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J Sci Food Agric 1998, 78, 220È224
Variation in Seed Protein Content in the Annual
Wild Cicer Species
Bruno Ocampo,* Larry D Robertson and Kharag B Singh1
International Center for Agricultural Research in the Dry Areas (ICARDA), PO Box 5466, Aleppo, Syria
(Received 14 March 1997 ; revised version received 9 January 1998 ; accepted 4 February 1998)
Abstract : In a search for higher seed protein content than in cultivated chickpea
(Cicer arietinum L), the authors evaluated a collection of 228 accessions from the
International Center for Agricultural Research in the Dry Areas (ICARDA), representing the eight annual wild species of the genus Cicer, along with 20 cultivated chickpea check lines. Variation in seed protein content ranged from
168 g kg~1 in C cuneatum Hochst ex Rich to 268 g kg~1 in C pinnatiÐdum Jaub
& Spach, with an average seed protein content of 207 g kg~1 over the eight wild
species. C yamashitae Kitamura had the highest mean (217 g kg~1), while C
echinospermum PH Davis had the lowest (192 g kg~1). The mean protein content
of the cultivated checks was 188 g kg~1. SigniÐcant variation was present in C
judaicum Boiss, C pinnatiÐdum and C reticulatum Ladiz. C pinnatiÐdum had the
highest number of accessions with high protein content. Overall, protein content
showed negative association with harvest index, but little association with leaf
area, days to maturity and canopy width. Although the variation for seed protein
content of the collection showed accessions with higher protein content than
with the cultivated checks, it falls within the range reported for cultivated chickpea. It is expected that agronomically superior selections from interspeciÐc
hybrids involving C arietinum and its annual relatives should not be inferior to
the cultigen in protein content. Moreover, as usually occurs in distant hybridisation, unexpected epistatic e†ects could produce positive transgressive segregants, as has already been reported in Cicer. ( 1998 Society of Chemical
Industry
J Sci Food Agric 78, 220È224 (1998)
Key words : breeding ; chickpea ; Cicer arietinum ; germplasm ; legumes ; pulses ;
quality ; wild species
INTRODUCTION
its protein quality is superior to most food legumes
(Bressani 1973 ; Meiners and Litzenberger 1973 ;
Chavan et al 1986). Therefore, chickpea plays an
important role in complementing the biological
value of staples based chieÑy on cereals, roots, tubers
and plantain crops.
There is strong evidence of the possibility of substantial improvement of protein content in food legumes
(Moreno 1983).
The genus Cicer comprises 43 species, 33 perennials
and 9 annuals, including the cultivated chickpea and 1
unspeciÐed (van der Maesen 1987). The International
Center for Agricultural Research in the Dry Areas
(ICARDA, Aleppo, Syria) maintains the worldÏs largest
collection of wild Cicer species (270 accessions) and of
the kabuli-type chickpea (9870 accessions). The phenological, agronomic and stress reaction features of the
Protein quantity is one of the most serious aspects of
food deÐcit in developing countries. Chickpea is a valuable source of protein for diets in developing countries,
where about 95% of the crop is produced (FAOSTAT
1995).
Seed protein content is the most important quality
factor for chickpea breeding programmes. Chickpea
seed protein content is low compared with other food
legumes (Meiners and Litzenberger 1973) ; however,
* Joint publication from ICARDA and ICRISAT
(International Crops Research Institute for the Semi-Arid
Tropics), Patancheru PO, AP 502, 324, India.
1 Present address : KB Singh, 81 Chander Nagar, Janakpuri,
A Block, New Delhi 110058, India.
* To whom correspondence should be addressed.
220
( 1998 Society of Chemical Industry. J Sci Food Agric 0022È5142/98/$17.50.
Printed in Great Britain
Seed protein content in annual wild Cicer species
221
TABLE 1
Annual wild Cicer species germplasm used in this study and their country of origin
(ICARDA Genetic Resources Unit)
Origin
Afghanistan
Ethiopia
Jordan
Lebanon
Palestine
Syria
Turkey
Total
Cicer speciesa
ari
ret
ech
jud
pin
bij
cho
yam
cun
4
2
3
1
2
7
1
È
È
È
È
È
È
51
È
È
È
È
È
È
11
2
2
8
17
9
22
7
È
1
È
1
5
8
34
È
È
È
È
È
4
33
5
È
È
È
È
È
È
3
È
È
È
È
È
È
È
4
È
È
È
È
È
20
51
11
67
49
37
5
3
4
a ari, arietinum (check) ; ret, reticulatum ; ech, echinospermum ; jud, judaicum ; pin, pinnatiÐdum ; bij, bijugum ; cho, chorassanicum ; yam, yamashitae ; cun, cuneatum.
annual wild Cicer species collection of ICARDA have
been catalogued (Robertson et al 1995).
Wild relatives of chickpea are reported to be promising sources of genes for resistance to the major biotic
and abiotic factors which a†ect yield stability in chickpea (Singh et al 1989 ; Weigand and Tahhan 1990 ;
Singh and Reddy 1993 ; Kaiser et al 1994 ; Singh and
Weigand 1994 ; Di Vito et al 1996). There are many
examples of crops improved by means of wide hybridisation (Prescott-Allen and Prescott-Allen 1988). For
almost a decade, ICARDA has embarked on a wideranging enterprise of exploiting the annual wild Cicer
species for the improvement of the cultigen (Ocampo
1995 ; Singh and Ocampo 1997).
The objective of this study was to estimate the variability of seed protein content of a collection of annual
wild Cicer species.
MATERIALS AND METHODS
The material of this study comprised 228 accessions of
eight annual wild Cicer species from the ICARDA genebank : C bijugum KH Rech, C chorassanicum (Bunge) M
Popov, C cuneatum Hochst ex Rich, C echinospermum
PH Davis, C judaicum Boiss, C pinnatiÐdum Jaub &
Spach, C reticulatum Ladiz and C yamashitae Kitamura
and 20 randomly selected kabuli-chickpea (C arietinum
TABLE 2
Statistical distribution of seed protein content (g kg~1, Kjeldahl procedure) in the annual Cicer species collection of ICARDA
State
Meanc
SE (^)
SD
Range
Skewness
Kurtosis
Cases
Cicer speciesa
Totalb
ari
ret
ech
jud
pin
bij
cho
yam
cun
188d
0É20
0É88
171È203
0É08
[0É62
20
201bc
0É10
0É69
188È205
[0É10
[0É66
51
192cd
0É25
0É84
174È210
[0É02
3É26
11
210ab
0É13
1É05
190È231
0É09
[0É85
65
210ab
0É21
1É42
194È268
1É92
5É05
47
212ab
0É11
0É66
200È226
0É53
[0É56
35
194c
0É70
0É99
187È201
NEd
NE
2
217a
2É19
3É79
174È247
[1É35
NE
3
201bc
1É23
2É46
168È220
[1É81
3É27
4
207
0É08
1É22
168È268
0É710
3É132
217
146
215
185
232
226
215
251
Accession numbers with highest seed protein content within each species
2639
182
179
193
226
178
2758
229
239
173
251
80
6455
233
180
206
221
83
a ari, arietinum (check) ; ret, reticulatum ; ech, echinospermum ; jud, judaicum ; pin, pinnatiÐdum ; bij, bijugum ; cho, chorassanicum ;
yam, yamashitae ; cun, cuneatum.
b calculated considering only the wild Cicer species.
c Means followed by same letters are not signiÐcantly di†erent at P \ 0É05.
d Not estimable.
B Ocampo, L D Robertson, K B Singh
222
TABLE 3
Analysis of variance for seed protein content (g kg~1) of Cicer
species
Source of variation
df
Mean
square
F-value
Accessions within species
C arietinum
C bijugum
C cuneatum
C echinospermum
C judaicum
C pinnatiÐdum
C reticulatum
C yamashitae
19
34
3
10
64
46
50
2
1É563
0É865
10É734
1É405
2É234
4É142
1É572
8É725
1É92
1É55
6É09
1É10
3É00**
4É96**
3É55**
5É39
7
2É075
5É48*
Species
* SigniÐcant at P \ 0É05 ; ** signiÐcant at P \ 0É01.
L) accessions representing the geographical distribution
of the wild Cicer collection. Table 1 shows the countries
of origin of the accessions evaluated in this study, along
with the number of accessions per species. Seed samples
were obtained from plants grown during 1993È94 at Tel
Hadya (36¡35@E, 36¡51@N and 284 m asl), Syria, the
main research station of ICARDA. Morphological, phenological, agronomic and seed details and stress reactions of these 248 accessions are given in Robertson et
al (1995). This site has a semi-arid continental Mediterranean climate. Rainfall during the 1993È94 season was
373 mm. Tel Hadya soils are Ðne clay montmorillonitic,
thermic calcixerollic xerochrept with a pH of about 8É0.
They are low in organic matter (about 1É0%) and in
available phosphorus (about 5 lg g~1 at 0È20 cm, and
about 3 lg g~1 at 20È40 cm).
The 248 accessions were grown in a randomized complete block layout with two blocks. Each accession was
sown in a three-row plot 2 m long with spacing of
45 cm between and 15 cm within rows on 29 November
1993. Forty seeds of each accession were sown in each
plot. The plots were fertilised with 50 kg P O ha~1.
2 5
Hand-weeding was done three times. The crop was protected from ascochyta blight (Ascochyta rabiei (Pass)
Lab) by a periodic spraying of the fungicide chlorothalonil (tetrachloroisopenthalonitrite) at the rate of 0É8 kg
a.i. ha~1.
Seed protein content was determined according to the
macro-Kjeldahl procedure AACC 46-12 (AACC 1983) ;
the N to protein factor used was 6É25. The g kg~1 data
were based on dry matter using seeds from three
randomly-selected plants of the central row of the plots.
Analyses of variance were carried out using
MSTAT-C (1988) version 2.10. Simple correlation coefÐcients (Pearson coefficients) and frequency distributions of selections were obtained using SPSS for
Windows, Release 6.0 (SPSS 1993). Derivatives accessions, previously established based on morphological
Fig 1. Frequency distributions of derivatives (y axis) for seed
protein content (g kg~1) (x axis). The Ðrst number below the
species name refers to the International Legume Wild Cicer
accession number of the original accession, while the following
number in parenthesis refers to the collection number (number
or pedigree identiÐcation code used by the donor). The black
vertical line within each chart indicates the original accession
seed protein content.
grounds, were analysed to determine variation within
populations (accessions) for protein content.
RESULTS
The present evaluation showed wide variation for seed
protein content in the annual wild Cicer species (Table
2). Distribution patterns varied from normal to strongly
skewed with high kurtosis. Protein content ranged from
168 g kg~1 in C cuneatum to 268 g kg~1 in C pinnatiÐdum. Mean seed protein content of the annual wild
Cicer collection was 207 g kg~1. SigniÐcant mean differences (P \ 0É05, Table 3) were recorded among the
species, where C yamashitae, C bijugum, C judaicum and
Seed protein content in annual wild Cicer species
223
C pinnatiÐdum showed the highest means and C echinospermum the lowest. The mean seed protein content of
the cultigen set used in this study was signiÐcantly
lower than those of the wild Cicer species, except for C
echinospermum (Table 2).
SigniÐcant variation was present among accessions of
C judaicum, C pinnatiÐdum and C reticulatum (Table 3).
Protein content among derivatives of single accessions was variable (Fig 1). The variation was less pronounced in C bijugum compared with C echinospermum,
C judaicum, C pinnatiÐdum and C reticulatum. Most
derivatives of C judaicum accessions showed higher
protein content compared with the original accessions.
Linear phenotypic correlations between seed protein
content and morphological, phenological and agronomic characters di†ered among species (Table 4). The
highest number of signiÐcant associations were recorded in C pinnatiÐdum and the least in C judaicum.
Overall, the highest correlations were between seed
protein content and harvest index (negative). Less signiÐcant associations were found with 100-seed weight
(negative), days to Ñowering (positive), seed yield
(negative) and number of seeds per pod (negative and
positive correlations) (Table 4).
DISCUSSION
The variability for seed protein content of the ICARDA
collection of annual wild Cicer species was large. The
present results di†er substantially from those of Singh
U and Pundir (1991), who reported the protein content
to range from 265 g kg~1 in C yamashitae to
327 g kg~1 in C bijugum. These di†erences might have
been caused by di†erences in the environment and in
the methodology used (decorticated samples) and by the
small number of accessions used by Singh and Pundir
(21 compared with 248 in the present work), who
scanned only a small proportion of the available annual
wild Cicer species genetic diversity. The data reported
here suggest that the prospects for upgrading the nutritional value (protein content) of chickpea via introgression of wild Cicer species genes into the domesticated
are remote, since the seed protein content variability of
the wild accessions falls within the range reported for
cultivated chickpea (Chavan et al 1986 ; Hulse 1994). A
more realistic approach to chickpea improvement using
these species in distant hybridisation may be to ensure
that the seed protein content of hybrid selections does
not fall below that of existing cultivars. This should be
easy to do, as most wild species (except C pinnatiÐdum)
had mostly non-signiÐcant correlations between protein
content and most agronomic traits (Table 4). Furthermore, as usually occurs in distant hybridisation, unexpected epistatic e†ects could produce positive
transgressive segregants, as has already been reported in
Cicer (Ocampo 1995) and other crops for quantitative
traits (Cox et al 1984 ; Frey et al 1984 ; Carpenter and
Fehr 1986).
Variation for seed protein content among derivatives
from a single accession underline the necessity for
careful evaluation within accessions discriminated on
morphological traits.
The variation between species in phenotypic correlations between seed protein content and some morphological, phenological and agronomic descriptors are an
TABLE 4
Linear correlations (Pearson coefficients) between seed protein and some morphological, phenological and
agronomic descriptors
Descriptor
Leaf area
Days to 50% Ñowering
Days to maturity
Plant height
Canopy width
Pods/plant
Seeds/pod
Biological yield
Seed yield
Harvest index
Seeds/plant
100-seed weight
Cicer speciesa
ari
(20)
ret
(50)
ech
(11)
jud
(65)
pin
(47)
bij
(35)
0É104
[0É066
0É128
0É253
[0É152
0É186
0É168
[0É249
[0É383
[0É536*
0É296
[0É450*
0É027
0É088
[0É017
[0É291*
[0É106
0É019
[0É117
0É075
[0É094
[0É443**
[0É018
[0É120
[0É038
0É654*
0É444
[0É088
[0É142
[0É433
0É237
[0É482
[0É678**
[0É756**
[0É487
[0É334
0É084
0É048
[0É170
0É097
0É024
[0É102
0É268*
[0É038
[0É049
0É014
[0É051
0É028
[0É149
0É432**
0É145
[0É245
[0É254
[0É381**
[0É480**
[0É324**
[0É386**
[0É562**
[0É410**
[0É409**
0É133
0É340*
0É109
0É002
0É171
0É059
[0É138**
[0É026
[0É218
[0É490**
0É108
[0É624**
a ari, arietinum (check) ; ret, reticulatum ; ech, echinospermum ; jud, judaicum ; pin, pinnatiÐdum ; bij, bijugum.
Number of accessions in parenthesis.
* SigniÐcant at P\0É05 ; ** signiÐcant at P\0É05.
B Ocampo, L D Robertson, K B Singh
224
indication of genetic di†erences in biological pathways
among Cicer species. Nevertheless, except for C judaicum, all share a signiÐcant negative association between
protein content and harvest index. This association,
along with those of smaller magnitude between protein
content and seed weight or seed yield (both negative),
suggests that selection for desirable protein content
would also allow the selection of genotypes with high
biomass, low seed yield and low seed weight. This is
reported in most legume literature (PAG 1973).
It is acknowledged that evaluation of wild genetic
resources per se is only a preliminary step in the exploitation of wild relatives for the genetic improvement of
crops, because comprehensive estimation of the breeding value of wild accessions is possible only after their
introgression into cultivated genotypes. Genetic
reshuffling of diverse taxa, along with breeding procedures which enable breakage of undesirable linkages,
may produce agronomically suitable genotypes not
expected from parental performances. Introgression of
C echinospermum and C reticulatum genes into chickpea,
with the attainment of positive transgressive selections
for quantitative characters such as seed yield, biomass,
plant height and seed weight (Singh and Ocampo 1997),
supports this conclusion for the genus Cicer.
ACKNOWLEDGEMENT
The authors thank Mr Hani Nakkoul for providing
technical research assistance.
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