See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/273774776

Genetic variation of Citrus and related genera with ornamental potential

Article in Euphytica · March 2015

DOI: 10.1007/s10681-015-1423-2

CITATIONS READS

20 68,474

6 authors, including:

Alanna Santos Everton Hilo Souza

Universidade Federal do Recôncavo da Bahia Universidade Federal do Recôncavo da Bahia
2 PUBLICATIONS 22 CITATIONS 136 PUBLICATIONS 1,156 CITATIONS

SEE PROFILE SEE PROFILE

Fernanda Vidigal Souza Walter dos Santos Soares Filho

Brazilian Agricultural Research Corporation (EMBRAPA) Brazilian Agricultural Research Corporation (EMBRAPA)
92 PUBLICATIONS 1,016 CITATIONS 191 PUBLICATIONS 1,912 CITATIONS

SEE PROFILE SEE PROFILE

All content following this page was uploaded by Everton Hilo Souza on 26 March 2015.

The user has requested enhancement of the downloaded file.

Euphytica
DOI 10.1007/s10681-015-1423-2

Genetic variation of Citrus and related genera

with ornamental potential
Alanna Rachel Andrade dos Santos • Everton Hilo de Souza •

Fernanda Vidigal Duarte Souza • Michaella Fadini •

Eduardo Augusto Girardi • Walter dos Santos Soares Filho

Received: 13 January 2015 / Accepted: 11 March 2015

 Springer Science+Business Media Dordrecht 2015

Abstract The interest in Citrus and related genera as ‘Chinese box-orange’, besides accessions of the
ornamental plants has increased in recent years, genera Fortunella, Poncirus and Microcitrus. Among
motivating studies aimed at identifying genotypes, the accessions identified as having potential for use as
varieties and hybrids suitable for this purpose. The minifruit plants, the common ‘Sunki’ mandarin was
Citrus Active Germplasm Bank of the Embrapa the most suitable, and in the hedge category, ‘Chinese
Cassava & Fruits, a research unit of the Brazilian box-orange’ and ‘Trifoliate limeberry’ stood out. The
Agricultural Research Corporation—Embrapa, con- results obtained provide information to support citrus
tains more than 750 accessions with wide genetic breeding programs for ornamental purposes.
variability, and their utilization for ornamental pur-
poses is the objective of this study. For this purpose, Keywords Fruits  Floriculture  Genetic diversity 
we characterized 37 accessions with ornamental Morphological descriptors  Ornamental plants 
potential, classified in four categories for use in Pre-breeding
floriculture: potted plants, minifruit, hedges and
landscaping. Through the use of 39 quantitative and
Abbreviations
qualitative morphological descriptors, the following
CAGB Citrus active germplasm bank
accessions stood out for use landscaping and as potted
UPGMA Unweighted pair group method using an
plants: ‘Variegated’ calamondin, ‘Nasnaran’ mandar-
arithmetic average
in, ‘Chinotto’ orange, ‘Trifoliate limeberry’, ‘Papeda
Kalpi’, ‘Talamisan’ orange, ‘Wart Java’ lime, and

Introduction
A. R. A. dos Santos  M. Fadini
Federal University of Recôncavo of Bahia, Citrus L. and related genera belong to the family
Cruz Das Almas, Bahia, Brazil
Rutaceae and contain species with huge economic
E. H. de Souza  F. V. D. Souza  E. A. Girardi  value, the highlights being trees producing sweet
W. dos S. Soares Filho (&) oranges [C. sinensis (L.) Osbeck], besides lemons [C.
Embrapa Cassava & Fruits, Brazilian Agricultural limon (L.) Burm. f.], limes (various species), tan-
Research Corporation, Cruz Das Almas,
Bahia 44380-000, Brazil gerines and mandarins (various species) and grape-
e-mail: [email protected] fruits (C. paradisi Macfad.). In 2012, global
E. H. de Souza production of citrus fruits reached 131.3 million
e-mail: [email protected] metric tons (FAO 2015). The potential uses of citrus

123
 Euphytica

fruits, however, go beyond consumption of fresh fruit six citrus varieties and identified the ornamental
and juice, including raw materials such as essential potential of the Buddha’s hand citron [C. medica
oils for the production of medicines, pesticides, var. sarcodactylis (Hoola van Nooten) Swingle], so
fragrances and flavorings (Silva 1995; Bizzo 2009). named because its fruits are similar to a hand and have
Regarding the use of citrus plants for ornamental strong yellow color, as well as the ‘Cipó’ and
purposes, the first reports date to circa 1000 B.C. in ‘Imperial’ sweet oranges, because of their drooping
China (Donadio et al. 2005). Despite this long branches and variegated fruits and leaves.
heritage, the ornamental exploitation of citrus plants Likewise, the purpose of this study was to charac-
is still incipient and restricted to recommendations by terize the accessions of the Citrus Active Germplasm
a few landscape experts. In Europe in particular, a Bank of Embrapa Cassava & Fruits by means of
movement is starting to gain force in favor of quantitative and qualitative morphological descrip-
ornamental citriculture, not only for use of varieties tors, to identify genotypes with ornamental potential
described and cultivated in the past, but also to and to classify them in different use categories.
establish genetic improvement programs to develop Another objective was to generate information for
hybrids for this purpose, such as the efforts of research use in genetic improvement programs for develop-
institutions in Italy (Del Bosco 2003). ment of ornamental citrus varieties.
The Citrus Active Germplasm Bank (CAGB) of
Embrapa Cassava & Fruits, located in Cruz das
Almas, Bahia state, Brazil, contains more than 750 Materials and methods
accessions, making it highly representative in num-
ber of species and genera. It has potential for This study was conducted at the CAGB experimental
identification and generation of ornamental varieties, area, located at 128400 1900 south latitude and 398060 2200
considering the significant genetic variability of its west longitude, in the municipality of Cruz das Almas,
accessions. The study of this variability can support Bahia, Brazil.
genetic improvement programs to generate orna- According to the Köppen classification, the climate
mental hybrids. In this respect, the characterization in Cruz das Almas is a transition between the Am and
of the accessions preserved is an essential step to Aw zones, with average annual rainfall of 1143 mm,
identify the potential of this germplasm bank, average temperature of 24.28 C and relative humidity
because the data obtained from such studies will of 60.47 %. The soil of the experimental area is a
define the diversity of the accessions and determine typical dystrophic Yellow Latosol, A moderate, sandy
their potential for employment in different cate- clay loam texture, kaolinite, hypoferric, transition
gories of ornamental use, such as for potted plants, zone between subperennial and semideciduous rain-
minifruit, landscaping or hedges. forest, with slope of 0–3 %.
Similar studies have been conducted for charac- The CAGB is composed of at least two plants of
terization of fruit-bearing species and their classifica- each accession, which receive routine crop treatments.
tion in ornamental use categories with pineapple The rootstocks used are the ‘Rangpur’ lime (C.
(Ananas) (Souza et al. 2012a) and banana (Musa) limonia Osbeck), ‘Volkamer’ lemon (C. volkameriana
(Souza et al. 2012b), resulting in a rich database for Ten. & Pasq) and ‘Cleopatra’ mandarin (C. reshni
diverse applications as well as for genetic breeding, hort. ex Tanaka). The plants are grown with spacing of
refinement of knowledge on taxonomy and evolution 5 m 9 4 m or 6 m 9 4 m, in function of the vigor of
and conservation studies. the different accessions.
Investigation of the genetic resources available in We selected 37 accessions of citrus with ornamen-
the CAGB is important to generate new products to tal potential: ‘Nasnaran’ mandarin {C. amblycarpa
meet the needs of the market (Koehler-Santos et al. [(Hassk.) Ochse]}, ‘Galego Inerme Key’ lime [C.
2003). The most important traits involve the plant aurantiifolia (Christm.) Swingle], ‘Narrow Leaf’ sour
crown, leaves and fruits, where the major part of the orange (C. aurantium L.), ‘Bergamot’ orange (C.
available descriptors are concentrated. bergamia Risso & Poit.), ‘Taiwan’ mandarin (C.
Similar studies have been conducted by Mazzini depressa Hayata), ‘Mauritius papeda’ (C. hystrix
and Pio (2010), who characterized the morphology of DC.), C. hystrix hybrid, ‘Variegated’ true lemon (C.

123
Euphytica

limon), ‘Talamisan’ orange (C. longispina Wester), One desirable common feature of plants in this
‘Etrog’ citron (C. medica L.), ‘Variegated’ calamond- category is absence or low density of spines.
in (C. madurensis auct.), ‘Chinotto’ orange (C.
The data were submitted to analysis of variance and
myrtifolia Raf.), ‘Star Ruby’ grapefruit (C. paradisi
the means were compared by the Scott–Knott test at
Macfad.), ‘Cleopatra’ mandarin (C. reshni hort. ex
5 % probability, using the SAS statistical program
Tanaka), ‘Fairchild’ tangerine-tangelo [C. clementina
(SAS Institute 2010). The colors were compared with
hort. ex Tanaka 9 (C. paradisi 9 C. tangerina hort.
the color chart of the Royal Horticulture Society
ex Tanaka)], ‘Szincom’ mandarin (C. reticulata
(RHS). The relative contribution of each quantitative
Blanco), ‘Valencia Trepadeira’ sweet orange (C.
variable was calculated using the criterion of Singh
sinensis), ‘Variegated’ sweet orange (C. sinensis),
(1981) by the Genes program (Cruz 2006). Finally, the
‘Jaboti’ tangor (C. sinensis 9 C. unshiu Marcow.),
Gower algorithm (1971) was applied for joint analysis
common ‘Sunki’ mandarin [C. sunki (Hayata) hort. ex
qualitative and quantitative data by determining the
Tanaka], ‘Tachibana’ orange [C. tachibana (Makino)
genetic distance.
Tanaka], ‘Mency’ tangor (C. tangerina 9 C. sinen-
The hierarchical clusterings of the accessions were
sis), ‘Papeda Kalpi’ (C. webberi Wester var. montana
achieved by the UPGMA methods (unweighted pair
Wester), ‘Jindou’ kumquat [Fortunella hindsii
group method using an arithmetic average) based on
(Champ. ex Benth.) Swingle], Fortunella sp., ‘Chang-
the average Euclidean distance between all the
shou’ kumquat (F. xobovata hort. ex Tanaka); ‘Jindan’
accessions. The validation of the clusterings was
kumquat (F. xcrassifolia Swingle); ‘Wart Java’ lime
determined by the cophenetic correlation coefficient
(Citrus sp.), Microcitrus papuana Winters, ‘Benecke’
(r) (Sokal and Rohlf 1962).
trifoliate orange [Poncirus trifoliata (L.) Raf.], ‘Cole-
The statistical software system (R Development
man’ citrange (C. sinensis 9 P. trifoliata), ‘Flying
Core Team 2006) was used for the analyses of genetic
Dragon’ trifoliate orange (P. trifoliata), ‘Chinese box-
distance, hierarchical clusterings and cophenetic cor-
orange’ (Severinia buxifolia [(Poir.) Ten.], ‘Limeber-
relation. The cophenetic correlation was calculated by
ry’ {Triphasia trifolia [(Burm. f.) P. Wilson]}, ‘Cravo’
the t and Mantel tests (10,000 permutations). The
mandarin (C. reticulata), ‘Citros Processo’ (Citrus
dendrogram was generated based on the distance
sp.), and ‘Jerônimo’ lime (Citrus sp.).
matrix by the MEGA 4 software system (Tamura et al.
We applied 39 descriptors, 10 of them quantitative
2007).
and 29 qualitative (IPGRI 1999). Among the quanti-
tative descriptors, three were related to traits of the
plants, four to leaf traits and three to fruit traits. Of the
Results and discussion
qualitative descriptors, five were related to attributes
of the plants, nine to the leaves, five to the flowers and
From applying the morphological descriptors utilized
ten to the fruits. The definition of each ornamental
it was possible to characterize the accessions with
category for classification of the accessions was based
ornamental potential, besides classify them in the use
on the following characteristics:
categories. The variability found was probably due to
• Potted plants Plant height below 170 cm, crown the great diversity among individuals in the CAGB
diameter smaller than 150 cm, moderate or dense regarding size, color and shape of the leaves (Fig. 1),
branching, preferably with few or no spines. fruits (Fig. 2) and flowers (Fig. 3). The evaluation of
Accessions with larger height and crown diameter the relative importance of the 10 quantitative descrip-
could be considered, if associated with dwarf tors in judging the variability among the accessions
rootstock or plants manageable by topiary to keep was carried out by the method of Singh (1981). The
them small. crown diameter descriptor contributed 68.93 % of the
• Minifruits plants Fruit diameter (or length for morphological divergence between individuals, fol-
elongated fruits) varying from 2.5 cm to 4.5 cm. lowed by plant height, which accounted for 30.92 %.
• Hedges plants Dense branching. These results show that these two variables are
• Landscaping plants Broad category, possibly responsible for a significant part of the phenotypical
including potted plants, minifruit and hedges. variability identified (Table 1).

123
 Euphytica

Fig. 1 Morphological variability of leaves of 37 accessions of tangor (C. sinensis 9 C. unshiu), t common ‘Sunki’ mandarin
Citrus L. and related genera. a ‘Nasnaran’ mandarin (C. (C. sunki), u ‘Tachibana’ orange (C. tachibana), v ‘Mency’
amblycarpa), b ‘Galego Inerme Key’ lime (C. aurantiifolia), tangor (C. tangerina 9 C. sinensis), w ‘Papeda Kalpi’ (C.
c ‘Narrow Leaf’ sour orange (C. aurantium), d ‘Bergamot’ webberi var. montana), x ‘Jindou’ kumquat (Fortunella hindsii),
orange (C. bergamia), e ‘Taiwan’ mandarin (C. depressa), y Fortunella sp., z ‘Changshou’ kumquat (F. xobovata), aa
f ‘Mauritius papeda’ (C. hystrix), g C. hystrix hybrid, ‘Jindan’ kumquat (F. xcrassifolia), ab ‘Wart Java’ lime (Citrus
h ‘Variegated’ true lemon (C. limon), i ‘Talamisan’ orange sp.), ac Microcitrus papuana, ad ‘Benecke’ trifoliate orange
(C. longispina), j ‘Etrog’ citron (C. medica), k ‘Variegated’ (Poncirus trifoliata), ae ‘Coleman’ citrange (C. sinensis 9 P.
calamondin (C. madurensis), l ‘Chinotto’ orange (C. myrtifolia), trifoliata), af ‘Flying Dragon’ trifoliate orange (P. trifoliata), ag
m ‘Star Ruby’ grapefruit (C. paradisi), n ‘Cleopatra’ mandarin ‘Chinese box-orange’ (Severinia buxifolia), ah ‘Limeberry’
(C. reshni), o ‘Fairchild’ tangerine-tangelo [C. clementi- (Triphasia trifolia), ai ‘Cravo’ mandarin (C. reticulata), aj
na 9 (C. paradisi 9 C. tangerina)], p ‘Szincom’ mandarin ‘Citros Processo’ (Citrus sp.), ak ‘Jerônimo’ lime (Citrus sp.).
(C. reticulata), q ‘Valencia Trepadeira’ sweet orange (C. Bars 5 cm
sinensis)\, r ‘Variegated’ sweet orange (C. sinensis), s ‘Jaboti’

The joint analysis of the qualitative and quantitative well as the elements of the simplified matrix
data of the 37 accessions evaluated led to the obtained by the grouping method. Values near one
formation of eight groups (Fig. 4) by UPGMA based indicate better graphical representation (Rohlf and
in the pairwise Euclidean distance between all the Fisher 1968). According to the results, there was a
accessions, using the genetic dissimilarity (D good fit between the graphical representation of the
dg = 0.4) as the cutoff point. Euclidean distances and the original matrix. In a
The dendrogram generated presented cophenetic similar study with pineapple, Souza et al. (2012a)
correlation coefficient of r = 0.70 (P \ 0.0001, found a relatively high cophenetic correlation coef-
10,000 permutations). This coefficient permits ficient (r = 0.81), a value considered good when
assessing the consistency of the grouping pattern dealing with quantitative and qualitative morpho-
between the elements of the dissimilarity matrix as logical data.

123
Euphytica

Fig. 2 Morphological variability of fruits of 37 accessions of tangor (C. sinensis 9 C. unshiu), t common ‘Sunki’ mandarin
Citrus L. and related genera. a ‘Nasnaran’ mandarin (C. (C. sunki), u ‘Tachibana’ orange (C. tachibana), v ‘Mency’
amblycarpa), b ‘Galego Inerme Key’ lime (C. aurantiifolia), tangor (C. tangerina 9 C. sinensis), w ‘Papeda Kalpi’ (C.
c ‘Narrow Leaf’ sour orange (C. aurantium), d ‘Bergamot’ webberi var. montana), x ‘Jindou’ kumquat (Fortunella hindsii),
orange (C. bergamia), e ‘Taiwan’ mandarin (C. depressa), y Fortunella sp., z ‘Changshou’ kumquat (F. xobovata), aa
f ‘Mauritius papeda’ (C. hystrix), g C. hystrix hybrid, ‘Jindan’ kumquat (F. xcrassifolia), ab ‘Wart Java’ lime (Citrus
h ‘Variegated’ true lemon (C. limon), i ‘Talamisan’ orange sp.), ac Microcitrus papuana, ad ‘Benecke’ trifoliate orange
(C. longispina), j ‘Etrog’ citron (C. medica), k ‘Variegated’ (Poncirus trifoliata), ae ‘Coleman’ citrange (C. sinensis 9 P.
calamondin (C. madurensis), l ‘Chinotto’ orange (C. myrtifolia), trifoliata), af ‘Flying Dragon’ trifoliate orange (P. trifoliata), ag
m ‘Star Ruby’ grapefruit (C. paradisi), n ‘Cleopatra’ mandarin ‘Chinese box-orange’ (Severinia buxifolia), ah ‘Limeberry’
(C. reshni), o ‘Fairchild’ tangerine-tangelo [C. clementi- (Triphasia trifolia), ai ‘Cravo’ mandarin (C. reticulata), aj
na 9 (C. paradisi 9 C. tangerina)], p ‘Szincom’ mandarin ‘Citros Processo’ (Citrus sp.), ak ‘Jerônimo’ lime (Citrus sp.).
(C. reticulata), q ‘Valencia Trepadeira’ sweet orange (C. Bars 5 cm
sinensis), r ‘Variegated’ sweet orange (C. sinensis), s ‘Jaboti’

Group G1 is composed of only one accession, M. ornamental qualities as well as to generate rootstocks,
papuana, which originates from tropical Asia (USDA given the high drought tolerance of the genus
2014) and has several attractive characteristics from Microcitrus (Swingle) (Swingle 1967).
the ornamental standpoint. Its small size and dense Group G2 is formed of two well-defined subgroups,
ellipsoidal crown (Table 2) make this species highly the first composed of the ‘Benecke’ and ‘Flying
recommended for the potted plant and landscaping Dragon’ trifoliate oranges and the ‘Coleman’ citrange.
categories. Its high branch density and presence of Varieties of P. trifoliataare widely distributed in
spines allows its use to form hedges and its small northern and central China (USDA 2014). The trees
elongated fruits (Tables 3, 4; Fig. 5a) are attractive are small to medium in size, with long spines
and decorative. Probably the distinctive morpho- (Table 2). Their leaves are trifoliated (Fig. 1ad, af)
logical traits of the fruits and leaves were decisive and their fruits (Fig. 2ad, af) have a papillate texture
for this accession to be alone in this group. M. papuana and are bright yellow when ripe, besides being highly
has been successfully employed by the Citrus Genetic aromatic, an important characteristic of ornamental
Improvement Program of Embrapa Cassava & Fruits plants. The flowering of Poncirus Raf. is abundant and
as a parental in crosses aiming to obtain plants with its flowers and spines are large (Table 5; Figs. 3q, s,

123
 Euphytica

Fig. 3 Morphological variability of flowers of 21 accessions of orange (C. sinensis), l ‘Papeda Kalpi’ (C. webberi var.
Citrus L. and related genera. a ‘Nasnaran’ mandarin (C. montana), m ‘Jindou’ kumquat (Fortunella hindsii), n Fortunel-
amblycarpa), b ‘Galego Inerme Key’ lime (C. aurantiifolia), la sp., o ‘Changshou’ kumquat (F. xobovata), p ‘Jindan’
c ‘Taiwan’ mandarin (C. depressa), d ‘Mauritius papeda’ (C. kumquat (F. xcrassifolia), q ‘Benecke’ trifoliate orange
hystrix), e C. hystrix hybrid, f ‘Variegated’ true lemon (C. (Poncirus trifoliata), r ‘Coleman’ citrange (C. sinensis 9 P.
limon), g ‘Talamisan’ orange (C. longispina), h ‘Etrog’ citron trifoliata), s ‘Flying Dragon’ trifoliate orange (P. trifoliata),
(C. medica), i ‘Variegated’ calamondin (C. madurensis), j ‘Star t ‘Chinese box-orange’ (Severinia buxifolia), u ‘Limeberry’
Ruby’ grapefruit (C. paradisi), k ‘Valencia Trepadeira’ sweet (Triphasia trifolia). Bars 5 cm

Table 1 Relative contribution (%) of quantitative descriptors 5b), favoring use in landscaping and as hedges of for
to the morphological variability of 37 accessions of Citrus L., production of minifruit plants.
related genera, based on the criterion of Singh (1981) and The ‘Coleman’ citrange has very similar traits to
Mahalanobis distance
those of the Poncirus accessions, which compose its
Descriptors S.j S.j1 (%) group (‘Benecke’ and ‘Flying Dragon’) and can also
Crown diameter 19,068,161.3 68.93
be recommended in the potted plant category.
Plant height 8,553,852.5 30.92
Also in this group, the accessions ‘Wart Java’ lime,
Leaf length 9283.8 0.03
‘Valencia Trepadeira’ sweet orange and ‘Talamisan’
orange form a second grouping. According to the
Trunk diameter 8506.3 0.03
system of Tanaka (1961), C. sinensis and C. long-
Fruit length 6271.4 0.02
ispina originated in Asia and are part of the subgenus
Fruit diameter 5957.8 0.02
Archicitrus. Due to the presence of highly dense
Leaf width 3527.7 0.01
crowns and uniform branching, the ‘Talamisan’
Phyllode length 2963.7 0.01
orange and ‘Wart Java’ lime are recommended as
Number of fruits per bunch 2781.9 0.01
potted plants and for landscaping (Fig. 5c). The ‘Wart
Phyllode width 1257.7 0.01
Java’ lime is also suitable for producing small fruits,
S.j = contribution of the variable x for the value of the because they have a rough peel and light yellow color
Euclidean distance between genotypes i and j when ripe (Fig. 2ab; Table 4).

123
Euphytica

Fig. 4 Genetic dissimilarity dendrogram for 37 accessions of Citrus L. and related genera, obtained by the UPGMA (unweighted pair
group method using arithmetic average) based on the Gower algorithm, for 39 qualitative andquantitative traits

The ‘Valencia Trepadeira’ sweet orange is an the ‘Cipó’ sweet orange, a synonym of ‘Valencia
accession of Asian origin (USDA 2014) and although Trepadeira’, also finding it to have the same recom-
it produces relatively large leaves (Fig. 1q) and fruits mended uses as found here.
(Fig. 2q) among sweet orange varieties (Table 4), it Group G3 is composed of only two accessions, the
has an ovoid crown, with drooping branches, which ‘Variegated’ sweet orange (Fig. 5e, f) and ‘Variegat-
can be supported on lattices to form pergolas, making ed’ true lemon (Fig. 5g, h). These accessions, whose
it recommended for landscaping (Fig. 5d). Besides species belong to the subgenus Archictrus (Lanjouw
this, its flowering is intense, with large flowers and 1961; Tanaka 1961), are very similar and can be easily
pinkish floral buds (Fig. 3k). It is also recommended confused. They are medium-sized erect plants with
as a parental to form hybrids because of its small size. ellipsoid crown (Table 2). They have great ornamental
In a similar study, Mazzini and Pio (2010) evaluated potential and can be managed through pruning or

123
 Euphytica

Table 2 Quantitative and qualitative plant traits in 37 accessions from the Citrus Active Germplasm Bank of Embrapa Cassava &
Fruits with ornamental potential
Name of the accession PLH TRD CRD CRS DBR SPD SPL SPS

‘Nasnaran’ mandarin 175.00 d 5.90 d 160.00 e OVO DEN SPA B5 mm STR

‘Galego Inerme Key’ lime 330.00 a 11.20 b 540.00 a OVO DEN MED B5 mm STR
‘Narrow Leaf’ sour orange 354.00 a 10.20 c 335.00 c ELI MED ABS ABS ABS
‘Bergamot’ orange 335.00 a 9.90 c 245.00 d ELI MED ABS ABS ABS
‘Taiwan’ mandarin 315.00 b 10.75 c 475.00 b ELI DEN ABS ABS ABS
‘Mauritius papeda’ 283.00 b 9.60 c 290.00 c OVO DEN MED B5 mm STR
C. hystrix hibrid 215.00 c 7.50 d 225.00 d SPH DEN MED 6–15 mm STR
‘Variegated’ true lemon 250.00 c 7.50 d 200.00 d ELI SPA SPA 6–15 mm STR
‘Talamisan’ orange 110.00 d 6.70 d 155.00 e ELI DEN SPA 6–15 mm STR
‘Etrog’ citron 210.00 c 10.00 c 330.00 c OVO SPA HIG 16–40 mm STR
‘Variegated’ calamondin 115.00 d 3.65 f 120.00 e SPH MED ABS ABS ABS
‘Chinotto’ orange 190.00 c 6.20 d 160.00 e OVO SPA ABS ABS ABS
‘Star Ruby’ grapefruit 220.00 c 9.00 c 246.00 d SPH DEN SPA 6–15 mm STR
‘Cleopatra’ mandarin 365.00 a 11.70 b 465.00 b ELI MED ABS ABS ABS
‘Fairchild’ tangerine-tangelo 297.50 b 9.30 c 360.00 c OVO MED ABS ABS ABS
‘Szincom’ mandarin 290.00 b 9.60 c 347.50 c SPH DEN ABS ABS ABS
‘Valencia Trepadeira’ sweet orange 140.00 d 8.85 c 260.00 d OVO MED SPA 6–15 mm STR
‘Variegated’ sweet orange 215.00 c 6.50 d 155.00 e ELI MED ABS ABS ABS
‘Jaboti’ tangor 336.00 a 10.40 c 415.00 b SPH DEN ABS ABS ABS
Common ‘Sunki’ mandarin 375.00 a 11.15 b 445.00 b SPH DEN ABS ABS ABS
‘Tachibana’ orange 365.00 a 9.75 c 375.00 c OVO DEN ABS ABS ABS
‘Mency’ tangor 328.00 a 9.30 c 380.00 c SPH MED SPA 16–40 mm STR
‘Papeda Kalpi’ 190.00 c 7.00 d 250.00 d OVO DEN ABS ABS ABS
‘Jindou’ kumquat 160.00 d 3.20 f 108.00 e ELI MED MED 6–15 mm STR
Fortunella sp. 235.00 c 6.65 d 140.00 e ELI MED SPA 6–15 mm STR
‘Changshou’ kumquat 220.00 c 7.70 d 143.33 e ELI MED ABS ABS ABS
‘Jindan’ kumquat 245.00 c 8.10 d 163.00 e ELI SPA ABS ABS ABS
‘Wart Java’ lime 170.00 d 5.10 e 150.00 e SPH MED SPA B5 mm STR
Microcitrus papuana 140.00 d 3.05 f 85.00 e ELI DEN HIG 6–15 mm STR
‘Benecke’ trifoliate orange 245.00 c 5.40 e 185.00 e ELI MED HIG [40 mm STR
‘Coleman’ citrange 266.00 b 6.90 d 213.00 d ELI MED HIG 16–40 mm STR
‘Flying Dragon’ trifoliate orange 223.00 c 5.90 d 115.00 e ELI MED HIG 16–40 mm CUR
‘Chinese box-orange’ 210.00 c 8.15 d 180.00 e SPH DEN HIG 16–40 mm STR
‘Limeberry’ 170.00 d 5.15 e 205.00 d SPH DEN MED 6–15 mm STR
‘Cravo’ mandarin 362.50 a 13.05 a 390.00 c SPH DEN ABS ABS ABS
‘Citros Processo’ 380.00 a 12.40 a 350.00 c ELI MED SPA 6–15 mm STR
‘Jerônimo’ lime 160.00 d 6.60 d 245.00 d OVO SPA SPA 6–15 mm STR
Averages followed by the same letter do not differ by the Scott–Knott test at 5 % probability
PLH plant height (cm), TRD trunk diameter (cm), CRD crown diameter (cm), CRS crown shape, DBR density of branches, SPD spine
density, SPL spine length, SPS spine shape, OVO ovoid, ELI ellipsoid, SPH spheroid, DEN dense, MED medium, SCA sparse, ABS
absent, HIG high, STR straight, CUR curved

123
 Table 3 Quantitative and qualitative leaf traits in 37 accessions from the Citrus Active Germplasm Bank of Embrapa Cassava & Fruits with ornamental potential
Name of the accession LFL LFW LFD LVA LCO LLI LLS LLM LAP PHY PHL PHW PHS
Euphytica

‘Nasnaran’ mandarin 7.41 d 3.45 d SIM ABS DAR (Fan3-147a) SES OVA SIM ATT PRE 1.43 f 0.33 e OBO
‘Galego Inerme Key’ lime 9.12 c 4.49 d SIM ABS LIG (Fan3-143b) SES OVA SIM ATT PRE 1.09 h 0.36 e OBD
‘Narrow Leaf’ sour orange 13.17 a 2.59 e SIM ABS DAR (Fan3-N137a) LON LAN SMO ACU PRE 3.12 c 0.35 e OBD
‘Bergamot’ orange 9.13 c 6.18 b SIM ABS MED (Fan3-146b) SES ORB SMO ROU ABS ABS ABS ABS
‘Taiwan’ mandarin 7.51 d 3.61 d SIM ABS DAR (Fan3-N137c) SES OVA SIM ATT ABS ABS ABS ABS
‘Mauritius papeda’ 9.38 c 4.05 d SIM ABS LIG (Fan3-137a) LON OVA SIM ATT PRE 4.52 b 3.51 b OBD
C. hystrix hibrid 10.81 b 4.35 d SIM ABS DAR (Fan3-N137b) LON ELP SIM ATT PRE 5.01 a 3.87 a OBO
‘Variegated’ true lemon 9.75 c 5.81 b SIM PRE VAR SES ELP CRE ATT ABS ABS ABS ABS
‘Talamisan’ orange 8.80 c 4.06 d SIM ABS DAR (Fan3-137b) BRE ELP SMO ATT PRE 2.41 d 1.19 d OBO
‘Etrog’ citron 13.21 a 4.15 d SIM ABS LIG (Fan3-N137a) SES ELP SIM ATT ABS ABS ABS ABS
‘Variegated’ calamondin 5.71 d 2.74 e SIM PRE VAR SES OVA SMO ATT ABS ABS ABS ABS
‘Chinotto’ orange 3.24 e 1.36 f SIM ABS DAR (Fan3-147a) SES OVA SMO ATT ABS ABS ABS ABS
‘Star Ruby’ grapefruit 9.20 c 6.20 b SIM ABS DAR (Fan3-135a) BRE OBO CRE ATT PRE 1.20 g 1.00 d OBD
‘Cleopatra’ mandarin 7.97 c 3.72 d SIM ABS DAR (Fan3-N137c) SES ELP SIM ATT ABS ABS ABS ABS
‘Fairchild’ tangerine-tangelo 9.08 a 3.33 d SIM ABS MED (Fan3-146a) BRE ELP SIM ATT PRE 1.85 e 0.33 e OBO
‘Szincom’ mandarin 8.26 c 2.51 e SIM ABS DAR (Fan3-N137d) SES LAN CRE ACU ABS ABS ABS ABS
‘Valencia Trepadeira’ sweet orange 11.03 a 5.74 b SIM ABS MED (Fan3-N147b) BRE OVA SIM ATT PRE 2.27 d 0.98 d OBC
‘Variegated’ sweet orange 9.56 b 5.03 c SIM PRE VAR BRE ELP CRE ATT PRE 1.35 g 0.45 e OBC
‘Jaboti’ tangor 8.64 b 3.49 d SIM ABS DAR (Fan3-N137c) BRE ELP SIM ATT ABS ABS ABS ABS
Common ‘Sunki’ mandarin 6.34 b 3.39 c SIM ABS DAR (Fan3-N137c) SES ELP SIM ATT ABS ABS ABS ABS
‘Tachibana’ orange 6.26 c 3.16 c SIM ABS MED (Fan3-137c) SES ELP SIM ROU ABS ABS ABS ABS
‘Mency’ tangor 7.06 c 3.31 e SIM ABS DAR (Fan3-N137b) SES OVA SIM ACU ABS ABS ABS ABS
‘Papeda Kalpi’ 11.77 a 4.29 d SIM ABS DAR (Fan3-139a) LON OVA CRE ATT PRE 5.17 a 3.19 c OBD
‘Jindou’ kumquat 5.00 d 2.30 e SIM ABS LIG (Fan3-N144a) SES ELP SMO ACU ABS ABS ABS ABS
Fortunella sp. 8.28 c 2.88 e SIM ABS MED (Fan3-138a) SES ELP CRE ACM ABS ABS ABS ABS
‘Changshou’ kumquat 6.78 d 4.13 d SIM ABS MED (Fan3-137d) SES OVA CRE ROU ABS ABS ABS ABS
‘Jindan’ kumquat 8.42 c 3.10 e SIM ABS MED (Fan3-137d) SES ELP CRE ATT ABS ABS ABS ABS
‘Wart Java’ lime 6.30 d 2.79 e SIM ABS MED (Fan3-138a) SES ELP CRE ATT PRE 1.57 f 0.42 e OBO
Microcitrus papuana 2.28 e 0.96 f SIM ABS MED (Fan3-138a) SES OVA CRE ATT ABS ABS ABS ABS
‘Benecke’ trifoliate orange 7.31 d 6.78 b TRI ABS LIG (Fan3-144a) LON OBO CRE ROU PRE 2.32 d 0.45 e OBO
‘Coleman’ citrange 9.57 c 8.73 a TRI ABS LIG (Fan3-N143b) BRE OBO CRE ATT PRE 1.50 f 0.42 e OBO
‘Flying Dragon’ trifoliate orange 6.66 d 6.27 b TRI ABS LIG (Fan3-143a) LON OBO CRE ROU PRE 2.09 e 0.39 e OBD

123
 Euphytica

Averages followed by the same letter do not differ by the Scott–Knott test at 5 % probability. Colors compared with the Color Chart of the Royal Horticulture Society (RHS)

LAP leaf apex, PHY phyllode, PHL phyllode length (cm), PHW phyllode width (cm), PHS phyllode shape, SIM simple, TRI trifoliate, ABS absent, PRE present, LIG light, MED
LFL leaf length (cm), LFW leaf width (cm), LFD leaf division, LVA leaf variegation, LCO leaf color, LLI leaf lamina insertion, LLS leaf lamina shape, LLM leaf lamina margin,

medium, DAR dark, VAR variegated, SES sessile, BRE brevipetiolate, LON longipetiolate, ELP elliptic, OBO obovate, LAN lanceolate, OVA ovate, ORB orbicular, SIN sinuate,
topiary, for use in pots or for landscaping. Their leaves

ABS
ABS
ABS
ABS
ABS
PHS
have varied colors, with green and white or light cream
shades and elliptical shape (Fig. 1h, r; Table 3). The
PHW

ABS
ABS
ABS
ABS
ABS
fruits also have varied color, from yellow to dark green
(Fig. 2h, r). They have the medium size of the
common sweet orange, but the plant can be classified
ABS
ABS
ABS
ABS
ABS
PHL

in the minifruit ornamental category because of the

CRE crenate, SMO smooth, DEN dentate, ATT attenuate, ACU acute, ROU rounded, EMA emarginate, ACM acuminate, OBD obdeltate, OBC obcordate
fruits appealing appearance when unripe. Probably the
morphological traits of coloration and leaf shape were
PHY

ABS
ABS
ABS
ABS
ABS

decisive in these two accessions isolation in this group.

The decorative value of the ‘Variegated’ sweet
ATT
ATT
ATT
ATT
ATT
LAP

orange and ‘Variegated’ true lemon can be significant-

ly enhanced by using dwarf rootstocks, a strategy that
can also be applied to the other accessions evaluated.
LLM

DEN

DEN
SIM
SIM
SIM

Group G4 contains C. hystrix, along with a hybrid

of this species and the ‘Galego Inerme Key’ lime.
According to Tanaka (1961), these species belong to
LLS

ELP
ELP
ELP
ELP
ELP

the subgenus Archicitrus. The ‘Galego Inerme Key’

lime is recommended for use in landscaping and in
SES
SES
SES
SES
SES
LLI

crosses aimed at producing ornamental hybrids, since

this accession of totally free of spines (Fig. 5i).
The species C. hystrix is native to temperate and
MED (Fan3-146b)
MED (Fan3-137d)
LIG (Fan3-144a)
LIG (Fan3-143a)
LIG (Fan3-143a)

tropical Asia (USDA 2014). It has a dense crown with

branches starting near the base (Fig. 5j). Its leaves are
dark green and longipetiolate, with large phyllodes,
composing up to 50 % of their size (Fig. 1f). The fruits
LCO

are aromatic, green and highly attractive from the

ornamental viewpoint due to their rough peels
LVA

ABS
ABS
ABS
ABS
ABS

(Fig. 2f; Table 4). This accession is recommended

for minifruit and landscaping plants.
According to Swingle (1967), C. hystrix is naturally
LFD

SIM

SIM
SIM
SIM
TRI

hybridized with other species of the Citrus genus, and

some of these hybrid varieties being included among
3.96 d
3.85 d
4.17 d
5.16 c
1.81 f
LFW

the different forms described by Wester in the period

between 1913 and 1915. This can explain the origin of
the C. hystrix hybrid evaluated in this study, whose
10.24 b
4.40 d
3.62 e
8.28 c
6.67 c

characteristics of size and foliage (Fig. 1g) are very

LFL

similar to those of other C. hystrix varieties and is

suitable for landscaping.
Three accessions formed Group G5: ‘Limeberry’,
‘Chinese box-orange’ and ‘Chinotto’ orange. The first
is small, with dense branching (Table 2) and elliptical
trifoliated leaves (Fig. 1ah; Table 3). The flowers are
Name of the accession

‘Chinese box-orange’

small and white and have three petals (Table 5;

Table 3 continued

‘Cravo’ mandarin
‘Citros Processo’

Fig. 3u). Its fruits are small and abundant, with dark
‘Jerônimo’ lime

green color (Fig. 2ah; Table 4), a trait that contrasts

‘Limeberry’

with the leaf color, giving it good ornamental potential

(Fig. 5k). The ‘Limeberry’ probably originated in
Asia (USDA 2014), and it is widely cultivated in

123
Euphytica

tropical and subtropical regions as an ornamental and ripe. They are widely cultivated in Japan and China
hedge plant. The observations in this study corroborate along with other subtropical regions (Swingle 1967).
the indications by Swingle (1967) for this accession, Group G7 is formed of 17 accessions, of them 12
which can be used as a potted plant, in landscaping and species and hybrids in the tangerine or micro-tanger-
to form hedges. ine category. Tangerines and mandarins trees fall in an
S. buxifolia, commonly called the ‘Chinese box- extensive and diversified group, containing different
orange’ or boxthorn, is native to tropical and temper- species and varieties that often have sharp distinctions,
ate Asia (USDA 2014). It has medium size and a dense making it hard to list traits common to all of them. In
crown (Table 2; Fig. 5l, m) with high density of leaves general, they produce small flowers and medium-sized
and spines (Fig. 1ag) and small fruits (Fig. 2ag) and fruits with orange color that are easy to peel (Hodgson
flowers (Fig. 3t). The fruits, which resemble berries, 1967; Saunt 1990).
are black when ripe and abundant. This accession can These results are in accordance with the findings of
be used as a potted plant or for landscaping. Nicolosi et al. (2000), who studied the phylogenetic
C. myrtifolia, also known as the ‘Chinotto’ orange aspects of accessions of Citrus and related genera
(Hodgson 1967), is small and without spines based on RAPD and SCAR markers, finding consid-
(Table 2), with branches completely covered by small, erable genetic similarity among tangerine accessions.
shiny, dark green leaves (Table 3). The coloration of A similar result was obtained by Bastianel et al.
its abundant fruits ranges from dark yellow to orange, (2001), who grouped tangerine and sour orange
making this species recommended for ornamental use species in the same group, like in this study.
in pots and landscaping (Fig. 5n). It is cultivated in The ‘Cravo’ mandarin tree is probably native to Asia
Italy as a decorative plant (Saunt 1990; USDA 2014). (USDA 2014). It is tall, without spines, with dense
It can also be recommended in the minifruit category. spheroid crown (Table 2) and produces medium-sized
In this study, we evaluated four species of For- fruits with slightly rough surface and deep orange color
tunella (Swingle), or kumquat, all of them in Group when ripe (Fig. 2ai; Table 4). Because of its size, it is
G6: F. hindsii, known as the ‘Jindou’ kumquat only recommended for landscaping (Fig. 5r), but is an
(Fig. 5o), F. xobovata, also called the ‘Changchou’ interesting candidate for genetic alteration with parentals
kumquat (Fig. 5p), Fortunella sp. and F.xcrassifolia, to reduce its stature, as has been achieved with
popularly known as the ‘Jindan’ kumquat (Fig. 5q). Fortunella, Poncirus and Microcitrus. The size of the
The data found for the ‘Jindou’ kumquat coincide hybrids obtained could be reduced even more by using
with the descriptions of Swingle (1967) and Saunt dwarf rootstock varieties. Another C. reticulate accession
(1990), who stated that the plants of this species are is the ‘Szincom’ mandarin, which has similar character-
small with thin branches, differing from other species istics to the ‘Cravo’ variety and the same potential use.
of the genus, which are much larger. This accession The ‘Sunki’ mandarin tree is widely grown in
produces small, bright orange colored fruits and has temperate Asia (USDA 2014) and produces fruits
strong ornamental potential (Fig. 2x; Table 4). The classified as micro-tangerines (Fig. 5s, t). According
use of this species for ornamental landscaping was to Araújo and Salibe (2002), this term refers to species
mentioned by Saunt (1990), and we can recommend it or varieties of Citrus that have small leaves, flowers
as a potted and/or minifruit plant as well. and (generally sour) fruits. As an adult, it reaches up to
The other three Fortunella accessions analyzed are 4 meters (Table 2), with a dense spheroid crown and
very similar to each other and are recommended for no spines. Its leaves are small and dark green (Fig. 1t;
use in the same categories mentioned above. The Table 3) and it yields plentiful fruit for most of the
Changchou stands out for its pyriform fruits, which are year. These micro-tangerines are oblate, with few
quite different from the other kumquat species. These seeds and have deep orange peels when ripe (Fig. 2t).
small fruits can also be used in decorative arrange- Despite its tall size, the ‘Sunki’ mandarin tree is
ments (Fig. 2z; Table 4). widely used for ornamental purposes due to the sharp
Species of the Fortunella genus all produce small contrast between its fruits and foliage. It can be used
and abundant orange-colored fruits that are highly for landscaping of large open areas, although its best
aromatic. The peel is fleshy and edible when the fruit is use is for production of small fruits. At the Citrus

123
 Table 4 Quantitative and qualitative fruit traits in 37 accessions from the Citrus Active Germplasm Bank of Embrapa Cassava & Fruits with ornamental potential
Name of the accession FRL FRD FRS FSB FSA FRV IFC RFC FST ALC PUC NFB AFB

123
‘Nasnaran’ mandarin 2.58 h 3.19 e OBL TRU TRU ABS GRE YEL RGH WHI YEL 1.45 d 2–4
‘Galego Inerme Key’ lime 3.46 g 3.94 d SPH ROU CON ABS GRE LYE SMO WHI GRE 1.80 d 2–4
‘Narrow Leaf’ sour orange 7.14 c 7.41 b SPH ROU CON ABS GRE YEL RGH WHI YEL 1.40 d 2–4
‘Bergamot’ orange 6.38 d 7.69 b OBL TRU TRU ABS GRE DYE RGH WHI YEL 1.30 d 2–4
‘Taiwan’ mandarin 2.75 h 3.90 d OBL TRU TRU ABS GRE ORA SMO WHI ORA 3.45 b 4–6
‘Mauritius papeda’ 3.91 g 4.25 d PYR CON NEC ABS GRE GRE RGH WHI GRE 2.25 c 2–4
C. hystrix hibrid 8.80 a 5.53 b PYR CON NEC ABS GRE GRE SMO WHI GRE 1.00 d 2–4
‘Variegated’ true lemon 6.36 d 5.82 c SPH MAM CON PRE VAR YEL RGH WHI YEL 1.20 d 2–4
‘Talamisan’ orange 5.50 e 5.35 c SPH ROU CON ABS GRE YEL RGH WHI YEL 1.25 d ?6
‘Etrog’ citron 12.48 c 8.95 b OVO ACU CON ABS GRY YEL RGH WHI YEL 1.00 d 2–4
‘Variegated’ calamondin 2.91 h 2.89 e SPH ROU CON PRE VAR YEL SMO ORA ORA 1.25 d 2–4
‘Chinotto’ orange 4.93 f 5.63 c SPH TRU TRU ABS GRE DYE SMO WHI YEL 2.30 c 2–4
‘Star Ruby’ grapefruit 9.10 b 9.80 a SPH ROU TRU ABS GRY YEL SMO PIN RED 1.40 d 2–4
‘Cleopatra’ mandarin 3.73 g 4.00 d OBL TRU TRU ABS GRE ORA SMO WHI ORA 3.65 b 4–6
‘Fairchild’ tangerine-tangelo 5.30 e 6.10 c SPH TRU TRU ABS GRE ORA SMO YEL ORA 1.20 d 2–4
‘Szincom’ mandarin 3.67 g 3.88 d SPH TRU CON ABS GRE LOR SMO WHI YEL 1.35 d 2–4
‘Valencia Trepadeira’ sweet orange 6.64 d 7.26 b SPH ROU TRU ABS GRE YEL SMO WHI YEL 1.85 d 2–4
‘Variegated’ sweet orange 6.41 d 6.40 c SPH ROU CON PRE VAR YEL RGH WHI YEL 1.20 d 2–4
‘Jaboti’ tangor 4.63 f 6.27 c OBL TRU TRU ABS GRY ORA SMO WHI YEL 1.30 d 2–4
Common ‘Sunki’ mandarin 3.35 g 4.20 d OBL OUT TRU ABS GRE ORA SMO ORA ORA 9.55 a ?6
‘Tachibana’ orange 3.33 g 3.23 e OBL TRU TRU ABS GRE LYE SMO WHI YEL 1.35 d 2–4
‘Mency’ tangor 4.28 f 4.33 d OBL TRU TRU ABS GRE ORA SMO WHI YEL 1.30 d 2–4
‘Papeda Kalpi’ 6.76 d 7.90 b PYR ROU NEC ABS GRE GRE SMO WHI GRE 1.20 d 2–4
‘Jindou’ kumquat 1.61 i 1.42 f SPH ROU CON ABS GRY ORA SMO WHI YEL 1.40 d 2–4
Fortunella sp. 2.65 h 2.50 e ELL ROU CON ABS GRE ORA SMO WHI YEL 1.25 d 2–4
‘Changshou’ kumquat 4.10 f 4.16 d PYR TRU NEC ABS GRE YEL SMO WHI LOR 1.33 d 2–4
‘Jindan’ kumquat 2.75 h 2.50 e ELL ROU CON ABS GRE ORA SMO WHI YEL 1.40 d 2–4
‘Wart Java’ lime 2.68 h 3.34 e OBL TRU TRU ABS GRE LYE RGH YEL YEL 2.30 c 2–4
Microcitrus papuana 5.45 e 1.90 f OUT OUT OUT ABS GRE YEL RGH GRS GRE 1.25 d 2–4
‘Benecke’ trifoliate orange 4.23 f 4.31 d SPH ROU TRU ABS GRE YEL PAP WHI YEL 1.60 d 2–4
‘Coleman’ citrange 5.80 e 6.00 c SPH ROU CON ABS GRE LYE PAP WHI YEL 1.35 d 2–4
‘Flying Dragon’ trifoliate orange 3.90 g 4.05 d SPH ROU TRU ABS GRE YEL PAP YEL YEL 1.20 d 2–4
‘Chinese box-orange’ 0.98 j 0.91 f SPH ROU CON ABS GRE OUT SMO OUT OUT 1.20 d ?6
Euphytica
Euphytica

color, FST fruit surface texture, ALC albedo color, PUC pulp color, NFB number of fruits per bunch, AFB average amount of fruits per bunch, ELL ellipsoid, SPH spheroid, OBL

GRY green–yellow, VAR variegated, YEL yellow, LYE light yellow, DYE dark yellow, ORA orange, LOR light orange, RED red, RGH rough, SMO smooth, PAP papillate, WHI
AFB

FRL fruit length (cm), FRD fruit diameter (cm), FRS fruit shape, FSB shape of fruit base, FSA shape of fruit apex, FRV fruit variegation, IFC immature fruit color, RFC ripe fruit

obloid, PYR pyriform, OVO ovoid, OUT outer, TRU truncate, ROU rounded, MAM mammiform, ACU acute, CON convex, NEC necked, PRE present, ABS absent, GRE green,
Genetic Improvement Program of Embrapa Cassava &

2–4
2–4
2–4
2–4
Fruits the common ‘Sunki’ stands out as an important
1.80 d female parental in controlled crosses (Soares Filho
1.25 d
1.00 d
1.15 d
et al. 2013, 2014). Observations in populations of
NFB

hybrids in the field indicate that the ‘Sunki’ mandarin

has great potential to minifruit production.
ORA
ORA
RED

YEL
PUC

The ‘Cleopatra’ mandarin, Citrus sp. (in this article

identified as ‘Citros Processo’), ‘Tachibana’ orange
and C. depressa (‘Taiwan’ mandarin) are similar to the
ORA
ORA
ALC

WHI
RDS

common ‘Sunki’ mandarin and can be recommended

for the same ornamental uses. The ‘Cleopatra’, which
is widely cultivated in tropical Asia and South
SMO

SMO
SMO
RGH
FST

America (USDA 2014), is a prolific fruit producer,

making it attractive as an ornamental plant, mainly in
the minifruit category (Hodgson 1967).
ORA
RED
LAE

LYE
RFC

Citrus sp. refers to an accession that was impossible

to identify to the species level, but it has characteristics
very near those of the common ‘Sunki’ mandarin, as
GRE
GRE
GRE
GRE
IFC

well as some similarity with the ‘Cleopatra’ variety,

although the latter’s fruits are larger. The fruits are
small (Table 4) and differ from the ‘Sunki’ variety
ABS
ABS
ABS
ABS
FRV

only by the lighter orange color (Fig. 2aj). It is

recommended for landscaping and decorative arrange-
Averages followed by the same letter do not differ by the Scott–Knott test at 5 % probability

ments of minifruit plants.

CON

CON
TRU
TRU
FSA

C. amblycarpa, also known as ‘Nasnaran’ mandarin

(USDA 2014), is a micro-tangerine species with dense
ovoid crown and sparse spines (Table 2). The fruits
ROU
TRU
TRU
TRU
FSB

are oblate and have rough peels which turn yellow

when ripe (Fig. 2a; Table 4). It is a species recom-
mended as a potted plant, for landscaping and as a
OBL
OBL
ELL
SPH
FRS

minifruit plant (Fig. 5u).

The ‘Tachibana’ orange, native to Japan (USDA
4.02 d
4.70 e

6.29 c

2014), has similar appearance to micro-mandarin

1.08 f
FRD

species, with tall stature, dense crown and no spines

(Table 2). The fruits are small and oblate and turn
yellow when ripe (Fig. 2u; Table 4). This accession can
3.38 h
3.24 g
7.51 c
1.77 i
FRL

be recommended for landscaping and minifruit plants.

white, PIN pink, GRS greenish, RDS reddish

The ‘Jaboti’ tangor is a hybrid of the ‘Natal’ sweet

orange and the ‘Satsuma’ mandarin. The accession is
tall, with dense spheroid crown and has no spines
(Table 2). Its leaves are dark green (Fig. 1s; Table 3).
The fruits are oblate and medium sized, with deep
orange color when ripe (Fig. 2s; Table 4). Due to the
Name of the accession

size of its crown, it is recommended for landscaping,

Table 4 continued

‘Cravo’ mandarin
‘Citros Processo’

but can also be used as a parental in crosses to obtain

‘Jerônimo’ lime

hybrids with other potential ornamental uses.

‘Limeberry’

The ‘Mency’ tangor is a hybrid of the ‘Dancy’

tangerine and the ‘Mediterranean’ sweet orange
(Hodgson 1967), with similar characteristics to the

123
 Euphytica

‘Jaboti’ tangor, so the ornamental recommendations Fig. 5 Plant and detail of the branches of accessions of Citrus c
are the same. L. and related genera. a M. papuana, b ‘Flying Dragon’ trifoliate
orange (P. trifoliata), c ‘Talamisan’ orange (C. longispina),
The ‘Fairchild’ tangerine-tangelo is a hybrid of the d ‘Valencia Trepadeira’ sweet orange (C. sinensis), e, f ‘Varie-
‘Clementine’ tangerine (C. clementina) and the ‘Or- gated’ sweet orange (C. sinensis), g, h ‘Variegated’ true lemon
lando’ tangelo (C. paradisi x C. tangerina), commer- (C. limon), i ‘Galego Inerme Key’ lime (C. aurantiifolia),
cially launched in 1964 (Soost and Roose 1996). It has j ‘Mauritius papeda’ (C. hystrix), k ‘Limeberry’ (Triphasia
trifolia), l, m ‘Chinese box-orange’ (Severinia buxifolia),
medium size, ovoid crown and no spines (Table 2). It n ‘Chinotto’ orange (C. myrtifolia), o ‘Jindou’ kumquat
produces many fruits, which are orange and spheroid, (Fortunella hindsii), p ‘Changshou’ kumquat (F. xobovata),
with slightly truncated apex and base (Fig. 2o; q) ‘Jindan’ kumquat (F. xcrassifolia), r ‘Cravo’ mandarin (C.
Table 4). The description of Hodgson (1967) for this reticulata), s, t common ‘Sunki’ mandarin (C. sunki), u ‘Nas-
naran’ mandarin (C. amblycarpa), v ‘Variegated’ calamondin
hybrid coincides with our observations. It is recom- (C. madurensis), w ‘Bergamot’ orange (C. bergamia), x ‘Papeda
mended for landscaping and as a parental to produce Kalpi’ (C. webberi), y ‘Etrog’ citron (C. medica)
genotypes with ornamental potential.
The ‘Variegated’ calamondin is short, with spherical
crown, no spines and medium to dense branching C. bergamia, known as ‘Bergamot’, is a natural
(Fig. 5v; Table 2). Its leaves are variegated, oval and hybrid from crossing C. medica and [C. maxima
small (Fig. 1k; Table 3), giving it good ornamental (Burm.) Merr. x C. reticulata] (USDA 2014). The
potential. The fruits are abundant, small, spherical and crown is pronouncedly erect (Fig. 5w), it does not
variegated when immature (Fig. 2k; Table 4). It is have spines and its leaves stand out for their orbicular
recommended for use as a potted plant, for landscaping shape, bright green color and curled format (Fig. 1d).
and as a minifruit plant. It is sold by nurseries in Florida It is recommended for landscaping and in genetic
and California (USA) as a potted plant (Hodgson 1967). improvement programs due to its unique foliage.
Besides the 12 accessions with fruits classified as C. webberi var. montana, also known as ‘Papeda
tangerines or mandarins already mentioned, five Kalpi’, is medium-sized, with a dense ovoid crown
others are contained in Group G7: ‘Jerônimo’ lime, and no spines (Fig. 5x; Table 2). Its leaves are oval
‘Narrow Leaf’ sour orange, ‘Bergamot’ orange, and longipetiolate, with winged petioles having the
‘Papeda Kalpi’ and ‘Etrog’ citron. same size as the leaf limbus (Fig. 1w; Table 3). It is
The ‘Jerônimo’ lime was classified as Citrus sp., attractive for landscaping due to the shape and density
although it is possibly a natural hybrid of the rough of the crown, and can also be recommended as a potted
lemon (C. jambhiri Lush.). This accession has small plant and for forming hedges.
size, ovoid and drooping crown, with sparse to average The ‘Etrog’ citron probably is native to China and
branching (Table 2). It was included in this study India (USDA 2014), and is one of the basic Citrus
mainly because of its small size and drooping branches, species. Along with C. maxima and C. reticulate sensu
allowing it to be used as coverage for pergolas. Swingle, it is at the root of the ancestral species of
The ‘Narrow Leaf’ sour orange is cultivated in Citrus (Barrett and Rhodes 1976; Velasco and Lic-
tropical and subtropical regions, and possibly origi- ciardello 2014). It has medium size, a crown with
nates from China (USDA 2014). It is a tall tree that scarce to medium branching and has spines (Fig. 5y;
grows vertically straight, with elliptical crown and no Table 2). The fruits are large and ovoid, with a
spines (Fig. 2o; Table 2). It has dark green lanceolate characteristic fragrance and yellow color when ripe
leaves that are long and narrow (Fig. 1c; Table 3), (Fig. 2j; Table 4). Some varieties of the citron group,
hence its name. According to Saunt (1990), sour such as the ‘Buddha’s Hand’, are already widely used
orange varieties are grown for ornamental purposes in for ornamental purposes (Swingle 1967). The ‘Etrog’
public and private gardens in many countries due to citron can be used as a potted plant or for landscaping.
their perceived beauty. This is especially the case Group G8 only contains one accession, the ‘Star
along the Mediterranean coast and in places in Arizona Ruby’ grapefruit. The tree is mediums-sized with a
and California. Therefore, the ‘Narrow Leaf’ tree can spheroid crown that has plentiful branches and low
be used for landscaping and in genetic improvement density of spines (Table 2). The ripe fruits are yellow
programs to generate hybrids with other potential and reddish pulp. This is the trait that sets it apart from
ornamental uses. the other accessions (Fig. 2m). It is recommended for

123
Euphytica

123
 Euphytica

Table 5 Quantitative and Name of the accession COF FLL FLP ARO ARP
qualitative flower traits in
37 accessions from the ‘Nasnaran’ mandarin WHI BOT BOT FRU NPE
Citrus Active Germplasm
‘Galego Inerme Key’ lime WHI BOT BOT BOT NPE
Bank of Embrapa Cassava
& Fruits with ornamental ‘Narrow Leaf’ sour orange WHI BOT BOT FLO NPE
potential ‘Bergamot’ orange WHI BOT BOT FRU NPE
‘Taiwan’ mandarin WHI BOT BOT FRU PER
‘Mauritius papeda’ WHI BOT BOT FRU PER
C. hystrix hibrid WHI BOT BOT FRU PER
‘Variegated’ true lemon WHI BOT BOT FRU NPE
‘Talamisan’ orange WHI BOT BOT FRU NPE
‘Etrog’ citron WHI BOT BOT FRU NPE
‘Variegated’ calamondin WHI BOT BOT FRU NPE
‘Chinotto’ orange WHI BOT BOT FRU NPE
‘Star Ruby’ grapefruit WHI INF BOT FRU NPE
‘Cleopatra’ mandarin WHI BOT BOT FRU NPE
‘Fairchild’ tangerine-tangelo WHI BOT BOT BOT NPE
‘Szincom’ mandarin WHI BOT BOT FRU NPE
‘Valencia Trepadeira’ sweet orange WHI BOT BOT FRU NPE
‘Variegated’ sweet orange WHI BOT BOT FRU NPE
‘Jaboti’ tangor WHI BOT BOT FRU NPE
Common ‘Sunki’ mandarin WHI BOT BOT FRU NPE
‘Tachibana’ orange WHI BOT BOT FRU NPE
‘Mency’ tangor WHI BOT BOT FRU PER
‘Papeda Kalpi’ WHI BOT BOT FRU NPE
‘Jindou’ kumquat WHI BOT BOT BOT NPE
Fortunella sp. WHI BOT BOT BOT NPE
‘Changshou’ kumquat WHI BOT BOT BOT NPE
‘Jindan’ kumquat WHI BOT BOT BOT NPE
‘Wart Java’ lime WHI BOT BOT FRU NPE
Microcitrus papuana WHI BOT BOT FRU NPE
‘Benecke’ trifoliate orange WHI BOT BOT FRU PER
COF colour of open flower, ‘Coleman’ citrange WHI BOT BOT FRU NPE
FLL flower layout, FLP ‘Flying Dragon’ trifoliate orange WHI BOT BOT FRU NPE
flower/inflorescence ‘Chinese box-orange’ WHI BOT BOT FRU NPE
position, ARO aroma, ARP
‘Limeberry’ WHI BOT BOT FRU NPE
aroma persistence, WHI
white, PIN pink, BOT both, ‘Cravo’ mandarin WHI BOT BOT FRU NPE
INF inflorescence, FLO ‘Citros Processo’ WHI BOT BOT FRU NPE
flours, FRU fruits, NPE not ‘Jerônimo’ lime PIN BOT BOT FRU NPE
persistent, PER persistent

landscaping and its fruits can be used in decorative ‘Variegated’ true lemon, ‘Variegated’ sweet orange,
arrangements. ‘Jaboti’ tangor, ‘Etrog’ citron, ‘Galego Inerme Key’
Although the fruit persistence on trees was not lime, ‘Papeda Kalpi’, ‘Narrow Leaf’ sour orange,
directly evaluated in this work, it was observed that the ‘Bergamot’ orange, ‘Mauritius papeda’ and C. hystrix
accessions P. trifoliata selections, ‘Chinotto’ orange, clearly presented more persistent fruits. On the other
‘Star Ruby’ grapefruit, ‘Wart Java’ lime, M. papuana, hand, mandarins, tangerines, micro-tangerines, and
‘Jerônimo’ lime, ‘Variegated’ calamondin, Fortunella spp., visually presented lower fruit

123
Euphytica

persistence, indicated by the precocious fruit drop, in Barrett HC, Rhodes AM (1976) A numerical taxonomic study of
spite of their profuse fruiting. Fruit persistence is one affinity relationships in cultivated Citrus and its close
relatives. Syst Bot 1:105–136
of the traits to considerate for ornamental use in citrus, Bastianel M, Dornelles ALC, Machado MA, Wickert E, Mar-
besides flowering and fruit set. Fruit persistence is aschin SF, Coletta Filho HD, Schäfer G (2001) Carac-
particularly of interest because it determines the terização de genotypes de Citrus spp. através de
general value and attractiveness of a citrus ornamental marcadores RAPD. Ciênc Rural 31:763–768. doi:10.1590/
S0103-84782001000500004
tree, and might be a limitant factor in windy locations. Bizzo HR (2009) Brazilian essential oils: general view, devel-
All these traits are typical of the genotype and are opments and perspectives. Quı́m Nova 32:588–594. doi:10.
genetically controlled, even though several environ- 1590/S0100-40422009000300005
mental and physiological conditions might influence Cruz CD (2006) Programa GENES: análise multivariada e
simulação. UFV, Viçosa
on them being also mediated by abiotic and biotic Del Bosco SF (2003) The use for ornamental purposes of an
stresses and horticultural practices. ancient Citrus genotype. Acta Hortic 598:65–67
Development Core Team R (2006) A language and environment
for statistical computing. R Foundation for Statistical
Computing, Vienna
Conclusion Donadio LC, Mourão Filho FAA, Moreira CS (2005) Centros de
origem, distribuição geográfica das plantas cı́tricas e
histórico da citricultura no Brasil. In: Mattos Júnior D, De
1. The great morphological variability of the citrus Negri JD, Pio RM, Pompeu Junior J (eds) Citros. Instituto
accessions studied allows their classification in Agronômico e Fundag, Campinas, pp 1–18
different ornamental use categories. FAO (2015) FAOSTAT. Agricultural statistics database. World
Agricultural Information Center, 2009 Rome. http://
2. The ‘Nasnaran’ mandarin, ‘Talamisan’ orange, faostat.fao.org/site/567/default.aspx#ancor. Accessed 4
‘Variegated’ calamondin, ‘Chinotto’ orange, ‘Wart Jan 2015
Java’ lime, ‘Limeberry’, ‘Variegated’ true lemon, Gower JC (1971) A general coefficient of similarity and some of
‘Variegated’ sweet orange, as well as the accessions its properties. Biometrics 27:857–874
Hodgson RW (1967) The botany of Citrus and its wild relatives.
belonging to the genera Fortunella and Poncirus, In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus
can be used in the potted plant and landscaping industry. University of California, Riverside
categories, although attention should be paid to the IPGRI—International Plant Genetic Resources Institute. De-
presence of spines in the case of Poncirus. scriptors for Citrus. Rome: IBPGR (1999). http://www.
bioversityinternational.org/e-library/publications/detail/
3. ‘Chinese box-orange’, ‘Limeberry’ and M. descriptors-for-citrus-emcitrusem-spp/. Accessed 8 May
papuana can be employed as ornamental hedges. 2012
4. The common ‘Sunki’ mandarin can be used as a Koehler-Santos P, Dornelles ALC, Freitas LB (2003) Charac-
minifruit plant. terization of mandarin citrus germplasm from Southern
Brazil by morphological and molecular analyses. Pesq
5. The accessions studied can be used as parentals in Agrop Bras 38:797–806. doi:10.1590/S0100-204X2003
crosses to generate ornamental citrus hybrids. 000700003
Lanjouw J (1961) International code of botanical nomenclature.
Adopted by the Ninth International Botanical Congress
Acknowledgments The authors acknowledge the support of (Montreal, 1959). Utrecht, 1961
Conselho Nacional de Desenvolvimento Cientı́fico e Mazzini RB, Pio RM (2010) Morphological characterization of
Tecnológico—CNPq (472492/2011-0), and Coordenação de six citrus varieties with ornamental potential. Rev Bras
Aperfeiçoamento de Pessoal de Nı́vel Superior (CAPES) for the Frutic 32:463–470. doi:10.1590/S0100-2945201000500
scholarships granted. We also thank the researcher Orlando 0043
Sampaio Passos, curator of the Citrus Active Germplasm Bank Nicolosi E, Deng ZN, Gentile A, La Malfa S, Continella G,
of Embrapa Cassava & Fruits, and the anonymous reviewers for Tribulato E (2000) Citrus phylogeny and genetic origin of
their valuable suggestions. important species as investigated by molecular markers.
Theor Appl Genet 100:1155–1166. doi:10.1007/
s001220051419
Rohlf FJ, Fisher DR (1968) Tests for hierarchical structure in
References random data sets. Syst Biol 17:407–412. doi:10.1093/
sysbio/17.4.407
Araújo ARG, Salibe AA (2002) Caracterização fı́sico-mor- SAS Institute (2010) SAS user’s guide: statistic: version 9.2.
fológica de frutos de microtangerinas (Citrus spp.) de po- SAS Institute, Cary
tencial utilização como porta-enxertos. Rev Bras Frutic Saunt J (1990) Citrus varieties of the world: an illustrated guide.
24:618–621. doi:10.1590/S0100-29452002000300009 Sinclair International, Norwich

123
 Euphytica

Silva KT (1995) Development of essential oil industries in de- Souza EH, Souza FVD, Costa MAPC, Costa DS Jr, Santos-
veloping countries. In: Silva KT (ed) A manual on the Serejo JA, Amorim EP, Ledo CAS (2012b) Genetic var-
essential oil industry. United Nations Industrial Develop- iation of the Ananas genus with ornamental potential.
ment Organization, Vienna, pp 1–13 Genet Resour Crop Evol 59:1357–1376. doi:10.1007/
Singh D (1981) The relative importance of characters affecting s10722-011-9763-9
genetic divergence. Indian J Genet Plant Breed 41:237–245 Swingle WT (1967) The botany of Citrus and its wild relatives.
Soares Filho WS, Cunha Sobrinho AP, Passos OS, Souza AS In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus
(2013) Melhoramento genético. In: Cunha Sobrinho AP, industry. University of California, Berkeley, pp 190–430
Magalhães AFJ, Souza AS, Passos OS, Soares Filho WS Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: mole-
(eds) Cultura dos citros. Embrapa, Brası́lia, pp 61–102 cular evolutionary genetics analysis (MEGA) software
Soares Filho WS, Souza U, Ledo CAS, Santana LGL, Passos OS version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/
(2014) Polyembryony and potential of hybrid production in molbev/msm092
citrus. Rev Bras Frutic 36:950–956. doi:10.1590/0100- Tanaka T (1961) Citrologia. Semi-centennial commemoration
2945-345/13 papers on citrus studies. Citrologia Supporting Foundation,
Sokal RR, Rohlf FJ (1962) The comparison of dendrograms by Osaka
objective methods. Taxon 11:33–40 USDA (2014) ARS, National Genetic Resources Program.
Soost RK, Roose ML (1996) Citrus. In: Janick J, Moore JN (eds) Germplasm Resources Information Network—(GRIN).
Fruit breeding; tree and tropical fruits. Wiley, New York, National Germplasm Resources Laboratory, Beltsville,
pp 257–323 Maryland. http://www.ars-grin.gov/cgibin/npgs/html/tax
Souza EH, Costa MAPC, Souza FVD, Costa DS Jr, Amorim EP, genform.pl?language=pt. Accessed 12 Feb 2014
Silva SO, Santos-Serejo JA (2012a) Genetic variability of Velasco R, Licciardello C (2014) A genealogy of the citrus
banana with ornamental potential. Euphytica 184:355–367. family. Nature 32:640–642. doi:10.1038/nbt.2954
doi:10.1007/s10681-011-0553-4

123

View publication stats