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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
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Article outline
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Abstract
Keywords
1. Introduction
2. Materials and methods
3. Results
4. Discussion
5. Conclusion
Acknowledgements
References
Scientia Horticulturae
Table 1
doi:10.1016/j.scienta.2010.02.021
Table 2
Abstract
To assess the intra-population genetic variability and draw criteria for distinctiveness, 25 accessions
belonging to the Italian tomato landrace A pera Abruzzese were analyzed with morphological and
molecular descriptors and compared with the similar landraces Canestrino di Lucca and Cuore di bue di
Albenga. Whereas intra-accession variation for qualitative morphological descriptors was low, interaccession variability was high. Accessions from the Abruzzese landrace could be separated into three
groups according to the fruit shape, i.e. flat, round and obovoid. This variability was studied in detail by
digital analysis of fruit sections using the software programme Tomato Analyzer. Four descriptors were
Table 3
effective in distinguishing the Abruzzese round-fruited types from the Canestrino and Albenga controls.
The molecular analysis, based on 11 polymorphic microsatellite markers, differentiated the Abruzzese
from the Canestrino type, but was not able to separate the former from the Albenga type. Although
morphological and molecular descriptions did not correlate, the data presented provide a basis for
distinguishing those Abruzzese accessions that are unequivocally distinct from similar landraces
cultivated in different regions. In addition to the specific objectives, the research represents a case study
for the description of the variability that is often found within tomato landraces and an approach to identify
(groups of) accessions that are eligible for distinction, protection and commercial exploitation.
Keywords
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A pera Abruzzese; Distinctiveness; Genetic variation; Landraces; Solanum lycopersicum L.; SSR
1. Introduction
The tomato (Solanum lycopersicum L.) was first introduced into Europe from Central and Southern
America at the beginning of the 16th century and cultivated as an ornamental. In the 17th century the
species gained popularity as an edible product and its cultivation spread rapidly throughout the Old World.
This introduction resulted in a genetic bottleneck, narrowing the genetic diversity of the cultivated
germplasm in Europe ( Rick, 1976). The genetic heritage of the tomato was further eroded by the
development of vintage and modern cultivars, when much of the original diversity within the cultivated S.
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
lycopersicum was lost ( Williams and St. Clair, 1993).
Despite the significant loss of genetic diversity and in stark contrast to the invariably round-shaped fruit of
its wild relatives, the cultivated tomato displays a large diversity of fruit morphology. It is now accepted that
this morphology is based on the allelic variation of a relatively small number of genes that recombined after
domestication and during the early cultivation of the species (Tanksley, 2004). In Europe, the tomato has
been most successful in the Mediterranean countries, including Spain and Italy (Soressi, 1969 and GarcaMartnez et al., 2006). In these countries, S. lycopersicum found a secondary centre for diversification (
Bailey et al., 1960) which resulted in a wide array of variations including round, obovoid, long, heart,
rectangular and even bell pepper-shaped fruits. This variation has given rise to a range of landraces that
have been cultivated for centuries and many of these are still commonly found at local markets ( Soressi,
1969 and Garca-Martnez et al., 2006).
Among the tomato landraces destined for fresh consumption, the so called salad tomatoes, those with
large isodiametric fruits are widely grown in both Spain and Italy (Garca-Martnez et al., 2006, Acciarri et
al., 2007 and Mazzucato et al., 2008). In many of these types the uneven development of the equatorial
diameter at the blossom or stem end causes the fruit to develop a typical pear (obovoid) or heart shape and
this distinctive feature is reflected in the name given to the particular landrace.
The landrace under study, known as A pera Abruzzese, is widely cultivated in Central Italy in the Northern
part of the Abruzzo region, along the Adriatic sea. This landrace, which has a local niche market where it is
appreciated for its outstanding organoleptic qualities, commonly includes both plants that produce
spherical and obovoid-shaped fruit (Sabatini et al., 2006). Morphologically very similar to the A pera
Abruzzese type are the so called Cuore di bue di Albenga (from Ligury; the name recalls an heart but the
fruit shape is actually obovoid) and the Canestrino di Lucca (from Tuscany) landraces. Whereas the
above mentioned landraces have pear-shaped fruits, the Cuore di bue tomato (different from Cuore di
bue di Albenga) differs because of the wider extension of the stem end diameter compared to the blossom
end, resulting in a characteristic heart shape. This tomato, which appears to have originated in Sicily,
differs from the pear-shaped tomatoes in that its fruit is pink, due to the colorless epidermis (y) mutation.
Finally, another round, multilocular tomato, known as Pomodoro di Sorrento, is cultivated in the Campania
region. Like the Cuore di bue, the Sorrento landrace also expresses the y phenotype giving the fruit a
typical pinkish tone ( Parisi et al., 2008).
Although these typologies are popular in the marketplace for their organoleptic qualities and their
characteristic traditional shapes, the intra-landrace levels of genetic variability as well as their genetic
relationships have been never studied in detail, nor have they ever been described according to clear and
distinctive criteria. In this study, we set out to examine the genetic variability present within the Abruzzese
landrace, with the aim of establishing the extent and nature of intra-landrace variability with special
reference to fruit size and shape. With this information we aim at defining the criteria that will allow us to
distinguish unequivocally Abruzzese accessions from those belonging to other landraces with similar fruit
attributes.
Accession
Year of
Fruit
Fruit
production
Landrace
Province
Site
name
code
acquisition
shape
size (g)a
(t ha1)a
A pera
Teramo
Teramo
Gigante
AB-FL1
2001
Flat
261
44.8
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Abruzzese
Giraldi
Teramo
Teramo
Gigante
d
AB-FL2
2001
Flat
ndb
ndb
AB-RD1
2002
Round
233
b-
58.1
a-d
Faggi
Teramo
Martinsicuro
Pera
Martinsicuro
Teramo
Morrodoro
Selezione
AB-RD2
2001
Round
298
57.2
a-d
AB-RD3
2002
Round
215
e-
48.0
c-i
41.4
g-l
De Santis
Teramo
Colleranesco
Globoso
dAbruzzo
Teramo
Colleranesco
Spitilli
m
AB-RD4
2001
Round
207
fm
Teramo
Teramo
Pera Santo
AB-RD5
2001
Round
221
d-l
50.9
b-g
Stefano
Teramo
Giulianova
Giulianova
AB-RD6
2001
Round
223
d-i
54.1
b-f
Teramo
Roseto
Belisari
AB-RD7
2003
Round
266
b-
58.5
a-c
46.3
e-l
44.3
f-l
40.2
g-m
Ernesto
Teramo
Teramo
Pera
c
AB-RD8
2001
Round
217
Rotolone
Teramo
Colleranesco
Colleranesco
m
AB-RD9
2001
Round
206
Teramo
Teramo
Roseto
Pera
e-
fm
AB-RD10
2002
Round
209
Obovoidson
fm
Teramo
S. Omero
Sabini Dino
AB-RD11
2003
Round
270
bc
40.2
g-m
Teramo
Villarosa
Pera
AB-RD12
2002
Round
232
c-
41.0
g-m
44.8
f-l
53.7
b-f
Ritrovati
Teramo
Colleranesco
Di Silvestro
h
AB-OB1
2001
Obovoid
203
fm
Teramo
Mosciano
Pera
SAngelo
Mosciano
AB-OB2
2001
Obovoid
212
f-
Teramo
Cologna
Castorani
AB-OB3
2001
Obovoid
366
38.1
i-m
Teramo
Villa Vomano
Pera
AB-OB4
2001
Obovoid
268
bc
52.8
b-f
Cantoro
Pescara
Pescara
Pescara 2
AB-FL3
2001
Flat
348
49.4
b-h
Pescara
Loreto
Pera
AB-FL4
2002
Flat
236
c-
59.8
ab
Aprutino
Ortoplant
Loreto
Loreto
52.5
b-f
Aprutino
Aprutino
Pescara
Pescara
Pescara 1
AB-RD13
2001
Round
244
c-f
41.8
g-l
Chieti
Chieti
Pera Chieti
AB-RD14
2001
Round
255
c-
67.3
40.5
g-m
67.2
55.5
b-e
Pescara
g
AB-FL5
2001
Flat
199
gm
e
Ascoli
Porto
Picenoc
DAscoli
Ascoli
Centobuchi
Picenoc
Canestrino di
Pisad
Pera Sentina
AB-OB5
2001
Obovoid
193
m
Pera
AB-OB6
2000
Obovoid
198
Centobuchi
Pisa
Lucca
Canestrino
Fornoli
Canestrino
gm
CAN1
2006
Obovoid
175
Pisa
Luccad
g-
mn
CAN2
1999
Obovoid
150
30.8
mn
Obovoid
193
g-
47.7
d-i
Lucca
Cuore di bue di
Commercial
Albenga
Albenga
seed
Olter
Commercial
Albenga
seed
Esasem
Commercial
Albenga ISI
seed
ALB1
m
ALB2
Obovoid
178
l-n
36.5
l-n
ALB3
Obovoid
189
h-
38.8
h-m
Means followed by the same lowercase letter in the same column are not significantly different (P 0.05) according to the Duncan multiple range test.
Marche region.
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d
Tuscany region.
Table options
A second field trial, including the control accessions, was established in 2008 using the same experimental
design and agronomic practices. On a single plant basis, the following traits were scored or measured:
flowering date (days from sowing to the first open flower), inflorescence type (scored on the 2nd truss; 1,
simple; 2, double; 3, compound), number of flowers per inflorescence (counted on the 2nd truss), style
exertion (scored on the 2nd truss; 1, inserted; 4, very exerted), green shoulder (scored on a representative
mature green fruit; 1, absent; 7, very strong), fruit shape (scored on representative red ripe fruits; 1, flat; 2,
round; 3, obovoid). Mean fruit weight was calculated as the mean of six fruits per plant and the potential
productivity, expressed in t ha1, was estimated on the basis of the individual production and the standard
plant density in open field production of fresh tomatoes.
With the exception of fruit shape that represented a purely categorical variable, differences in mean values
between accessions were estimated through an analysis of variance adopting the General Linear Model
(GLM) using the SAS software (SAS Institute Inc., 2002). Differences in the mean number of fruits per plant
and fruit weight as estimated in two different cultivation years were estimated according to the GLM for
combined experiments (McIntosh, 1983).
size
First
Chromo-
Annealing
range
describeda
some
temperature
2008)b
present study
(bp)
A pera
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All
Abruzzese
genotypes
accessions
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
LEMDDNa
(1)
55
211
229
LE20592
(1)
11
55
LESSRPSPGb
(1)
ndc
50
LEEF1Aa
(1)
ndc
55
11
184
187
325
328
208
216
TMS42
(2, 3)
11
52
TMS52
(3)
12
5247d
TMS60
(3)
5247d
TMS63
(3)
55
253
258
152
162
244
246
130
156
EST253712
(3)
51
140
142
Tom4748
(4)
48
Tom236237
(4)
52
168
172
157
193
Total
71
43
33
Mean
6.5
3.9
3.0
(1) (Smulders et al., 1997), (2) (Areshchenkova, 2000), (3) (Areshchenkova and Ganal, 2002), (4) (Suliman-Pollatschek et al., 2002).
Not determined.
Touch-down PCR program with annealing temperature decreasing by 0.5 C per cycle in the first 10 cycles.
Table options
Each individual was genotyped at each locus by scoring the length of the amplified SSR band with
reference to molecular ladders and genotypes of known allelic composition. Three loci (LEACS4A, TMS58
and Tom5960) were monomorphic in the set of genotypes studied and were excluded from subsequent
analyses. Data from the 11 informative loci were converted into binary data and genetic distance (Nei et al.,
1983) matrices and cluster analyses based on the unweighted pair group method (UPGMA) of (Sneath and
Sokal, 1973) were calculated using the TREECON Ver. 1.3b software (Van de Peer and De Wachter,
1993).
The dissimilarity matrices obtained from the fruit section data and from the SSR analysis were compared
by Mantel test using the XLSTAT 7.5.2 software.
3. Results
3.1. Morphological analysis
All the accessions produced plants with indeterminate growth habit (not shown). The ANOVA revealed
significant differences between genotypes for all the other morphological and yield traits; the Abruzzese
accessions showed wide variability for all of them (Fig. 1). Flowering date ranged from 73 to 82 days after
sowing, inflorescence type from simple to compound, number of flowers per inflorescence from 8 to 21,
style exertion from inserted to very exerted; green shoulder from absent to present and very intense (Fig.
1AE). As regards the scoring of fruit shape (Fig. 1F), five Abruzzese accessions were classified as flat
(Fig. 2A), 14 as round (Fig. 2B) and six as obovoid (Fig. 2C). In the Abruzzese collection, fruit weight
ranged from about 190 to 366 g; the estimated productivity from 38 to more than 67 t ha1 (Table 1).
Notably, the accession AB-OB3 scored the highest fruit weight and the lowest estimated productivity at the
same time, thus indicating that these two traits are not positively correlated in the materials we have
studied.
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
Fig. 1.
Number of accessions of the A pera Abruzzese (n = 25, gray bars), Cuore di bue di Albenga (n = 3, white bars) and Canestrino di
Lucca (n = 2, black bars) landraces falling in different classes for seven morphological descriptors (AG) and estimated
productivity (H). Abscissa axes report class limits as days from sowing (A), score [B (1, simple; 2, double; 3, compound), D (1,
inserted; 4, very exerted), E (1, absent; 7, very strong), F (1, flat; 2, round; 3, obovoid)], ordinal number (C), grams (G) and t ha1
(H), whereas ordinate axes report absolute frequencies.
Figure options
Fig. 2.
Representative mature fruits from Abruzzese accessions having fruits scored as (A) flat, (B) round and (C) obovoid-shaped.
Figure options
The control accessions belonging to Canestrino and Albenga landraces showed a typically obovoid fruit
(Fig. 1F). Although here only few accessions have been considered, anecdotal evidence indicate that the
fruit shape in these landraces is more uniform (G.P. Soressi, personal communication). Fruits from the
Canestrino and Albenga accessions were also amongst the smallest in size (Fig. 1G; Table 1) and their
estimated production was low for the Albenga and intermediate for the Canestrino types (Fig. 1H; Table
1).
When data related to the productivity of Abruzzese landraces were compared between the 2007 and 2008
growing seasons, highly significant differences in fruit size and estimated productivity were apparent
between accessions, between years and for the Accession year interaction (data not shown). Only the
fruit size between years was not significantly different, indicating that the environment exerts a significant
influence on fruit setting and fruit size in these genotypes and that this influence can vary for individual
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accessions.
Acc
Inf
Type
Inf
***
***
fdI
***
***
Height max
flI
***
***
fsI
***
***
***
tri
***
***
ell
***
***
cir
***
***
pan
***
***
dan
Eccentricity
ecc
***
**
***
int
***
***
***
Lobedness degree
lob
***
***
Pericarp thickness
per
***
***
Descriptor namea
Symbol
Area
ar
Width max
All measurements are described in Brewer et al. (2006) and Gonzalo et al. (2009).
***, ** and * indicate differences between mean values statistically significant for P 0.001, 0.01 and 0.05, respectively.
Table options
The same analysis of variance was carried out after grouping the Abruzzese accessions according to the
fruit shape type, as judged in the previous section, into three groups, leaving Canestrino and Albenga as
two separate groups. All the variables showed significant differences between types, with the exception of
dan; in contrast, no highly significant difference was found between inflorescences or for the
Type inflorescence interaction ( Table 3). No variable could unequivocally differentiate all three
Abruzzese typologies from Canestrino and Albenga. However, the variables tri, pan, ecc and int showed
significant differences separating the groups Canestrino, Albenga and Abruzzese obovoid-shaped from
the others ( Fig. 3). In comparison to the latter, the Abruzzese flat and round groups had significantly
higher values for the tri and pan variables and significantly lower values for ecc and int variables ( Fig. 3).
For these four descriptors, the degree of overlapping between Canestrino, Albenga and Abruzzese
obovoid-shaped with the accessions of the other groups was low (data not shown).
Fig. 3.
Mean values of groups of accessions homogeneous for the fruit shape for the fruit section descriptors fruit shape triangle (tri),
proximal angle macro (pan), eccentricity (ecc) and internal fruit shape index (int). Bars represent the mean value of 1418
measurements SEM. Means indicated by the same lowercase letter for the same descriptor are not significantly different for
P 0.05.
Figure options
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
The dissimilarity matrix obtained from the fruit section descriptors was used for a clustering procedure. The
resulting dendrogram displayed two major groups of genotypes, the first including four flat plus one round
type and the second all the other accessions (Fig. 4A). The second cluster could be further divided into
subclusters, of which a lower level one was only composed of round-shaped accessions (Fig. 4A, shaded
box).
Fig. 4.
Grouping of accessions of the A pera Abruzzese and control types according to (A) the morphological and (B) molecular analysis.
The dendrogram in (A) has been generated using the morphometric fruit shape descriptors by the Agglomerative Hierarchical
Clustering method based on Manhattan distances and average linkage fusion criterion. The dendrogram in (B) has been
generated after genotyping for 11 SSR markers and clustering according to the unweighed pair group method (UPGMA) based on
Nei distances. The same nine round-shaped accessions are shaded in gray in the two dendrograms.
Figure options
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
descriptors and on the molecular markers were not significantly correlated (P = 0.46, r = 0.03).
4. Discussion
Among vegetable species, the tomato stands out from the crowd in terms of area under cultivation,
consumption and also for the variability offered by traditional types and landraces (Ercolano et al., 2008,
Mazzucato et al., 2008 and Terzopoulos and Bebeli, 2008). Unfortunately in Italy a great number of
landraces have been dropped from the National Register, due to lack of commercial interest from major
seed companies, and relatively few traditional types have been accepted into alternative variety protection
systems. To date, only the San Marzano landrace has received a Protected Designation of Origin
labelling, that guarantees the geographic and genetic origin of the produce (Rao et al., 2006); this landrace
has been the focus of a number of studies to determine the criteria upon which it can be distinguished from
similar selections and hybrids (Loiudice et al., 1995, Rao et al., 2006 and Caramante et al., 2009).
Large tomatoes with diameters of similar length represent a class of very popular table tomatoes,
appreciated for their outstanding organoleptic qualities, few seeds and the traditional shape of the fruit
(round, obovoid or heart). Italy has at least five geographically distinct landraces belonging to this category;
their genetic relationships as well as their distinctiveness have not been investigated thoroughly to date.
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Genetic diversity and distinctiveness in tomato (Solanum lycopersicum L.) landraces: The Italian case study of A pera Abruzzese
cultivation together with the round autochthonous accessions, they may have intercrossed and then been
subjected to selection by farmers. Alternatively, the Albenga type could have been derived from
Abruzzese morphotypes with obovoid-shaped fruits. A similar scenario may also be evoked to understand
the appearance of flat types, which may have been derived from crosses of round types with Marmande or
Marmande-like genotypes.
Whatever the origin, there is evidence that each landrace and morphotype was subjected to selection for
genetic adaptation to the physical and agronomic environment, because the Abruzzese entries remained
more productive than the others in their own environment of adaptation. A similar result was reported for
the Sorrento landrace, whose accessions, in their environment, were generally more productive than both
Abruzzese or Albenga types (Parisi et al., 2008).
In Spain, researchers studied the genetic variation in a collection of autochthonous landraces including
nine accessions of De la pera, a landrace that shows morphological similarities to the Abruzzese type.
Although these authors did not perform a morphological characterization of the materials, the use of
molecular analysis was not sufficient to discriminate all the De la pera accessions from the other materials
(Garca-Martnez et al., 2006).
A distinctiveness analysis of the Abruzzese and Albenga types has previously been carried out by
Sabatini et al. (2006) who established that the two types were distinct in the stem end blockiness and, at
the molecular level, by a CAPS marker based on the mutation of the Ovate gene ( Liu et al., 2002) that
could be of help in marker-assisted selection. However, the same authors found a line with the Albengatype Ovate allele in the Abruzzese germplasm ( Sabatini et al., 2006). In the present research, although
analyses of the Ovate locus were not performed, we bring evidence that accessions with the typical
morphology of the Albenga type are rather frequent in the Abruzzese germplasm and probably derived
from intercrossing and subsequent selection between the two main types.
5. Conclusion
Taken altogether, the data indicates that genotypes with obovoid-shaped fruits could not be clearly
distinguished as originating from the tomato germplasm of Ligury or Abruzzo. In contrast, those accessions
representing the group with round-shaped fruit may be distinguishable from similar landraces (Albenga
and Canestrino) and from obovoid and flat-shaped accessions of the same landrace by fruit shape
descriptors that are objectively scorable. Thus the factors that define and distinguish Abruzzese from
other landraces with large fruits with similar diameters (fsI between 0.9 and 1.1), will be those
distinguishing the round-shaped accessions, i.e. values of tri between 0.8 and 1.1, pan between 1.9 and
2.3, ecc between 0.57 and 0.61 and finally int between 0.8 and 1.0. The combination of these limits with the
molecular marker based on the allelic status at the Ovate locus ( Sabatini et al., 2006) can definitely be
employed to identify a group of the landrace accessions, so that they may then be recognized and
labelled as typical produce of the Abruzzo region and finally valued and protected from undesirable
substitutions.
Acknowledgements
The authors wish to thank Mr. M.E. Picarella and L. Bonifazi for expert technical assistance, Dr. E. van der
Knaap for suggestions on the tomato shape nomenclature, Prof. G.P. Soressi and two anonymous
reviewers for helpful comments on the manuscript. This study was supported by the Agenzia Regionale pe
r i Servizi di Sviluppo Agricolo (ARSSA) of the Abruzzo region, project Colture Orticole.
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Corresponding author. Tel.: +39 0761 357370; fax: +39 0761 357242.
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