Introgressive Hybridization in Potato Revealed by Novel Cytogenetic and Genomic Technologies
American Journal of Potato Research
Introgressive Hybridization in Potato Revealed by Novel Cytogenetic and Genomic Technologies
Paola Gaiero 0 1 2
Pablo Speranza 0 1 2
Hans de Jong 0 1 2
0 Laboratory of Genetics, Wageningen University & Research , Droevendaalsesteeg 1, P.O. Box 16, 6708, PB Wageningen , The Netherlands
1 Department of Plant Biology, Facultad de Agronomia, Universidad de la Republica , Garzon 780, 12900 Montevideo , Uruguay
2 Hans de Jong
Potato is the third most important food crop in the world and is crucial to ensure food security. However, increasing biotic and abiotic stresses jeopardize its stable production. Fortunately, breeders count on a rich pool of wild relatives that provide sources for disease resistance and tolerance to environmental stresses. To use such traits effectively, breeders require tools that facilitate exploration and exploitation of the genetic diversity of potato wild relatives. Introgression programs to incorporate such alien chromatin into the crop have so far relied on cytogenetic and genetic studies to tap desired traits from these wild resources. The available genetic and cytogenetic tools, supplemented with more recent genomic technologies, can assist in the use of potato relatives in pre-breeding. This information can also facilitate cisgenesis and genome editing to improve potato cultivars. Despite the abundant and rapidly growing genomic information of potato, that of its wild relatives is still limited.
Potato wild relatives; Introgression; Comparative genomics; Pre-breeding
supplies at the same time a good source of energy and
(Birch et al. 2012)
increasing biotic and abiotic stresses represent a serious and
constant risk for food security and so jeopardize stable
. The genetic diversity of cultivated
potato that may provide allelic resources for controlling such
stresses has been substantially reduced in the process of
domestication and selection. Only a few clones of tetraploid
cultivated Solanum tuberosum from the Andes were
introduced to Europe and though they must have contained a lot
of genetic variation, the available biodiversity was only
(Hawkes 1990; Spooner et al. 2005; Ríos et al.
2007; J.M. Bradeen and Haynes 2011; Ramsay and Bryan
2011; Birch et al. 2012; Kloosterman et al. 2013)
. This limited
genetic diversity was further reduced due to genetic
bottlenecks during photoperiod adaptation and losses resulting from
viruses and the late blight epidemics of 1845–1846 (Bethke et
al. 2017). However, cultivated potato and its wild relatives
signify a more diverse (Fig. 1) and accessible germplasm
resource than that of any other crop
(Ross 1986; Hanneman
1989; Peloquin et al. 1989; Hawkes 1990)
. Their value as
breeding material is given by their wide geographical
distribution and great range of ecological adaptation (Fig. 1)
(Hawkes 1994), together with their availability through the
Inter-genebank Potato Database (IPD) (http://germplasmdb.
cip.cgiar.org) established by the CIP (International Potato
Centre) and the Association for Potato Intergenebank
Collaboration. To use potato wild relatives (WR) efficiently
to expand its genetic base, breeders require tools that facilitate
exploration and exploitation of their genetic diversity.
This diversity coming from potato WR can transfer specific
traits to potato by introgressive hybridization. It involves the
introduction of alien chromatin carrying a gene of interest from
a wild relative to the crop genome. After the interspecific
hybridization and repeated backcrossings, the selected gene(s) of
interest are incorporated into the crop chromosomes by
homoeologous recombination. The offspring are then selected
for the desired trait while the wild genetic background is
removed by selection in consecutive backcross generations as
far as possible. Linkage drag may occur when the introgressed
chromatin still contains tightly linked wild traits from the
ancestral donor that cannot be removed by recombination
and Bryan 2011)
. An alternative approach is genetic base
broadening (Bradshaw 2016), which favours allelic variation
besides incorporating genes of interest, and thus maximizes
the heterozygosis and epistasis required for yield improvement
(Mendoza and Haynes 1974)
, but completely loses the genetic
background of the original cultivar. Base broadening, which is
often the underlying objective of breeders
uses the broadest possible starting material and depends on
recombination between the parental genomes in the hybrid. It is
then followed by weak selection in target environments but
requires enough time to produce advanced backcrosses of
improved material that can be crossed with elite germplasm
without negative effects on yield and agronomic performance. This
process results in improved genotypes that can be used as
parents in breeding programmes (Bradshaw 2016).
Determining Existing Introgression Events
in Potato Cultivars
Several reports of natural hybrids suggest that potato WR
readily hybridize in the wild
(Spooner and Hijmans 2001;
Camadro 2012; Spooner et al. 2014)
. Examples of such events
include the triploid hybrids between Solanum commersonii
and S. chacoense, or S. commersonii and S. gourlayi
(Masuelli and Camadro 1992; Ortiz 1998)
. When samples
are collected from natural populations, these may carry
introgressions from other wild species
(Camadro 2012; Spooner et
al. 2014; Bethke et al. 2017)
. Such introgressed segments
represent a source of variability through new allele
combinations but also a challenge for the ex situ conservation
and utilization of potato WR.
Potato wild relatives like diploid Solanum bulbocastanum,
S. stoloniferum and S. chacoense or hexaploid S. demissum
(Pavek and Corsini 2001)
have been extensively used in potato
introgressive hybridization breeding
Peloquin et al. 1989; Watanabe et al. 1994; Jansky 2000;
Pavek and Corsini 2001; Bradshaw et al. 2006; Bradshaw
2007a; Bradshaw 2007b; Bradshaw and Ramsay 2009;
Jansky 2009a; Bradshaw and Bonierbale 2010; Ramsay and
. Such taxa not only display various advantages
over cultivated germplasm
(Jansky and Peloquin 2006)
as resistance to the late potato blight, caused by Phytophthora
infestans and other diseases caused by bacteria and viruses
(Jansky 2000; Simko et al. 2009)
, they also provide the genetic
basis for tolerance to cold, frost and other environmental
stresses. It is widely accepted that many modern cultivars have wild
species donors in their pedigrees
. Andean farmers
allow wild populations of potato species to grow on their fields,
so wild germplasm is introduced into both diploid and
. Moreover, the use of potato WR
in introgressive hybridization breeding before the existence of
common pedigree records implies that the original introgression
events have not been documented and that the sources of certain
desirable traits are unknown
(Love 1999; Leisner et al. 2018)
One of the direct methods to demonstrate introgressed alien
chromatin in the crop chromosomes is comparative
chromosome painting by Fluorescent in situ Hybridization, that
establishes the structural and numerical comparisons of
chromosome sets between species of the genus Solanum
(Tang et al.
2008; Iovene et al. 2008; Szinay et al. 2008; Szinay et al. 2010;
Lou et al. 2010; Verlaan et al. 2011; Szinay et al. 2012)
low stringency conditions, it is possible to use tomato or potato
probes in these experiments to perform cross-species
chromosome painting and to display homoeologous chromosomal
positions in related Solanum species. In this way, many hitherto
unknown inversions could be described
(Tang et al. 2008; Lou
et al. 2010; Szinay et al. 2010; Peters et al. 2012; Szinay et al.
. BAC-FISH also allowed the accurate mapping of the
Ty-1 gene introgressed from S. chilense into cultivated tomato
and provided an explanation for observed linkage drag
resulting from suppression of recombination (Verlaan et al.
2011). There are no such studies in potato cultivars, although
there are many reports of introgressions based on molecular
(Hosaka 1995; Bryan et al. 1999; Provan et al. 1999;
van der Voort et al. 1999; Gebhardt et al. 2004; Flis et al. 2005;
Sokolova et al. 2011)
Resequencing studies in tomato have identified
polymorphisms related to introgressions
(Causse et al. 2013)
, while in
potato, these have been shown in some diploid and tetraploid
landraces as well as in cultivars
(Hardigan et al. 2017)
Bioinformatic tools like iBrowser
(Aflitos et al. 2015)
been developed to use SNPs identified from the increasing
genome sequence data available to pinpoint past undescribed
introgressions from wild relatives in the genomes of cultivated
Solanum species. These approaches together with other
modern technologies will also prove useful when designing new
introgressive hybridization schemes.
Tools for Establishing Introgressive Hybridizations
In spite of the widely available diversity in germplasm
collections worldwide, only 10% of the potato species have been
explored for use in breeding programmes
This is a rather low percentage, bearing in mind that by
manipulation of ploidy and other biotechnological interventions,
virtually any potato species can be used in introgressive
(Ortiz 1998; Jansky 2006; Ortiz et al.
. Moreover, the few species that have been employed
in breeding programs to provide specific traits have not been
Knowledge of genome organization and divergence
between potato and its wild relatives is most helpful to create
new introgressive hybridization schemes. Before choosing a
wild relative as donor, it is important to know if there are
inversions or translocations that will impede introgression or
cause linkage drag (Fig. 2). Another key aspect is to always
take into account hybridization barriers that have been
thoroughly reviewed elsewhere
(Camadro et al. 2004; Jansky
2009b; Bethke et al. 2017)
. The great potential recognized in
these wild relatives encouraged scientists to develop strategies
for overcoming such barriers
(Jansky 2006; Bradshaw and
Bonierbale 2010; Bethke et al. 2017)
. Once the crossing
barriers are overcome, stabilizing the introgression in the potato
genotypes still represents a challenge due to its tetraploid
inheritance. Additionally, inbreeding depression forces breeders
to use different genotypes as recurrent parents for backcross
progenies. Despite all these obstacles to recover a superior
cultivated background after hybridization with a wild species,
the value of these potato WR makes it worth the effort. A wide
variety of cytogenetic, genetic and genomic tools can be used
to assist in these efforts.
Classical Cytogenetics Tools
Classical cytogenetics should be the first tool to study potato
WR to be used as donors and their hybrids with potato. It helps
to establish ploidy levels and Endosperm Balance Number
(EBN) of the interspecific hybrids
(Peloquin et al. 1989;
Jansky 2009; Ono and Hosaka 2010)
and to assess the effects
of ploidy changes in the parental species and their hybrids
(Mok and Peloquin 1975;
Adiwilaga and Brown 1991
Carputo et al. 1997; Ortiz 1998;
Carputo et al. 2000
rn and Veilleux 2007
; Jansky 2009; Ortiz et al.
Only recombinations outside
the inverted region lead to
Several backcrosses with
selection for the trait of
Fig. 2 shows two simplified examples of structural chromosome
rearrangements and the consequences they may have for plant genetics
and breeding. Both examples represent a hybrid F1, which carries
chromosomes from the crop (white) and the wild relative (WR, black).
a) In the case of a (paracentric) inversion a distal region of the long arm is
inverted in the WR (black). In the hybrid in which one chromosome
contains the inversion, chromosomes fail to pair in this region or form a
loop structure. Crossovers in this region result in a sterile spore so viable
spores pass only the non-recombined region to the next generation. If the
trait of interest is located in the inverted region, after several backcrosses
with selection for this trait, the genetic background of the crop (white) will
be recovered but the inverted region will be maintained as a block
containing the selected trait together with undesired wild chromatin, a
2009). Direct cytogenetic analysis is also the most direct
approach to observe meiotic chromosome pairing behaviour in
interspecific hybrids and their progenies
(de Jong et al. 1993;
Carputo et al. 1995; Masuelli and Tanimoto 1995; Barone et
al. 1999; Carputo 2003; Chen et al. 2004; Gaiero et al. 2017)
Genome differentiation between wild potato species is
assumed to play a minor role as an isolation mechanism
1983; Camadro et al. 2004)
. For potato and its relatives,
genomic formulas were proposed by Matsubayashi (1991)
who distinguished five genomes in Section Petota (A, B, C,
D and P) through classical genome analysis of meiotic
behaviour and pollen fertility in interspecific hybrids. Genomes
identified with different letters show little or no pairing in
the meiosis of their amphidiploid hybrids, which display
pollen sterility. The most common genome is type A, which
presents different degrees of structural variants depending on the
scale of the chromosomal rearrangements. Genome E is
proposed for the closely related non-tuber-bearing species of the
Pseudolinkage. (Semi)sterility in unbalanced
segregants favors parental combinations
genetic phenomenon known as linkage drag. b) In the case of a reciprocal
translocation, fragments of two non-homologous chromosomes are
swapped in the chromosomes originating from the wild relative. In
meiosis of the hybrid F1, two outcomes can be considered: a balanced
segregation in which the two non-translocated chromosomes and the two
translocated chromosomes go to opposite poles, resulting in balanced
viable spores. In the second case, a non-translocated and a translocated
chromosome are included in the same daughter cell, which contains a
duplicated fragment of one chromosome and a deletion of a fragment of
the other chromosome and hence results in a sterile spore. Reduced
fertility of the unbalanced products favors the maintenance of the parental
combinations causing the apparent linkage of loci in the chromosomes
involved in the translocation
Section Etuberosum. For potato breeders, homoeologous
pairing and crossovers in their hybrids with cultivated
potatoes is of more interest than their phylogenetic relationships
because it predicts their success for breeding via crossing. The
most stringent test for pairing between homoeologous
chromosomes is the analysis of meiosis of triploid hybrids. If the
chromosomes form trivalents in the meiosis of triploids, then
introgression is possible
. The chances of alien
chromatin introgression are greater as homoeologous pairings
are more likely to occur in the triploid compared to the meiotic
pairing in tetraploids in which potentially there is always a
homolog for each chromosome which may pair preferentially
(Sybenga 1996; Jansky 2006)
. Although the factors that
determine homeologous pairing are not clear yet, homology in
repetitive sequences seems to play an important role. Genome
divergences caused by repeats have been assessed within and
between the potato and tomato clades, characterizing the
abundance and dynamics of the repetitive fractions of their
genomes (Gaiero et al. in prep). These can have significant
consequences in genome homology, genome expansion and in
the occurrence and impact of structural rearrangements.
Molecular Cytogenetics Tools
Molecular cytogenetics has been one of the major instruments
in tracing the course of alien chromosomes in introgressive
hybridization breeding. It has been applied for most major
(Benavente et al. 2008)
, including potato
and Peloquin 1965; Mok et al. 1974; Pijnacker and Ferwerda
1984; Visser and Hoekstra 1988; Mohanty et al. 2004;
. It allows identification of whole
chromosome sets or of specific chromosome pairs and it also enables
comparisons of the chromosomal positions of markers or
regions of interest across related species.
Genome painting or GISH (Genomic in situ hybridization)
is a powerful FISH technique used for tracing homoeologous
chromosome pairing, recombination and transmission. It
consists in labelling genomic DNAs from one or both parental
species as probe(s) to hybridize on chromosome slides of the
interspecific hybrid and its progeny (Fig. 3a). If the genomes
of the parental species (especially their dispersed and tandem
repeats) have diverged sufficiently, chromosomes of the two
species can be easily discriminated in the hybrid nuclei
through different fluorescent dyes. In nuclei from interspecific
(sexual or somatic) hybrids between potato (genome A) and
non-tuber bearing relatives (genomes E, B or P) GISH has
been successful in discriminating chromosomes
(Dong et al.
1999; Dong et al. 2001; Gavrilenko et al. 2002; Gavrilenko et
al. 2003; Dong et al. 2005)
. In wider hybrids such as S. nigrum
(+) S. tuberosum and its backcrosses (Horsman et al. 2001),
alien chromosomes are easily distinguishable. These studies
provide further evidence of genome differentiation, in the
sense that genomes identified with different letters not only
do not pair in the meiosis of their hybrids but also can be
discriminated by GISH. When divergence is not so high,
contrast in the hybridization differentiation can be improved by
adjusting washing stringency and proportion of blocking
(unlabelled) DNA in the FISH experiments
(Jiang and Gill
. However, there is a technical limit to what can be
discriminated by GISH. As an example, the technology has
not been successful in studies of hybrids between potato and
its closer A-genome tuber-bearing wild relatives, with the
exception of S. bulbocastanum, a diploid (1EBN, Ab genome)
(Iovene et al. 2007)
. Hybrids between S.
commersonii and S. tuberosum Group Phureja behaved as
near autopolyploids during male meiosis and it was not
possible to discriminate the chromosomes coming from each
parental species through GISH
(Gaiero et al. 2017)
results suggest that repetitive sequences have not diverged much
among the genomes of cultivated and wild potatoes.
Fig. 3 Examples of the various technologies available to assist in
introgressive hybridization breeding. a) genome painting (GISH) with
S. commersonii genomic DNA probe (green) on the chromosomes of a
triploid interpecific hybrid (S. commersonii x S. tuberosum Group
Phureja) in a meiotic cell complement. Notice that all chromosomes are
hybridized with the probe. b) Chromosome identification through
BACFISH on the chromosomes of a triploid interpecific hybrid (S.
commersonii x S. tuberosum Group Phureja) in a meiotic cell
complement. Three chromosomes from pair 1 are identified with a yellow
probe and three chromosomes from pair 2 are identified with a blue probe.
c) Example of optical mapping in which high-molecular weight Solanum
DNA molecules are stained with YOYO (blue) showing
sequencespecific single strand nicks (green), and then stretched by moving along
a nanochannel array. Millions of such images are integrated to build a
consensus genome map. d) Dot-plot comparison of the genome
assemblies of Solanum commersonii and S. tuberosum (DM) obtained
through the software MUMmer. It shows a high degree of collinearity
with only few small inversions (inverted stretches of dots across the
Chromosome rearrangements between related species can
cause specific problems at different meiotic stages of their
interspecific hybrids (Fig. 2). Typical examples are
heterozygosity for paracentric inversions which can cause anaphase I
(and or II) bridges and hence sterility or aneuploidy (Fig. 2a)
or reciprocal translocations, which can lead to semi-sterility or
aneuploidy (Fig. 2b). Such rearrangements between the
homoeologues represent an important limitation in
introgressive breeding due to the unintended retention of large blocks
of DNA surrounding a gene of interest (Fig. 2a), genetically
described as linkage drag
(Jacobsen and Schouten 2007)
There are no reports of large scale chromosome
rearrangements in potato and its wild relatives, in contrast to some
detailed descriptions of rearrangements among Solanaceous
(Iovene et al. 2008; Tang et al. 2008; Lou et al. 2010;
Peters et al. 2012; Szinay et al. 2012)
. Linkage drag represents
a limitation for introgressive hybridization breeding because
blocks of alien chromatin surrounding the gene of interest can
be retained even after many generations of backcrossing. The
impact of genetic drag is even greater when the linked regions
have a negative effect on agronomic performance (Fig. 2a).
Selection against such undesired blocks can be simplified by
marker-assisted breeding and genomic selection, but these
approaches are still challenging (Warschefsky et al. 2014),
especially in autotetraploid genotypes. While the literature on
comparative FISH analysis in Solanum is vast, there are only
a few studies that have utilized sufficient high-quality
sequence data needed to reveal fine-scale structural differences
related to introgression barriers
(Datema et al. 2008; Peters et
al. 2012; Causse et al. 2013; Aflitos et al. 2014; Aflitos et al.
2015; de Boer et al. 2015)
A considerable body of literature on FISH applications for
breeding is available for tomato as reviewed by
Szinay et al.
, with reports of many structural rearrangements among
tomato and its wild relatives that have significant impacts on
(Anderson et al. 2010; Verlaan et al. 2011; Szinay et
. With multi-colour fluorescence microscopy it is
possible to hybridize many probes each labelled with a
different fluorescent dye in a single experiment, reducing the
examination of any chromosome set to only a few experiments
(Tang et al. 2009; Szinay et al. 2010)
. For potato, a set of
chromosome-specific cytogenetic DNA markers (CSCDM)
made from DNA probes selected from a S. bulbocastanum
library was developed to associate all twelve linkage groups
to potato chromosomes and build a reference karyotype
(Dong et al. 2000; Song et al. 2000)
. The RHPOTKEY
BAC library was developed for the diploid potato clone
. The positions of the BACs in
this library were anchored to AFLP markers in the ultrahigh
density (UHD) genetic map
(van Os et al. 2006)
. From this
library, a set of 60 BACs with known positions in the Ultra
High Density (UHD) linkage map were selected for
localization on pachytene chromosomes, thus providing a useful tool
to study collinearity between potato and its wild relatives
(Tang et al. 2009; Achenbach et al. 2010; de Boer et al.
. Gaiero et al. (2016) used this BAC set to build
cytogenetic maps for S. commersonii and S. chacoense and to
compare them to that of cultivated potato. Their results indicate a
high collinearity at the chromosomal scale between the three
species which makes them promising donors in introgressive
hybridization schemes. They also used them to identify
specific chromosome pairs in triploid hybrids between S.
commersonii and S. tuberosum Group Phureja (Fig. 3b).
Using a higher number of BAC probes which are located
closer together in linkage maps, high resolution cytogenetic
mapping has been employed to describe rearrangements in
chromosome 6 coming from potato and tomato
(Iovene et al.
2008; Tang et al. 2008)
. Such fine mapping has also been
useful to design strategies for the sequencing projects of these
(Xu et al. 2011; The Tomato Genome Consortium
. They have helped by identifying the boundaries
between the highly condensed heterochromatin and
euchromatin, which is easier to sequence and assemble
(Szinay et al.
2008; Tang et al. 2009; Szinay 2010; Tang et al. 2014)
the sequencing and assembly efforts could be better directed
to the euchromatic regions. Because these crops were
sequenced using BAC libraries, cytogenetic maps have also
been used to construct the backbone for sequence assembly
(Szinay et al. 2008)
(Visser et al. 2009)
The seed BAC clones that were chosen to start the assembly
were confirmed through BAC-FISH, the BAC positions on
genetic and physical maps were verified and gaps in the
assembly were identified and sized
(Iovene et al. 2008; Szinay et
al. 2008; Tang et al. 2008; Tang et al. 2009)
. The use of a very
large number of BAC-FISH probes, coupled with information
from physical maps (restriction and optical maps) allowed for
the correction of miss-assemblies in the tomato genome and
identification of scaffolds that were not in the correct order or
orientation, or both
(Shearer et al. 2014)
. The potato assembly
was similarly improved using information from physical and
genetic maps to achieve a reference genome at the level of
pseudomolecules (equivalent to chromosomes)
(Sharma et al.
2013; Hardigan et al. 2016)
. Such integration of technologies
has only been applied to date for S. chacoense among the
potato WR (Leisner et al. 2018).
The cutting edge technology of genome mapping through
(Lam et al. 2012; Cao et al. 2014)
is the ideal
tool for completing genome assemblies and even identifying,
spanning and assembling repeated sequences. In addition to
assisting in genome assembly, genome mapping can assess
structural variation among related species or genotypes within
a species (Cao et al. 2014). This technology uses nicking
enzymes to create DNA sequence-specific nicks that are
subsequently labelled by a fluorescent nucleotide analogue
(Xiao et al. 2007)
. The DNA is linearized by confinement in
a nanochannel array
(Das et al. 2010)
and then photographed
(Fig. 3c). The DNA loading and imaging cycle can be
automatically repeated many times, so data can be obtained at high
throughput and high resolution
(Hastie et al. 2013)
mapping using nanochannels has been used only recently for
genome assembly in higher plants such as spinach
(Xu et al.
, subterranean clover
(Kaur et al. 2017)
, quinoa (Jarvis et al. 2017) and bread wheat
Staňková et al. 2016
). In the genus Solanum, the related
method known as optical mapping
(Zhou et al. 2004)
used for whole genome analysis in tomato
(Shearer et al.
and also in othe
r crops like rice (Zhou et al. 2007
(Zhou et al. 2009)
and for crop relatives such as
Medicago truncatula (Young et al. 2011). One of the
limitations for its use in the higher plant genomics community, is the
challenge of obtaining sufficient amounts of high molecular
weight nuclear DNA (HMW DNA) due to the thick cell walls
and cytoplasmic polyphenols and polysaccharides.
Moving from physical to genetic mapping, considerable
effort has been put into mapping traits of interest on the
genetic maps of the few potato WR that have been used in potato
breeding. Understandably, most attention has been devoted to
mapping resistance to late blight (Phytophthora infestans), the
most important potato disease and responsible for the
infamous Irish Potato Famine in 1845–46. The most remarkable
source for resistance to P. infestans is S. bulbocastanum
(Naess et al. 2001; Lokossou et al. 2010)
. Resistance to P.
infestans was also mapped in Solanum demissum (Jo et al.
2011), S. venturii
(Pel et al. 2009)
, S. pinnatisectum
, S. avilesii
(Verzaux et al. 2011)
, S. paucisectum
(Villamon et al. 2005)
and in S. phureja x S. stenotomum
(Costanzo et al. 2005; Simko et al. 2006)
. Different alleles
from a single locus on chromosome 8 from S. bulbocastanum,
which carries resistance to late blight, have been the subject of
physical mapping and positional cloning
(Bradeen et al. 2003;
Song et al. 2003; Van Der Vossen et al. 2003)
. Resistance to
important potato viruses like PVX and PVY has also been the
focus of mapping efforts
SolomonBlackburn and Barker 2001; Flis et al. 2005; Y.-S. Song et
al. 2005; Sato et al. 2006; Simko et al. 2009)
, together with
other traits of interest (Anithakumari et al. 2011) and with
pyramiding of resistance genes
association studies (GWAS) have been particularly useful for
complex traits in cultivated potato
(Ewing et al. 2004;
Gebhardt et al. 2004; Simko 2004; Simko et al. 2004; Simko
et al. 2006; Visser et al. 2015)
, but only one study includes the
use of wild relatives (Hardigan et al. 2017). All these efforts
have allowed the use of tightly linked molecular markers to
select resistant genotypes or to select against donor genome in
backcross progenies from an introgression scheme, in the
so-called marker-assisted breeding (reviewed by
Tiwari et al. (2013)
). Most literature on selection
against wild genome comes from studies on the introgression
of S commersonii into a S. tuberosum tetraploid background
(Barone et al. 2001; Carputo et al. 2002; Barone 2004; Iovene
et al. 2004)
. The greatest impact of these molecular breeding
technologies has been on pre-breeding and parental
(De Koeyer et al. 2011)
and also on the exploration of
(Bamberg and del Rio 2013; Carputo et
al. 2013; Manrique-Carpintero et al. 2014; Warschefsky et al.
The available genomic knowledge on wild potatoes is
relatively limited compared to that of tomato WR
(Szinay et al.
2012; Aflitos et al. 2014; Bolger et al. 2014)
. The tendency
now is to slowly move to more sophisticated genomics of
WR, elucidating the available diversity and desirable traits
(Bradeen and Haynes 2011; Ramsay and Bryan 2011)
increasing number of molecular markers and DNA sequence
data to be generated will allow for faster progress in breeding
by simultaneously selecting genes/QTLs while selecting
against wild species genome content
With the development of high-throughput DNA
sequencing, genome assemblies for tomato
(The Tomato Genome
(Xu et al. 2011)
and several of their
(Aflitos et al. 2014; Bolger et al. 2014; Aversano et al.
2015; Leisner et al. 2018)
have become available. Concerted
genomics and bioinformatics efforts have improved genome
(Sharma et al. 2013; Shearer et al. 2014; Hardigan
et al. 2016)
. However, only a few studies have utilized
sufficient high-quality physical maps needed to reveal structural
differences (Fig. 3d) related to introgression barriers
al. 2012; Aflitos et al. 2014; Aflitos et al. 2015; de Boer et al.
. Although sequence data for some wild species are
available (e.g., S. chacoense, S. commersonii), the only
comparative structural analysis performed so far used DArT
markers, finding microscale genome sequence variation
(Traini et al. 2013)
. A vast survey of genome-wide sequence
variation across a diversity panel of cultivated and wild potato
species was performed by
Hardigan et al. (2017)
, finding more
variation than in any other crop resequencing project. In most
cases of crop wild relatives (CWR) only a draft genome is
available and it is of limited use, depending on the quality of
(Pérez-de-Castro et al. 2012)
. Such is the case of
the whole genome draft sequence available for Solanum
commersonii (Aversano et al. 2015). Assembly to the level
of pseudomolecules is achieved when mapping against the
reference potato genome. This approach does not cater for
structural variation between the two species. In the case of S.
chacoense, the genotype that was sequenced (M6) was an
inbred clone, so increased homozygosity facilitated genome
assembly. The construction of pseudomolecules was achieved
including information from genetic maps using M6 as parent
of the segregating population, so it does not assume
collinearity with a reference genome
(Leisner et al. 2018)
breeders should count on fully assembled and well annotated
reference genomes for potato WR to assist in gene discovery
and dissection of the genetic basis of a trait.
Making the Most of Biotechnological Approaches through Wild Relatives
One might argue that resorting to potato WR as donors of
desirable traits through introgressive hybridization seems no
longer necessary with modern technologies such as cisgenesis
or the CRISPR-Cas9 genome editing, as it allows researchers
to transfer directly the gene of interest or to change the
native sequence into a tailor-made version, respectively.
Nevertheless, it is first necessary to identify the original genes
conferring the trait of interest and to mine their allele diversity
in order to isolate them, clone them and accurately modify
them or transfer them into targeted cultivars. This is possible
through newly developed genetic and genomic tools
Knowledge on the physical position of the genes of interest
is useful to isolate them and transfer them to cultivated potato.
The identification, mapping, cloning and the techniques to use
resistance genes against Phytophthora infestans coming from
potato WR was reviewed by
(Park et al. 2009)
. Most mapped
and cloned genes come from S. demissum
(Jo et al. 2011)
(Naess et al. 2000; Naess et al. 2001; Bradeen
et al. 2003; J. Song et al. 2003; Lokossou et al. 2010)
although using an interspecific candidate gene approach,
et al. (2009)
were able to map and clone a dominant from an
alternative donor (S. venturii). These genes have already been
used or are in the pipeline for cisgenesis into cultivated potato
(Haverkort et al. 2008; Park et al. 2009; Zhu et
Recently, all known major R genes in potato have been
sequenced and an ‘omics’ approach was used to recognize
the genes responsible for late bight resistance
et al. 2016)
. The previously developed SolRgene database
provides easy access to the sequences of R genes across
Solanum section Petota, allowing the cloning of many of those
genes for downstream biotechnological uses (Vleeshouwers et
al. 2011). New sources of resistance have been identified and
their genes cloned using the latest third generation sequencing
technologies. These new variants are now available for
(Witek et al. 2016)
. The genome
sequence and transcriptomes of potato WR like S.
commersonii and S. chacoense have allowed the identification
of pathogen-receptor genes and to describe non-acclimated
and cold-acclimated gene expression as well as to get insights
on tuberization and glycoalkaloid production
(Narancio et al.
2013; Aversano et al. 2015; Leisner et al. 2018)
. A large
resequencing effort across potato cultivars and landraces
together with potato WR shed light on the kinds of traits and
genes that were under selection during the domestication
process and provided a useful catalogue of genomic variation
within the potato genepool
(Hardigan et al. 2017)
Microsatellite markers (SSR) transferred from potato to its
wild relatives can be used to screen for genetic variability.
An example of this is the evaluation of 10 accessions from
S. chacoense using 15 SSR markers developed for potato,
which showed high levels of heterozygosity in the collection
(Haynes et al. 2017)
. Using sequence data, new SSR markers
can be specifically devised for wild species, increasing their
amplification success and polymorphic information content.
This is what happened for a diversity panel of S. commersonii
accessions and for a biparental population both screened with
SSR markers developed from short read sequence data
(Sandro et al. 2016)
. Adding value to collected samples in
gene banks through all this genetic and genomic information
and mining allele variation from natural populations or ex situ
collections will be critical for the efficient use of potato WR in
the genomics era.
Breeders can use potato WR to introduce new genes in a
commercial cultivar or to select superior alleles to replace their
cultivated counterparts through cisgenesis. They can also use
structural and functional genomic information on potato WR
to adopt as templates to target specific sites and edit gene
sequences in elite cultivars. In the case of genome editing,
knowing the target genome sequence is essential to prevent
targeting of repeated sequences dispersed throughout the
genome and to respond to regulatory demands
However, most of the time breeders do not aim at transferring
only one gene of interest but to broaden the genetic base of a
(Bradshaw 2007b; Bradshaw 2016)
introduce adaptability and hardiness from potato WR usually
growing in a wide variety of environments
(Bethke et al.
. Such a time-consuming process depends on many
backcrosses to recover the cultivated background that was lost
with the initial hybridization. It is also claimed that the
undesirable traits that come from the potato WR are hard to
remove, especially in a tetraploid potato background. An idea
that is gaining popularity is the use of diploid inbred lines in
(Lindhout et al. 2011; Endelman and Jansky
2016; Jansky et al. 2016)
. These allow for easier genetic
mapping with increased resolution and simplify genetic analysis
because of their disomic inheritance
(Endelman and Jansky
. In breeding, they can be used to create F1 hybrid seed
with enhanced heterosis that can be propagated through true
(Lindhout et al. 2011; Jansky et al. 2016)
WR have a role to play both in the development of diploid
inbred lines and in their use as breeding material. One of the
most frequently used strategies to achieve diploid inbred lines
is through the crossing with a S. chacoense genotype carrying
a dominant self-incompatibility inhibitor allele called Sli
(Hosaka and Hanneman Jr 1998; Phumichai et al. 2005;
Lindhout et al. 2011; Jansky et al. 2016)
. After the diploid
inbred lines are obtained, they can generally be crossed
directly with diploid potato WR facilitating introgression at the
(Jansky 2006; Jansky et al. 2016)
Many of the limitations in introgressive hybridization
breeding can be overcome by an efficient use of new genomic
technologies and approaches. These will allow prediction of
homology and collinearity to anticipate the degree of pairing,
recombination and linkage drag expected in any interspecific
cross, together with mining of existing variation in natural
populations and optimal choice of the genotypes to start
introgression schemes. Genomics will not only facilitate
marker-assisted selection for the traits of interest but also
against the wild donor chromatin. To the question posed by
(Bethke et al. 2017)
in their review paper: Are we getting
better at using Wild Potato Species in Light of New Tools?
The answer is clearly Yes, but the possibilities are still endless.
The approaches we are now developing may still seem
expensive and difficult to apply to routine breeding; however,
information is accumulating fast. At the current rate of
technological advance in the automation of data acquisition and
analysis, it does not seem impossible to envision the fulfillment of
the promises of the use of potato WR in the near future, as
long as we keep going in that direction.
Acknowledgements P. Gaiero was supported by grant Proyecto 720 and
CSIC Recursos Humanos, University of the Republic. We thank
Alejandro Vaco and Germán Abad for kindly providing some of the
photographs in Fig. 1. We are grateful to Francisco Vilaró for useful
comments during the development of this work. We are also thankful to
four anonymous reviewers for their comments to improve this work.
Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://creativecommons.
org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to
the original author(s) and the source, provide a link to the Creative
Commons license, and indicate if changes were made.
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