601ab1 x S. tuberosum Stirling 94 / FF / LR
[71] Naess et al., 2000 -1K6 = J101K6 (S. bulbocastanum x S. tuberosum)] x S. tuberosum 64 1c FG / LR
Atlantic
[64] Oberhagemann -K31 = H80.577/1 x H80.576/16 ††† 113 1 c (K31) LT MT, PV LR
et al., 1999
-GDE = G87D2.4.1 [(DH Flora x PI 458.388) x (DH Dani x PI 109
230468)] x I88.55.6 {[DH (Belle de Fontenay x Kathadin) x PI
238141]x [DH Jose x (PI 195304 x WRF 380)]} †
[72] Sandbrink et al., -89-13 = S. microdontum MCD167 x S. tuberosum SH 82-44-111 67 1 (MCD167) FF / IM
2000
-89-14 = S. microdontum MCD167 x S. tuberosum SH 77-114-2988 46
-89-15 = S. microdontum MCD167 x S. tuberosum SH 82-59-223 47
-89-16 = S. microdontum MCD178 x S. tuberosum SH 82-44-111 82
-89-17 = S. microdontum MCD178 x S. tuberosum SH 77-114-2988 67
-89-18 = S. microdontum MCD178 x S. tuberosum SH 82-59-223 58
[40] Simko et al., 2006 - BD410 = BD142-1 (S. phureja x S. stenotomum) x BD172-1 125 1c WT MT MQM
(S. phureja x S. stenotomum)
[57] Sliwka et al., 2007 -98-21 = DG 83-1520 (P1) x DG 84-195 (P2) †††† 156 2 LT, TS MT LR
[73] Sorensen et al., -HGG = S. tuberosum 89-0-08-21 x S. vernei 3504 70 1 c (HGG) FF / MQM
2006
-HGIHJS = S. tuberosum 90-HAE-42 x S. vernei 3504 107
[36] Villamon et al., -PCC1 = MP1-8 (S. paucissectum PI 473489-1 x S. 184 1c FF, FG / CIM
2005 chromatophilum PI 310991-1) x S. chromatophilum PI 310991-1
[56] Visker et al., 2003 -CxE = USW5337.3 (S. phureja x S. tuberosum) x USW5337.3 67 / FF MT MQM
(S. vernei × S. tuberosum)
[58] Visker et al., 2005 -Progeny 5 SHxCE = S. tuberosum SH82-44-111 x CE51 227 / FF MT IM
(S. phureja x (S. vernei x S. tuberosum))
-Progeny 2 DHxI =S. tuberosum DH84-19-1659 x I88.55.6 201
((S. tuberosum x S. stenotomum) x S. tuberosum x S. stenotomum)
a
Population size for mapping; numbers could vary according to the phenotypic assessments for late blight resistance and maturity traits.
b
A single number indicates the number of parental maps included in meta-analysis, otherwise the parental map which has been included is given; c: consensus
map;/: no map was included because of a lack of common markers.
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c
Resistance assay: FF: foliage test in field, FG: foliage test in glasshouse, T%: tuber test in percentage of the number of infected tubers, WT: whole tuber test by
scoring the tuber damage, TS: tuber slice test, LT: leaf test, ST: stem test.
d
Maturity trait: MT: maturity type (assessment based on visual classification of senescence of the foliage), PH: plant height, PV: plant vigour.
e
LR: linear regression, IM: simple interval mapping, CIM: composite interval mapping, MQM: multiple QTL mapping.
†G87D2.4.1 pedigree includes S. kurtzianum, S. vernei, S. tuberosum, and S. tarijense; I88.55.6 pedigree includes S. tuberosum and S. stenotomum [64].
††P40 pedigree includes S. tuberosum and S. spegazzinii [41].
†††Unknown pedigree [64].
††††Parental clone pedigrees of 98-21 population include S. tuberosum, S. chacoense, S. verrucosum, S. microdontum, S. gourlayi, S. yougasense [57].

As far as the QTLs included in the meta-analysis are (chromosome XI [42]) and 61 cM (chromosome VI [42]),
considered, late blight and maturity QTLs spread on the with a mean of 20 cM.
12 potato chromosomes. The number of QTLs per
chromosome ranged between six and 21 for late blight Meta-analysis
resistance, and between one and eight for maturity. We determined the number of meta-QTLs per chromo-
For late blight resistance, R² values were available for some by using the modified Akaike Information Criterion
106 QTLs out of the 144 input QTLs and ranged (AICc) and by taking into account the consistency with
between 4% (chromosome I, foliage test [38]; chromo- the different criteria provided by the MetaQTL software
somes V, IX, XI, XII, foliage test [39]) and 63% (chromo- (Additional file 2). Our analysis yielded a total of 32
some X, tuber test [40]). 75% of the late blight QTLs had meta-QTLs. Each meta-QTL corresponded to clusters of
relatively small effects, ranging between 4% and 15%; 7% individual QTLs coming from different experiments.
of the QTLs had large effects, ranging between 30% and Meta-QTLs were composed of a maximum of 18 indivi-
63%. Confidence intervals ranged between 3 cM (chro- dual QTLs for late blight resistance (chromosome V) and
mosome III, leaf disc test [41]) and 66 cM (chromosome eight individual QTLs for maturity (chromosome V). The
VI, foliage test [42]), with a mean of 24 cM. QTL meta-analysis on the whole potato genome reduced
For maturity, R² values were available for 20 QTLs out by six-fold the initial number of late blight QTLs by pas-
of the 42 input QTLs and ranged between 4% (chromo- sing from 144 QTLs to 24 meta-QTLs and by ca. five-
somes IX and XII [39]) and 71% (chromosome V [42]). fold the number of maturity QTLs by passing from
75% of the maturity QTLs had R² values ranging between 42 QTLs to eight meta-QTLs. Figure 2 presents an exam-
4% and 15%; 10% of the QTLs explained more than 30% ple of the meta-analysis steps for chromosome IV, from
of the phenotypic variation (60% and 71% on chromosome QTL projection on the consensus map to QTL clustering
V [42]). Confidence intervals ranged between 4 cM into meta-QTLs.

Table 3 Published potato reference maps included in the QTL meta-analysis

Reference Cross Pop. No. of maps Marker types
sizea consideredb
[30,34] -F1840 = H82.337/49 (P18) x H80.696/4 (P40) †† 100 2c SSR, STS, RFLP, CAPS,
Gebhardt et al., 1991 BAC, pathogen
PoMaMo resistance
genes, DRL, RGA
-BC9162 = MPI= (H81.691/1 x H82.309/5) x H82.309/5)
[28] -Germicopa = GDE = G87D2.4.1[(DH Flora x PI 458.388) x (DH Dani x PI 91 2c SSR, RFLP, AFLP,
Milbourne et al., 1998 230468)] x I88.55.6 PCR-markers
{[DH (Belle de Fontenay x Kathadin) x PI 238141] x [DH Jose x (PI
195304 x WRF 380)]}
-MPI = BC9162 = (H81.691/1 x H82.309/5) x H82.309/5) 67
[26,29,37,74] -BCB = N263 = M200-30 (S. tuberosum USW2230 x S. berthaultii PI 150- 2c SSR, RFLP
Bonierbale et al., 1988 473331) x S. berthaultii PI 473331 155
Tanksley et al., 1992
Feingold et al., 2005
SGN
-N271=BCT= M200-30 (S. tuberosum USW2230 x S. berthaultii PI 473331) 150
x S.tuberosum HH1-9
[27] Integated SSR map based on SSR positions across 3 maps: BCT, PD, 92 1c SSR, RFLP
Ghislain et al., 2009 PCC1
[75] S. tuberosum 86.61.26 x S. tuberosum 84.194.30 152 1c SSR, AFLP, CAPS
Yamanaka et al., 2005
a b
, , ††: detailed in the caption of Table 2.
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and maturity QTLs altogether under a single “super-

250
No. common markers trait”, we observed that for all 12 chromosomes, matur-
43 No. individual markers ity QTLs were always clustered together with late blight
200
Number of markers

resistance QTLs in a “super meta-QTL” (data not

56 44 58
150 28 45 38 48 shown). On the other way round, we observed at least
38 46 one “super meta-QTL” free of maturity QTLs for 11
35 35
100
chromosomes; for chromosome XI only, both “super
meta-QTLs” included at least one maturity QTL.
50 The three most consistent late blight meta-QTLs were
located on chromosomes IV, V and X (MQTL_1_La-
0 te_blight of chromosome IV, MQTL_1_Late_blight of
I II III IV V VI VII VIII IX X XI XII chromosome V and MQTL_2_Late_blight of chromo-
.122 .102 .111 .83 .143 .108 .67 .121 .130 .98 .76 .100
some X; Additional file 3). These meta-QTLs were com-
cM cM cM cM cM cM cM cM cM cM cM cM posed of the highest number of QTLs (10 to 18 QTLs)
:22 :25 :22 :22 :25 :21 :20 :23 :23 :24 :24 :22 with the largest effects (R² up to 63%, tuber test [40]).
In addition, they corresponded to individual QTLs iden-
Potato chromosomes tified in different potato-related species or in plant
. Length in cM
: Number of integrated individual chromosome maps material with complex pedigree. This result suggests
that these regions could correspond to conserved resis-
Figure 1 Characteristics of the consensus potato map. For each
of the 12 potato chromosomes, the bar represents the total tance QTLs retrieved from several tuber-bearing Sola-
number of markers, the upper part corresponding to the proportion num species.
of common markers between at least two individual maps. The
length of the consensus chromosome maps in cM (Haldane) and Candidate gene analysis
the number of individual maps used for their construction are
Literature reported the map positions of several Rpi-
indicated for each chromosome, below the bars.
genes determining late blight resistance (reviewed in
[43,44]). However, only a few flanking markers were sup-
A graphical overview of the late blight and maturity plied (Rpi-genes were linked to a single marker or
meta-QTLs is presented on Figure 3. Late blight meta- included in a large marker interval), which hampered the
QTLs spread on the 12 chromosomes, with one to three accurate location of Rpi-genes on the consensus map
meta-QTLs per chromosome. Maturity meta-QTLs (Additional file 1). Due to their rough positions, it was
spread on only six chromosomes, with one or two meta- thus not possible to say definitely whether they were
QTLs per chromosome. Other maturity QTLs were included or not in the late blight meta-QTLs. Out of the
reported in literature on the other six chromosomes, 33 Rpi-genes positioned on our consensus potato map,
but they were single in their region and no meta-QTL 10 were included in the confidence intervals of late blight
could be computed. Single QTLs for late blight resis- meta-QTLs (Table 4). One example of overlap was on
tance and for maturity that were excluded from the chromosome IV, where the TG370-TG339 marker inter-
clustering step are shown in Additional file 1, with the val (~12 cM) containing a large NBS-LRR Rpi-gene clus-
other excluded QTLs which were anchored by a single ter (R2-like genes) largely overlapped the meta-QTL
marker to the consensus map. MQTL_1_Late_blight [45]. On chromosome VI, the
The confidence intervals of late blight meta-QTLs CT119 marker tagging the Rpi-blb2 R-gene was included
ranged between 0.27 cM (chromosome VII) to 49.81 cM in MQTL_1_Late_blight. On chromosome X, the TG422
(chromosome I), with a mean of 10.25 cM (SD±10.79). and TG403 markers flanking the Rpi-ber2 gene were
The confidence intervals of maturity meta-QTLs ranged included in MQTL_2_Late_blight. However, on chromo-
between 0.88 cM (chromosome V) to 39.28 cM (chro- some XI, the lack of anchor markers hindered the accu-
mosome VI), with a mean of 10.67 cM (SD±12.54). rate location of the 10 Rpi-genes (Rpi-Stirling, R5 to R11,
With respect to the length reduction of the mean confi- R3a and R3b). According to the flanking markers
dence interval from the published QTLs to the meta- (STM5130-STM5109 for Rpi-Stirling, TG105-GP250 for
QTLs, confidence intervals were reduced by 2.3-fold for R3a, TG26 for R3b and R5 to R11), only Rpi-Stirling
late blight resistance and by 1.9-fold for maturity (Addi- might be included in MQTL_2_Late_blight.
tional file 3). Conversely, a few Rpi-genes clearly did not belong to
Maturity meta-QTLs overlapped late blight meta- any late blight meta-QTLs. This was the case for Rpi1
QTLs on chromosomes VI and XI, while there was no on chromosome VII and for the Rpi-vnt1, Rpi-phu1 and
overlap on chromosomes IV, V, VII and VIII. However, Rpi-mcq1/moc1 loci of chromosome IX. In three addi-
by running meta-analysis on late blight resistance QTLs tional cases, the distinction between Rpi-genes and late
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Projected individual QTLs Meta-QTLs

Collins99_G87_42
Leonards94_P40_41_Pi1a

Collins99_G87_41
Collins99_I88_41

Bormann04_Leyla_41
Sliwka07_P2_42

Collins99_G87_43

MQTL_1_Maturity
Leonards94_P49_41_Pi1(g)

Oberhagemann99_K31_41
Leonards94_P40_42_Pi1b

MQTL_1_Late_blight
Sliwka07_P2_43
Sliwka07_P1_42b
Danan09_ROSA_41
Sliwka07_P1_41
Sliwka07_P1_43

Collins99_I88_42
Leonards94_P40_43_Pic

Sandbrink00_MCD167_41
Leonards94_P49_42_Pi0(g)

MQTL_2_Late_blight
Leaf disc Leaflet Whole Tub. St. Fol. Mat. Vig.
tuber slice field
5 cM
Late blight resistance tests Maturity tests
Figure 2 Meta-analysis steps from QTL-projection on the consensus map to clustering into meta-QTLs: chromosome IV example.
Projected QTLs (quantitative trait loci) are represented by vertical bars to the left of the consensus chromosome IV. Their length is representative
of their confidence interval once projected on the consensus map. They are sorted into assessment type, within late blight resistance traits (Leaf
disc, Leaflet, Whole tuber, Tuber slice, Stem, Foliage in field), on one hand, and within maturity traits (Maturity, Vigour), on the other hand. QTL
names are written to the left of the bars. QTL nomenclature is as follows: the name of the first author of the original publication juxtaposed to
the last two digits of the publication year, the name of the population consensus map or of the parental map where the QTL was detected, and
an Arabic number that can be followed by a letter. This latter Arabic number is the number of the chromosome juxtaposed to the QTL
mapping order on the chromosome; a letter was sometimes added to distinguish colocalizing QTLs that were detected with different traits. For
Leonards-Schippers et al.’s study, the original name of the QTL was added [41]. Ticks on the consensus chromosome indicate marker positions.
Marker names are only shown for markers that occur at least in four maps out of the 21 compiled maps. Vertical thick bars to the right of the
consensus chromosome indicate Meta-QTLs. Late blight meta-QTLs are in black and maturity meta-QTLs are in grey. Their length is
representative of their confidence interval. To show clearly the results of the clustering step, the QTLs or part of the QTLs that were assigned to
the ‘MQTL_1_Late_blight’ meta-QTL are in plain line and those assigned to the ‘MQTL_2_Late_blight’ meta-QTL are in dotted line. The QTL
Collins99_I88_42 was not clustered to any late blight meta-QTL and was reported as an outlayer QTL in Additional file 1.

blight meta-QTLs was doubtful. On chromosome V, R1 MQTL_2_Late_blight [46]. On chromosome X, the

gene (BA213c14 and BA87d17 BACs) was located less Rber/Rpi-ber1 locus was located between both meta-
than 2 cM far below the lower bound of MQTL_1_- QTLs of this chromosome, in a 3-cM interval (Addi-
Late_blight. On chromosome VIII, the RB cluster (Rpi- tional file 1).
blb1, Rpi-pta1, Rpi-plt1, Rpi-sto1, tagged by RB marker) In total, 80 RGAs and 72 DRLs were reported on our
was located 1 cM far up to the upper bound of consensus map, mainly from the PoMaMo functional
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I II III IV V VI

VII VIII IX X XI XII

5 cM
Late blight meta-QTL
Maturity meta-QTL

Figure 3 Graphical overview of the late blight and maturity meta-QTLs. The 12 consensus potato chromosomes are represented by 12
vertical thick bars. Ticks on the consensus chromosome indicate marker positions. Marker names are only shown for markers that occur at least
in four maps out of the 21 compiled individual maps. Vertical thick bars to the right of the consensus chromosomes represent Meta-QTLs. Late
blight meta-QTLs are in black and maturity meta-QTLs in grey. Their names start with “MQTL”, followed by their position rank on the consensus
chromosome from the top to the bottom of the chromosome, and the concerned trait used for clustering (Late_blight for late blight resistance
trait and Maturity for maturity trait).
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map [32,34]. Fourteen RGAs and 26 DRLs belonged to at least three maps come from the cultivated potato spe-
late blight meta-QTLs that covered about 20% of the cies (S. tuberosum) and 23 maps from crosses between
consensus map (Table 4). Comparatively, 24 RGAs and S. tuberosum and potato wild relatives (S. microdontum,
nine DRLs belonged to maturity meta-QTLs that cov- S. phureja, S. sparsipilum, etc., Tables 2 and 3). Sixteen
ered about 7% of the consensus map (Additional file 1). maps are already consensus maps of both parents, with
Independency Chi-2 tests indicate that the number of generally one being a S. tuberosum clone and the other
RGAs and Rpi-genes are under expectation in late blight one a resistant wild potato species. This ability to com-
meta-QTLs (p-value=0.035 under the hypothesis of pile genetic map information of S. tuberosum and its
independency) and over expectation in maturity meta- wild relatives indicates a high level of conservation of
QTLs (p-value<0.0001). The heterogeneous distribution the marker order, and thus, of genomic sequences all
of RGAs and Rpi-genes corroborate the fact that they over the genome. This stresses the very close genetic
are often clustered or alleles. Conversely, the distribu- relationships of those genetic backgrounds and gives evi-
tion of DRLs was independent on the distribution of dence of the validity to compile their deriving published
both late blight meta-QTLs (p-value=0.323) and matur- QTL data produced with their maps. The genetic rela-
ity meta-QTLs (p-value=0.909). tionships between the cultivated potato and its wild rela-
tives have been described in details by Spooner et al.
Discussion (2008) [47].
A dense consensus reference potato map for map Composed of 2,141 markers, the consensus map con-
comparisons structed in our study constitutes a new valuable dense
Twenty-nine published potato maps were merged reference map of potato. Marker positions are available
together into a single consensus map. From the infor- on the SGN database, enabling map comparisons
mation available in the publications of the genetic maps, [37,48]. This map can be used either as a source of

Table 4 Number of collected individual QTLs, meta-QTLs, and colocalizations with Rpi-genes, RGAs and DRLs, per
chromosome
Chrom. No. maturity No. No. late blight No. Rpi-genes No. Rpi-genes No. RGAs No. DRLs
QTLs included maturity resistance QTLs late positioned on colocalizing with colocalizing colocalizing
in meta- meta- included in meta- blight the consensus late blight meta- with late blight with late blight
analysis/No. QTLs analysis/No. QTLs meta- map QTLs/No. Rpi- meta-QTLs/No. meta-QTLs/No.
QTLs QTLs genes RGAs DRLs
I 3/3 0 10/10 2 - 0/0 0/10 4/8
II 1/1 0 6/7 3 - 0/0 5/7 5/8
III 3/4 0 15/21 3 - 0/0 0/2 0/5
IV 4/4 1 15/36** 2 R2, R2-like, Rpi- 7/7 2/7 1/5
blb3, Rpi-abpt,
Rpi-demf1, Rpi-
mcd, Rpi-mcd1
V 8/29* 1 21/44*** 2 R1 0/1 0/14 0/3
VI 5/5 2 8/12 2 Rpi-blb2 1/1 1/5 6/9
VII 3/3 1 9/12 1 Rpi1=Rpi-pnt1 0/1 0/4 0/2
VIII 6/6 1 12/13 2 RB, Rpi-blb1, Rpi- 0/5 0/2 3/11
pta1, Rpi-plt1,
Rpi-sto1
IX 1/1 0 9/13 1 Rpi-vnt1.1, Rpi- 0/5 0/2 1/9
vnt1.2, Rpi-vnt1.3,
Rpi-phu1, Rpi-
moc1= Rpi-mcq1
X 1/1 0 15/18 2 Rber=Rpi-ber1, 1/2 1/8 3/6
Rpi-ber2
XI 6/6 2 14/15 2 R3a, R3b, R5, R6, 1/11 5/18 3/3
R7, R8, R9, R10,
R11, Rpi-pcs, Rpi-
stirling
XII 1/1 0 10/10 2 - 0/0 0/1 0/3
Total 42/64 8 144/211 24 - 10/33 14/80 26/72
*18 QTLs, **15 QTLs, ***17 QTLs, in Bradshaw et al. [55].
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markers for regions of interest or as an anchor reference Consortium is currently exploiting the high genomic
map. However, for regions with a high density of mar- similarity between S. tuberosum and S. phureja to
kers, precise marker order has to be taken with care as reduce the complexity in assembly supports this hypoth-
the marker positions were calculated according to the esis [49]. A high level of sequence conservation was also
positions of common markers from different maps and observed at the nucleotide level of the coding sequence
not based on recombination fractions. Thus, precise among six Solanaceae genera (potato, tomato, pepper,
marker positions have to be checked by mapping in a petunia, tobacco and Nicotiana benthamiana) [50].
large population. Because the number of sequence matches among differ-
One feature of this consensus map is that markers are ent Solanaceae EST libraries was inversely correlated
not regularly spread along the chromosomes and tend with the phylogenetic distance, we assume that the
to concentrate in the medium regions. For example, on tuber-bearing species are also very similar at the level of
chromosome VIII, 18 markers are spread on the top expressed genes. These hypotheses have been already
71 cM while 167 markers are spread on the next 29 cM. proposed in other genera where meta-analysis was con-
This phenomenon is indeed observed on the published ducted across relatives (e.g. for cotton fiber [15] and for
maps where dense regions are often assimilated to cen- rice blast [2]). In potato, resistance QTLs from one
tromeric regions characterized by a small number of population frequently mapped, as far as resolution
recombinations and consequently compressed maps. We allows, in close proximity to those described in other
also assume that genomic regions known to be involved populations. At the gene level, high sequence homology
in late blight resistance mostly gather in medium of Rpi genes were described between potato relatives.
regions, which had been enriched with markers. Functional homologues of the R2 resistance gene to
Another explanation would be that distal markers gen- P. infestans located on potato chromosome IV were
erally originate from a single published map and their cloned by an allele mining approach in three related
positions could be due to genotyping errors or skewed species, and recognized the same effector protein of
segregations. P. infestans [45]. Rpi genes and their general functions
are overall well conserved across potato related species,
A clear picture of the structural organization of late variation being in fact limited to differences at the base
blight resistance loci on the potato genome pair and allele function levels [51]. At last, in a recent
The synthetic potato map with meta-QTLs offers a published study, meta-analysis was performed on popu-
refined overview of the structural organization of the lations involving different species related to bread wheat
loci of polygenic resistance to late blight in terms of to narrow-down the interval of a QTL controlling the
number of QTLs and lengths of confidence intervals. By nitrogen use efficiency [52]. The functional underlying
reducing the number of resistance loci by a factor of six gene has been identified and showed to be conserved at
(from 144 QTLs to 24 meta-QTLs), meta-analysis high- orthologous positions in wheat species and in much
lights the well-known resistance gene clusters on chro- further related cereals species such as rice, sorghum and
mosomes IV and V, and also points out loci which had maize. These different elements demonstrate that the
not appeared as notable in individual experiments like analysis of the genetic factors controlling a trait across
the loci on chromosomes I, III, VII, and XII. Twenty- genomes of different related species and even of differ-
four meta-QTLs summarized about 96% of the indivi- ent genera of a plant family can be very powerful to per-
dual QTLs included in the analysis, which illustrates the form a map-based dissection of a conserved gene that
power of QTL meta-analysis to combine QTLs from controls the same trait in several species.
various studies. In our study, the locus confidence intervals have been
One may question the validity of such QTL meta-ana- reduced by 2.3-fold in average. Locus accuracy has espe-
lysis compiling information of as different species as the cially increased for the loci for which colocalizing QTLs
cultivated potato (S. tuberosum) and its wild relatives are numerous, like on chromosome V where 18 coloca-
(S. stenotomum, S. berthaultii, S. bulbocastanum, etc.). lizing QTLs with an averaged confidence interval of
However, as we explained earlier, this meta-analysis 23 cM were clustered into a single meta-QTL of only
could only be performed thanks to the presence of com- 5 cM. In this way, meta-analysis refines the genomic
mon molecular markers mapped in a conserved order regions of interest frequently described. This enables the
across maps of different related species. This structural determination of a set of markers for selection and a
tight genetic relationships of the different backgrounds reasonable list of candidate genes when the genetic map
sets up the hypothesis that the same genes are present is anchored to the annotated genome sequence. The clo-
in the same order in the genome across species, and sest flanking markers of the locus are also provided for
that the genetic variation, if any, would take place at the subsequent fine-mapping in a real large population for
allele level. The fact that the Potato Genome Sequencing map-based gene cloning.
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However, confidence intervals of meta-QTLs have to individual maturity QTLs excluded from the meta-ana-
be taken with caution, as they are the result of two suc- lysis but anchored with a single common marker, other
cessive statistical transformations (projection onto a con- overlaps were presumed with late blight meta-QTLs on
sensus map and clustering), based themselves on the chromosome I, II, V, and XII, and reciprocally individual
individual QTL confidence intervals. This stresses the late blight QTLs overlapped maturity meta-QTLs on
importance of the accuracy of the initial mapping data. chromosomes IV, V, VI, VII, and XI (Additional file 1).
For our analysis, we took into account the individual In these cases, either pleiotropic genes might control
QTL confidence intervals as described in the original both traits, or the resolution is not accurate enough to
publication when available (interval length of a certain distinguish two closely linked genes.
LOD decrease). Otherwise, the confidence interval esti- The most famous association between QTLs for late
mate was calculated with the empirical formula of Dar- blight resistance and for maturity is located on the
vasi and Soller (1997) whose accuracy depends on the upper part of chromosome V [39,40,42,55-57]. Here,
population size and the QTL effect [53]. To reduce the meta-analysis results show that the maturity meta-QTL
risk of giving artificially too much weight to a locus, we MQTL_1_Maturity consisting in eight maturity QTLs
made a quite strict selection of the individual QTLs to be reported for this chromosome was very close but dis-
included in the meta-analysis by removing all possible tinct from the most consistent late blight meta-QTL
redundancy (e.g. several repetitions or related traits in MQTL_1_Late_blight consisting in 18 individual QTLs.
the same experiment). In our study, five meta-QTLs This result goes rather in favour of the hypothesis that
displayed confidence intervals lower than 1 cM (on chro- each trait would be controlled by independent genes but
mosomes III, V, VII, VIII and XI), while the confidence very closely linked. Nevertheless, this result has to be
interval of individual QTLs varied greatly. In these taken with care as two individual maturity QTLs that
regions, the consensus map appeared condensed in com- were not included in the meta-analysis were anchored
parison with the original maps; therefore, the projected to markers of the confidence interval of MQTL_1_La-
confidence intervals of individual QTLs were very tight. te_blight. Also, another individual late blight QTL was
Löffler et al. (2009) have also found in wheat a very tight anchored to a marker of the MQTL_1_Maturity’s confi-
meta-QTL of 0.1 cM that encompassed six QTLs only dence interval (Additional file 1).
[12]. These over-reduced confidence intervals underline Cases of clearly distinct maturity and late blight meta-
the necessity to validate the marker-trait association, QTLs were found on chromosomes IV, VII and VIII; the
either by association mapping or by transcriptomics hypothesis of a pleiotropic gene would then be excluded
when possible as performed by Norton et al. (2008) [14]. for these regions. In addition, anchored individual matur-
The meta-analysis implemented by the Meta-QTL ity QTLs did not coincide with late blight meta-QTLs on
software assumes that QTL experiments are indepen- chromosomes III and X, corroborating the independence
dent from each other. Therefore, it could not take into of late blight and maturity loci in these regions as sug-
account common features to several studies, such as the gested in previous studies [39,40,55,58]. The clearest
relatedness between mapping populations or between cases of physical independency between maturity and
Phytophthora isolates that would have increased the late blight resistance QTLs could be preferential targets
power of the analysis. Nevertheless, by projecting QTLs for introgression into elite cultivars for late blight resis-
on the same consensus map, meta-analysis still makes it tance breeding.
possible to rapidly compare QTL mapping results of
linked studies and highlights QTLs conferring isolate- Candidate genes for late blight resistance QTLs
specific resistance (same population and assessment but Most frequent hypotheses about resistance QTLs were
different isolates [54,55]) or with tissue-specificity effect either defeated R-genes with residual effects or defence
(same population and isolate but assessments on foliage genes. The confidence intervals of the late blight meta-
and tuber [35,40]). Another limit of the meta-analysis QTLs of chromosomes IV, VI, X and XI include
implemented in MetaQTL is that it does not provide R-genes of the NBS-LRR class (R2 cluster, Rpi-blb2, Rpi-
the direction of the allelic effects, meaning that QTLs ber2 and Rpi-Stirling respectively). The late blight resis-
composing a meta-QTL can have opposite direction tance locus of chromosome IV was particularly well
alleles. Consequently, we have to come back to the indi- documented with the Stirling cultivar and S. microdon-
vidual QTL data to be able to select the origin of the tum cases of study [55,59,60]. The detection of the same
target favourable allele. locus as an R-gene or a QTL can be accounted for sev-
eral factors such as the allelic form of the gene (for
Polygenic late blight resistance and maturity relationships instance, defeated complete resistance alleles could be
Late blight meta-QTLs overlapped maturity meta-QTLs detected as QTLs), the composition of the pathogen iso-
on chromosomes VI and XI. In addition, if we consider late, the way of scoring the disease or the genetic
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background. Bhaskar et al. (2008) demonstrated that the the same family, as achieved between rice and maize [67].
resistance level conferred by the RB gene was dependent This opens a new type of analysis that would integrate
on the quantity of proteins encoded by the essential cell gene evolution and functional conservation.
cycle regulator SGT1 gene. This showed the importance To improve meta-analysis, it would be necessary to
of the genetic background in the efficiency of R-gene- integrate the relationships between parental clones
triggered disease resistance [61]. A parallel can be made across experiments, along with their pedigree, to be able
with the fact that quantitative resistance is often con- to determine the donors of resistant alleles. In addition,
trolled by a few large-effect QTLs in association with adding information on P. infestans isolates used for
several minor-effect QTLs which can interact with the resistance assessments would enlighten on the resistance
major QTLs to modulate the expression of the given spectrum mediated by meta-QTLs, which is one of the
trait (reviewed in [62]). predictors of the durability of resistance to pathogens.
By analysing colocalizations between the 24 late blight We assume that broad-spectrum meta-QTLs probably
meta-QTLs and the 33 Rpi-genes, 80 RGAs and 72 target essential functions of the pathogen and that
DRLs, we observed that 25% of late blight meta-QTLs meta-QTLs supported by QTLs detected from several
included RGAs (33% included Rpi-genes or RGAs), and genitors or related species probably provide a selective
50% included DRLs. It also appeared that the frequency advantage. Consequently, we presume that meta-QTLs
of RGAs was not significantly greater inside late blight with a broad-spectrum and retrieved from different
meta-QTL confidence intervals than outside, and that genitors correspond to constrained genes, and could
DRLs were neither significantly associated with late therefore be preferential targets to increase the durabil-
blight meta-QTLs, nor with maturity meta-QTLs. Even ity of the resistance.
if our analysis was biased by the limited number of can-
didate genes and QTLs, our results do not favour one Methods
particular hypothesis for molecular basis of resistance Consensus potato map
QTLs rather than another, corroborating Ballini et al.’s The construction of the consensus map was performed
conclusions [2]. However, the meta-analysis presents the chromosome by chromosome. To be able to align the
advantage to reduce QTL confidence intervals, which chromosome maps in the right orientation, a chromo-
contributes to increase the resolution in selecting rele- some of a study should contain a minimum of two com-
vant candidate genes. As an example, the StAOS2 gene mon markers with the corresponding chromosome of
encoding the potato allene oxide synthase 2 was located another study. QTL maps that did not share common
within the MQTL_2_Late_blight’s confidence interval. markers were discarded from the construction of the
Pajerowska-Mukhtar et al. (2008) showed that the nat- consensus map. For several maps, few chromosomes
ural variation of this gene was associated with a late were also missing, which lead to a variation of the num-
blight resistance QTL identified by Oberhagemann et al. ber of input maps depending on the chromosome
(1999) [63,64]. Such congruency between meta-analysis (Figure 1).
and fine mapping results was also reported for the Vgt1 In case of inversions of two markers between maps,
QTL in maize [20,65]. only the marker that was present in the lowest number
of maps was manually removed to ensure that the most
Conclusions frequent common markers would be systematically
In our study, we produced the first consensus map and retained. We repeated this process until no more inver-
performed the first meta-analysis dealing with both sion was observed between maps.
development trait and resistance to a biotic stress in The ConsMap command of the MetaQTL software
potato. Through this study, we demonstrated that, as version 1.0 was used to create the consensus marker
soon as a large amount of QTL data is collected from dif- map [20]. The implemented method is based on a
ferent studies and connected by common genetic mar- Weighted Least Square (WLS) strategy, which made it
kers, meta-analysis becomes a powerful tool to highlight possible to compile all the input maps into a consensus
chromosomal regions to focus further researches on and map in a single step. It takes into account the distances
to use in breeding. To narrow-down the target loci confi- between adjacent markers from all individual maps
dence intervals, it is thus worth systematically integrating rescaled in Haldane unit. The size and type of the map-
all new QTLs into meta-analysis on a regular basis. The ping population are used to estimate the map accuracy
anchorage of the new annotated potato genome sequence and are integrated into the compilation. Marker names
to meta-QTLs will especially provide interesting targets and positions were provided in the input map files,
for candidate gene approach and for marker-assisted along with a file specifying the synonymous names of
breeding [66]. Meta-analysis could also be useful for the same markers that were mapped in different maps
comparative QTL mapping across widely related crops of (Additional file 4 and on the SGN database [37]).
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QTL meta-analysis were the lowest relatively to the criteria values of the
QTL meta-analysis was performed with the MetaQTL other possible models. It corresponds to the optimal
software version 1.0 [20]. MetaQTL requires a minimal number of clusters that best explain the observed QTL
set of descriptors characterizing each observed QTL: the distribution along the consensus chromosome map. As
QTL position, its confidence interval and/or its indivi- a result, each meta-QTL position and confidence inter-
dual R² value (at least one of them is mandatory), the val correspond to the consensus position of all the indi-
trait related to the QTL and the size of the QTL map- vidual QTLs attributed to this meta-QTL, weighted by
ping population used for the QTL detection. The statis- their individual accuracies and probability of being
tical method implemented in the MetaQTL software attributed to the meta-QTL.
hypothesizes that the input mapping studies are inde- A two-round QTL meta-analysis was adopted. First, a
pendent from each other. QTL mapping studies, which meta-analysis was performed by declaring late blight
were repeated in time and space, often detected redun- resistance distinct from maturity in the trait ontology;
dant QTLs at the same position for the same trait. In separated meta-QTLs were thus obtained for each trait
that case, we kept only the QTL with the highest effect in the same analysis. In the second round of QTL meta-
(R²) to avoid the attribution of a too strong weight to analysis, both traits were merged into one single “super
that QTL in the meta-analysis. trait”. The purpose of this second round was to investi-
QTLProj command enabled the homothetic projection gate whether maturity QTLs tended to cluster with late
of the positions and the confidence intervals of the indi- blight resistance QTLs or not. For convenience, meta-
vidual QTLs onto the consensus map. It is based on a QTLs of late blight resistance were called “late blight
scaling rule between the positions of the flanking mar- meta-QTLs”, and meta-QTLs of maturity, vigour and
kers of the QTLs on their original maps and the posi- plant height were called “maturity meta-QTLs”.
tions of these markers on the consensus map. The
MetaQTL software first took into account the confi- Additional material
dence interval reported in the study if available, other-
wise an estimation of the confidence interval was Additional file 1: Description of the consensus map with meta-QTLs
calculated using the empirical formula proposed by Dar- positions, additional individual QTLs, Rpi-genes, RGAs and DRLs.
The chromosome Arabic numbers, the locus names, and the positions of
vasi and Soller (1997) [53]: CI=530/NxR², where N is the loci on the consensus map (in cM, Haldane unit) are listed in the
the population size and R² the QTL effect as reported in ascending order of marker positions, from chromosome I to
the individual study. This formula generally gives larger chromosome XII. The occurrence number of the markers across the 21
compiled maps is indicated (meta.occurrence). The “type” information
confidence interval than the usual interval length of indicates whether the locus is a marker (M) or a meta-QTL (Q). If the
LOD-1 decrease. We used trait ontology to classify and marker sequence has been previously described as being a resistance
group original trait names according to their relatedness. gene analog (RGA) or a defence-related locus (DRL) (information mainly
retrieved from the PoMaMo database), the type “M_RGA” or “M_DRL” is
QTLClust command performed the clustering of the mentioned; in this case, a short description about the sequence is added.
projected QTLs referring to the same trait on a given Rpi-gene (R-gene to Phytophthora infestans) most probable locations are
chromosome into all possible numbers of hypothetic indicated by shaded areas between their two closest flanking markers, as
described in literature. Unless markers were designed from known Rpi-
clusters or “models”, i.e., from the model consisting in gene sequences (as for RB gene), Rpi-genes have most of the time an
only one hypothetic cluster to the model consisting in approximate location on the consensus map. Overlapping locations of
as many clusters as the total number of individual QTLs Rpi-genes in the same region are indicated in two different columns of
the table. Rpi-genes with different names are considered as being
reported for the chromosome. For a given model, a different genes, even if they are alleles [44].The columns “qtl.ci.from” and
Gaussian mixture approach was applied to jointly per- “qtl.ci.to” indicate the range of the meta-QTL confidence interval on the
form a quantitative clustering of the projected QTLs consensus map. In the table, the confidence intervals of late blight meta-
QTLs are framed in blue while those of maturity meta-QTLs are framed
and estimate meta-QTL positions and confidence inter- in red, and overlapping regions in purple. The column “meta-QTL trait”
vals by maximizing the likelihood of the initial QTL specifies the meta-QTL trait: late blight resistance (Late_blight) or
positions. The clustering could only be performed in the maturity (Maturity).The columns “anchored QTL, trait” and “outlayer QTL,
trait” show additional QTLs that have not been compiled in the final
genomic regions where at least two QTLs overlapped. If meta-analysis. The QTL nomenclature is described in the Figure 2 legend.
QTLs were single in a genomic region (referred as out- For “anchored QTLs”, the final number is the chromosome number
layer QTLs in Additional file 1), they were excluded alone; for “outlayer QTLs”, the final number is the chromosome number
juxtaposed to the QTL mapping order on the chromosome and a letter
from the clustering step. was sometimes added to distinguish colocalizing QTLs that were
QTLModel command determined the best clustering detected with different traits. The trait with which the QTL was detected
model based on information-based criteria that were is indicated after the comma by the trait code, as defined in the Table 2
legend."Anchored QTLs” are QTLs from non-compiled maps and they
computed for each possible model: AIC (Akaike infor- could only be anchored to the consensus map if the confidence interval
mation criterion), AICc, AIC3, BIC (Bayesian informa- comprised a common marker; they are mentioned at the position of the
tion criterion) and AWE (average weight of evidence) common marker. No confidence interval information is available."Outlayer
QTLs” are QTLs from compiled maps and, as they were alone in their
[20]. The best model was the one which criteria values
Danan et al. BMC Plant Biology 2011, 11:16 Page 14 of 16
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2. Ballini E, Morel J-Bt, Droc Gt, Price A, Courtois B, Notteghem JL, Tharreau D:
region on the consensus map, they eventually could not be clustered A genome-wide meta-analysis of rice blast resistance genes and
with other QTLs in a meta-QTL. Confidence intervals of these “outlayer quantitative trait loci provides new insights into partial and complete
QTLs” are represented by dotted areas. resistance. Molecular Plant-Microbe Interactions 2008, 21(7):859-868.
Additional file 2: Criterion values of the meta-QTL models. The 3. Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A,
values of the AIC, AICc, AIC3, BIC and AWE criteria provided by the Charcosset A: Genetic architecture of flowering time in maize as inferred
MetaQTL software are listed for the twelve chromosomes (first column), from quantitative trait loci meta-analysis and synteny conservation with
for both maturity and late blight resistance traits (second column), and the rice genome. Genetics 2004, 168(4):2169-2185.
for all possible meta-QTL models (third column, K is the number of 4. Coque M, Martin A, Veyrieras J, Hirel B, Gallais A: Genetic variation for N-
hypothetic meta-QTLs of a model). “Delta” is the rescaled value of the remobilization and postsilking N-uptake in a set of maize recombinant
criterion, it is the difference between the value of the given model and inbred lines. 3. QTL detection and coincidences. TAG Theoretical and
the value of the best model. The weight is the “weight of evidence” of Applied Genetics 2008, 117(5):729-747.
the model, the higher it is, the more confidence we can have in the 5. Courtois B, Ahmadi N, Khowaja F, Price AH, Rami JF, Frouin J, Hamelin C,
corresponding model. Ruiz M: Rice root genetic architecture: meta-analysis from a drought QTL
Additional file 3: Meta-QTL details: number per chromosome, database. Rice 2009, 2(2/3):115-128.
confidence intervals and composition in published QTLs. For each 6. Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L,
chromosome, late blight and maturity meta-QTLs are described. Meta- Orford S, Wingen L, Herry L, Faure S, Laurie D, Bilham L, Snape J: Meta-QTL
QTL numbers, names and confidence intervals (CI, in cM, Haldane unit) analysis of the genetic control of ear emergence in elite European
are specified. The QTL composition of each meta-QTL is detailed by winter wheat germplasm. TAG Theoretical and Applied Genetics 2009,
giving the individual QTL names, the species origins of the mapping 119(3):383-395.
parents (when pedigrees are known), R² values (if specified in the original 7. Guo B, Sleper DA, Lu P, Shannon JG, Nguyen HT, Arelli PR: QTLs associated
publication) and confidence intervals as described in the original with resistance to soybean cyst nematode in soybean: meta-analysis of
publication (in their original unit, Haldane or Kosambi) with their means QTL locations. Crop Science 2006, 46(2):595-602.
for each meta-QTL. The confidence intervals of the projected QTLs with 8. Hanocq E, Laperche A, Jaminon O, Lainé A, Le Gouis J: Most significant
their means are also indicated. The QTL nomenclature is described in the genome regions involved in the control of earliness traits in bread
Figure 2 legend. For Villamon et al. and Leonards-Schippers et al.’ studies, wheat, as revealed by QTL meta-analysis. TAG Theoretical and Applied
the original name of the QTL was added [36,41]. When QTLs are equally Genetics 2007, 114(3):569-584.
shared by two meta-QTLs, they are shown in italic (’LB’ for late blight 9. Khowaja F, Norton G, Courtois B, Price A: Improved resolution in the
resistance). The mean of the original confidence intervals of the QTLs position of drought-related QTLs in a single mapping population of rice
and the number of the QTLs composing the meta-QTL are given for by meta-analysis. BMC Genomics 2009, 10(1):276.
each meta-QTL. NA: not available. 10. Lanaud C, Fouet O, Clement D, Boccara M, Risterucci AM, Surujdeo-
Maharaj S, Legavre T, Argout X: A meta-QTL analysis of disease resistance
Additional file 4: Synonymous names of markers described in the traits of Theobroma cacao L. Molecular Breeding 2009, 24(4):361-374.
compiled published maps. Marker names that were the most often 11. Liu S, Hall MD, Griffey CA, McKendry AL: Meta-analysis of QTL associated
encountered for a marker and which had a familiar nomenclature were with fusarium head blight resistance in wheat. Crop Science 2009,
considered as standard names. Their corresponding synonymous marker 49(6):1955-1968.
names that were found in the compiled maps were collected. Only 12. Löffler M, Schon CC, Miedaner T: Revealing the genetic architecture of
standard names were used in the final consensus map. FHB resistance in hexaploid wheat (Triticum aestivum L.) by QTL meta-
analysis. Molecular Breeding 2009, 23(3):473-488.
13. Marandel G, Salava J, Abbott A, Candresse T, Decroocq V: Quantitative trait
loci meta-analysis of Plum pox virus resistance in apricot (Prunus
Acknowledgements armeniaca L.): new insights on the organization and the identification of
This work was financially supported by the BIOEXPLOIT Integrated Project genomic resistance factors. Molecular Plant Pathology 2009, 10(3):347-360.
FOOD CT2005-513959 that resides under the 6th framework programme of 14. Norton GJ, Aitkenhead MJ, Khowaja FS, Whalley WR, Price AH: A
the European Union. In addition, it was approved by the PEIFL (European bioinformatic and transcriptomic approach to identifying positional
fruits and vegetables innovative cluster), which is a competitiveness cluster candidate genes without fine mapping: an example using rice root-
at French national level. Sarah Danan received a PhD fellowship funded by growth QTLs. Genomics 2008, 92(5):344-352.
the European BIOEXPLOIT project. Authors warmly thank Lukas Mueller for 15. Rong J, Feltus FA, Waghmare VN, Pierce GJ, Chee PW, Draye X, Saranga Y,
his useful critical review of this manuscript. Wright RJ, Wilkins TA, May OL, Smith CW, Gannaway JR, Wendel JF,
Paterson AH: Meta-analysis of polyploid cotton QTL shows unequal
Author details contributions of subgenomes to a complex network of genes and gene
1
Institut National de la Recherche Agronomique (INRA), UR 1052 Génétique clusters implicated in lint fiber development. Genetics 2007, 176(4):2577-2588.
et Amélioration des Fruits et Légumes (GAFL), BP94, 84140 Montfavet, 16. Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J:
France. 2Institut National de la Recherche Agronomique (INRA-UPS-INA PG- Unraveling the Complex Trait of Crop Yield With Quantitative Trait Loci
CNRS), UMR 320 Génétique Végétale, Ferme du Moulon, 91190 Gif-sur- Mapping in Brassica napus. Genetics 2009, 182(3):851-861.
Yvette, France. 17. Truntzler M, Barrière Y, Sawkins CM, Lespinasse D, Betran J, Charcosset A,
Moreau L: Meta-analysis of QTL involved in silage quality of maize and
Authors’ contributions comparison with the position of candidate genes. Theor Appl Genet. 2010,
VL conceived of the initial idea and coordinated the study. All authors 121(8):1465-1482.
participated in the conception of the study. JBV originally coded the 18. Wisser RJ, Balint-Kurti PJ, Nelson RJ: The genetic architecture of disease
package MetaQTL and gave a significant support during the meta-analysis resistance in maize: a synthesis of published studies. Phytopathology
process. SD carried out the collection of data and applied the QTL meta- 2006, 96(2):120-129.
analysis. VL and SD contributed to the interpretation of the results and 19. Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A,
drafted the manuscript. All authors read and approved the final manuscript. Joets J: BioMercator: integrating genetic maps and QTL towards
discovery of candidate genes. Bioinformatics 2004, 20(14):2324-2326.
Received: 11 February 2010 Accepted: 19 January 2011 20. Veyrieras JB, Goffinet B, Charcosset A: MetaQTL: a package of new
Published: 19 January 2011 computational methods for the meta-analysis of QTL mapping
experiments. BMC Bioinformatics 2007, 8(1):49.
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set of clones reveal modes of chromosomal evolution in potato and and take full advantage of:
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75. Yamanaka S, Ikeda S, Imai A, Luan Y, Watanabe JA, Watanabe KN:
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