Plant Size

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Euphytica (2012) 184:369–376

DOI 10.1007/s10681-011-0597-5

The plant size and the spine characteristics of the first


generation progeny obtained through the cross-pollination
of different genotypes of Cactaceae
Lucica Mihalte • Radu E. Sestras

Received: 5 June 2011 / Accepted: 29 November 2011 / Published online: 7 December 2011
Ó Springer Science+Business Media B.V. 2011

Abstract The main characteristics (plant diameter, traits. The broad-sense heritability ranged between
number of spine/areoles and length of spines) of 16 0.909 (plant diameter) and 0.948 (spines length). All of
cactus hybrids were analysed and the genetic variabil- the characters analysed, in the present experience, have
ity and broad-sense heritability was studied. The a strong genetic determinism, being greatly influenced
descendants were obtained through a cyclic cross- by the genotype and to a lesser extent, by the
pollination pattern, with the parental forms chosen cultivation conditions (greenhouse).
based on aesthetic considerations. Cross-pollination
among Rebutia senilis 9 Aylostera muscula, Rebutia Keywords Cactaceae  F1 hybrids 
tarvitaensis 9 Aylostera muscula, Aylostera flavi- Interspecific hybridisation  Inter-generic
styla 9 Rebutia senilis, Rebutia senilis 9 Aylostera hybridisation  Genetic diversity
flavistyla, Aylostera muscula 9 Aylostera albiflora
and Rebutia senilis 9 Aylostera albiflora did not
succeed, whereas all of the other hand-pollinated
crosses succeeded and produced viable seeds. The Introduction
highest values of the analysed characters were
observed in the progeny of A. fiebrigii var. densise- The Cactaceae family (order Caryophyllales) includes
ta 9 R. senilis and A. buiningiana 9 A. vallegarden- plants with perennial photosynthetic succulent stems,
sis and the artificial selection to identify plants with spines produced on modified axillary buds (termed
special decorative traits was extremely efficient among areoles) and colourful flowers with numerous stamens.
them. In the F1 population of the studied crosses, a The multiple uses and the ability of cacti to thrive in
large genetic diversity was found within hybrid the arid and semiarid environments that other species
combinations (families), between combinations and a are unable to tolerate make it of interest to breeders
different variation was recorded among the analysed and molecular biologist seeking to develop crops for
areas typically unsuitable for conventional agriculture
L. Mihalte (&)  R. E. Sestras (Nobel 2002). A primary breeding goal should be the
Department of Genetics and Plant Breeding, expansion of the production area for cacti by devel-
University of Agricultural Science and Veterinary oping cold-tolerant cultivars because the current high-
Medicine, 3-5 Manastur, Cluj-Napoca 400372,
Romania yielding fruit, vegetable and forage varieties do not
e-mail: [email protected] survive between temperatures of -5 and -8°C (Loik
R. E. Sestras and Nobel 1991; Parish and Felker 1995; Wang et al.
e-mail: [email protected] 1998).

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370 Euphytica (2012) 184:369–376

The genetic diversity in cultivated cacti is limited hybridisation on Cactoideae, a more diverse subfam-
by the small number of progenitors and the loss of ily (Machado 2008). Therefore, in the present
genetic variation during cultivation (Nobel 2002) and research, we chose species from the Aylostera and
most of the domesticated cacti grown for fruit or Rebutia genera and therefore, the aim of this study was
ornamental flowers apparently originated from a to identify potential genitors for breeding programs
relatively narrow germplasm base. In the case of and to improve the genetic diversity, which will permit
Eastern cactus, over 100 distinct clones have been an efficient selection of new cultivars.
described, but Meier (1995) proposed that all are
probably the descendants of three plants (two Hatiora
gaertneri and one H. rosea). Materials and methods
Cacti are threatened by the loss and degradation of
their habitat and illegal collection (Oldfield 1997; Plant material and growth conditions
Boyle and Anderson 2002); the most important factor
causing the loss of biodiversity is intensive land use The Cactaceae species used in the present research were
(Zak et al. 2004). The ‘‘Red List’’ of threatened species grown in the greenhouse complex at the ‘‘Alexandru
of the International Union for the Conservation of Borza’’ Botanical Garden of Cluj-Napoca, Romania.
Nature (IUCN) provides a categorised list of species This Cactaceae collection comprises more than 4100
based on their relative risk of extinction at a global specimens belonging to 115 genera from the 241 total
scale; the list includes at least 104 cacti species (7% of known according to the Backeberg system (1968–1977).
all species) as vulnerable to extinction (IUCN 2008). Based on aesthetic considerations (shape of plant,
The majority of the studies regarding cacti hybrid- flower diameter and colour of flowers), we chose 19
isation have been restricted to the Opuntioideae genotypes as the genitors for the interspecific and
subfamily and little is known about the role of inter-generic hybridisations (Table 1).

Table 1 The main traits of the parental genotypes


Species Plant shapea No. spines/areoles Flower Flower
and length of spines diameter (cm) colours

Aylostera muscula Oval 23/2.4 mm 3.5 Orange


Aylostera flavistyla Globular 15–22/5–10 mm 3 Red
Aylostera fiebrigii Globular 30/40.1 cm 3.5 Orange
Aylostera fiebrigii var. densiseta Globular 40/50.1 cm 3.5 Orange
Aylostera spinosissima Globular 20–30/1.5 cm 3 Red
Aylostera narvacensis Globular 10–20/2–3 mm 4 Pink
Aylostera archibuingiana Globular 12/2–3 mm 4 Red
Aylostera buingiana Globular 14–16/0.6–1 cm 3 Pink
Aylostera vallegardensis Globular 20/3 cm 3.5 Pink
Aylostera albiflora Globular 15/5 mm 2.5 White
Rebutia senilis Globular 25/over 3 cm 3.5 Red
Rebutia senilis var. hyalacantha Globular 25/2 cm 3 Red
Rebutia travitaensis Globular 7–9/2–5 mm 6 Red
Rebutia cajasensis Globular 13/15.5 mm 3.5 Red
Rebutia spegazziana Cylindrical 23/4 mm 4 Dark red
Rebutia pseudominuta var schumaniana Globular 27/1.2 cm 2.5 Orange
Rebutia kuperiana Globular 13/15.5 mm 3.5 Red
Rebutia kuperiana var. spiniflora Globular 13/15.8 mm 3 Red
Rebutia donaldiana Globular 25/3 cm 3.5 Pink
a
All of the values represented the arithmetic mean

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Euphytica (2012) 184:369–376 371

The hybrid seeds were sown in small pots in a also possible that their seeds experience a dormancy
mixture, composed of three parts of sterilised fibrous period (Mihalte et al. 2010).
soil, one part peat moss and one part washed sand The experiment was structured following a com-
(Hewitt 1993) and were grown in the Botanical pletely randomised (CR) design with three replica-
Garden Cluj-Napoca, Romania. The seeds were free tions for each analysed trait (plant diameter, number of
of chemicals and fertiliser. In December, the minimum spine/areoles and length of spines). The differences in
temperature dropped to 5°C and the maximum the characteristics of the progeny were analysed
temperature reached 23.48°C in July. statistically using ANOVA, where the mean of the
experiment was the control and the coefficient of
Experimental design and statistical analyses variability (CV%) for traits was computed. The data
are presented as the means and standard deviations for
Using a cyclic hybridisation pattern, 14 interspecific each cyclic hybridisation.
combinations (between two species of the same genus)
and 16 inter-generic combinations (between two plants
belonging to two different genera) was achieved. Genetic parameters
To isolate a cross-pollinated flower from the
possibility of contamination by the pollen from other The main characteristics of the F1 hybrids inform the
plants and to distinguish the differences between interspecific and inter-generic hybridisation were
hybrid and non-hybrid fruits, each flower was insu- calculated and are discussed in terms of the coeffi-
lated individually with sticky paper and different cients of variability within each hybrid family. The
colours of thread were used for each flower (Mon- uniformity of the traits was computed based on the
dragon-Jacobo and Bordelon 1996). following coefficients: CV% \ 10%-low variability;
A total of ten plants were pollinated for each 10% \ CV% \ 20%-medium variability and CV%
combination and every plant contained approximately [ 20%-high variability (Reed et al. 2002; Sestras et al.
ten flowers. Hybrid seeds were obtained from 12 2009).
interspecific and 12 inter-generic combinations and To determine the genetic proportion in the pheno-
ten seeds were sown/pot. Viable F1 progeny were typic expression of the studied characteristics, the
obtained in 16 hybrid families and the plants were coefficient of heritability was also calculated, where
analysed in the first year of vegetative growth (Fig. 1). the individual of the F1 of a cross was the observa-
The low proportion of seed germination can be tional unit. The broad-sense heritability was noted and
explained by the different growth forms of cacti: computed by a classical model, H2 = rG2/rP2, where
columnar cacti have a higher rate of seed germination rG2 is the genotypic variance and rP2 is the pheno-
than globular cacti (Ortega-Baes et al. 2010). Aylos- typic variance (Holland et al. 2003; Piepho and
tera and Rebutia species are globular cacti and it is Möhring 2007; Sestras et al. 2008).

Fig. 1 The first generation of the progeny of the studied cacti species at several weeks (a) and during the first year of vegetative
growth (b)

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372 Euphytica (2012) 184:369–376

Results muscula 9 Aylostera albiflora, Rebutia senilis 9 Ay-


lostera albiflora were unsuccessful (Table 2). All of
The cross-pollination of parental forms the other artificial hybridisations were successful and
produced viable seeds; however, a viable F1 genera-
The cross-pollinations among Rebutia senilis 9 tion was obtained in only 16 hybrid combinations. The
Aylostera muscula, Rebutia tarvitaensis 9 Aylostera parental genotype, Aylostera fiebrigii, has been
muscula, Aylostera flavistyla 9 Rebutia senilis, reported to present a small capacity of germination
Rebutia senilis 9 Aylostera flavistyla, Aylostera when it has been used for studying the germination

Table 2 Hybrid combinations and results of hybridisations


No. Mother genotype ($) Father genotype (#) Results of hybridization Viable F1
(fruits and seeds) descendants

Interspecific hybridisations
1. R. spegazziana R. senilis ? -
2. R. pseudodeminuta var. schumaniana R. senilis ? -
3. R. cajasensis R. senilis ? ?
4. R. senilis R. kupperiana var. spiniflora ? ?
5. R. senilis R. spegazziana ? ?
6. R. senilis var. hyalacantha R. spegazziana ? -
7. A. flavistyla A. archibuinigiana ? -
8. A. buiningiana A. vallegardensis ? ?
9. A. muscula A. vallegardensis ? ?
10. A. fiebrigii A. vallegardensis ? ?
11. A. muscula A. buiningiana ? ?
12. A. buinigiana A. flavistyla ? -
13. A. muscula A. albiflora - -
14. A. spinosissima A. albiflora ? ?
Inter-generic hybridisations
15. R. senilis A. muscula - -
16. R. tarvitaensis A. muscula - -
17. R. cajasensis A. muscula ? ?
18. A. flavistyla R. senilis - -
19. A. fiebrigii var. densiseta R. senilis ? ?
20. A. spinosissima R. senilis ? -
21. A. muscula R. kupperiana var. spiniflora ? ?
22. A. narvaecensis R. kupperiana var. spiniflora ? ?
23. A. spinosissima R. spegazziana ? -
24. R. cajasensis A. archibuinigiana ? ?
25. R. senilis A. archibuinigiana ? ?
26. R. donaldiana A. buiningiana ? ?
27. R. kupperiana var. spiniflora A. buiningiana ? -
28. R. cajasensis A. flavistyla ? ?
29. R. senilis A. flavistyla - -
30. R. senilis A. albiflora - -
‘‘?’’ means that the specified hybrid combinations produced fruits and seeds, respectively and viable F1 progeny; ‘‘-’’ means that the
specified hybrid combinations did not produce fruits and seeds, respectively, or viable F1 progeny

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Euphytica (2012) 184:369–376 373

percentages of different cacti species (Mihalte et al. R. senilis 9 R. kupperiana var. spiniflorum; a large
2009). variability for the A. narvaecensis 9 R. kupperiana
var. spiniflorum and R. senilis 9 A. archibuinigiana
The plant diameter hybrid family and a medium variability for the
remainder of the hybrid combinations.
The plant diameters of the progeny were variable
(Table 3), with the average of the F1 hybrids in the The number of spines/areoles
studied families varying significantly compared with
the control. The variability of the number of the spines/areoles in
High values of plant diameter, suggesting high the F1 hybrids was quite small; only the combinations
vigour, presented in the hybrids of the following A. buiningiana 9 A. vallegardensis and R. cajasen-
combinations: R. senilis 9 R. kupperiana var. spini- sis 9 A. archibuinigiana presented hybrids with a
florum, A. buiningiana 9 A. vallegardensis, A. mus- medium variability of this trait (Table 3).
cula 9 A. vallegardensis. In general, the hybrids Compared with the mean of experience (21.0), the
derived from the interspecific combinations were number of spines/areoles in the F1 hybrids showed
more vigorous than the hybrids from the inter-generic positive values for the following crosses: A. fiebrigii var.
combinations. densiseta 9 R. senilis, A. muscula 9 R. kupperiana
The following different variations of characteristics var. spiniflorum, A. muscula 9 A. vallegardensis and A.
in the F1 populations were noted: a low variability spinosissima 9 A. albiflora. Of all of the hybrid
among the hybrids of R. cajasensis 9 R. senilis and combinations, the lowest number of spines/areoles

Table 3 The plant diameter, the number of spines/areolas and the length of spines, coefficient of variability and significance of
values* of the F1 hybrids
No. Hybrid combination Plant diameter CV% No. of spines/ CV% The length CV%
($ 9 #) (cm) areolas of spines (mm)

1. R. cajasensis 9 R. senilis 2.6 ± 0.1 8.4 14.5 ± 6.2°°° 8.9 20.0 ± 4.2* 11.3
2. R. senilis 9 R. kupperiana var. spiniflorum 3.2 ± 0.7** 8.4 22.3 ± 1.6 7.7 15.8 ± 0.1 7.2
3. R. senilis 9 R. spegazziana 1.8 ± 0.8°° 11.9 22.5 ± 1.8 5.7 17.2 ± 1.4 9.8
4. A. buiningiana 9 A. vallegardensis 3.3 ± 0.8** 23.0 15.5 ± 5.2°°° 13.4 20.6 ± 4.8* 9.4
5. A. muscula 9 A. vallegardensis 3.2 ± 0.7** 13.3 23.5 ± 2.8** 5.5 9.6 ± 6.3°° 17.7
6. A. fiebrigii 9 A. vallegardensis 2.5 ± 0.0 19.0 20.5 ± 0.2 6.3 26.2 ± 10.4*** 13.8
7. A. muscula 9 A. buiningiana 2.6 ± 0.1 8.6 22.5 ± 1.8 5.7 9.8 ± 6.0°° 13.6
8. A. spinosissima 9 A. albiflora 3.6 ± 1.1*** 8.2 23.3 ± 2.6** 11.8 15.5 ± 0.3 13.6
9. R. cajasensis 9 A. muscula 1.5 ± 1.0°°° 14.4 16.8 ± 4.0°°° 10.2 8.8 ± 7.1°°° 20.9
10. A. fiebrigii var. densiseta 9 R. senilis 2.4 ± 0.2 11.3 27.8 ± 7.1*** 6.2 27.1 ± 11.3*** 11.3
11. A. muscula 9 R. kupperiana var. spiniflorum 2.8 ± 0.3 6.2 25.5 ± 4.8*** 5.1 11.4 ± 4.4° 17.8
12. A. narvaecensis 9 R. kupperiana var. 2.2 ± 0.3 24.7 21.5 ± 0.8 6.0 12.8 ± 3.0 23.8
spiniflorum
13. R. cajasensis 9 A. archibuinigiana 2.1 ± 0.4 12.3 17.5 ± 3.2°°° 11.9 8.5 ± 7.4°°° 37.5
14. R. senilis 9 A. archibuinigiana 1.9 ± 0.6° 28.2 19.8 ± 0.9 8.6 14.4 ± 1.4 18.7
15. R. donaldiana 9 A. buiningiana 2.4 ± 0.1 17.7 20.8 ± 0.1 10.7 18.2 ± 2.4 28.8
16. R. cajasensis 9 A. flavistyla 2.0 ± 0.5° 12.7 21.5 ± 0.8 8.9 17.6 ± 1.8 19.0
Mean of experiment (control) 2.5 14.2 21.0 8.3 15.8 17.1
LSD 5% 0.5 2.5 3.7
LSD 1% 0.7 3.3 4.9
LSD 0.1% 0.9 4.3 6.4
*, **, ***/°, °°, °°° Significant at P \ 0.05, 0.01 and 0.001 (* means positive and ° means negative, respectively)

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was recorded for the hybrids derived from R. cajasensis hybrids with small plant diameters and small lengths
9 R. senilis and A. buiningiana 9 A. vallegardensis. of spines and with large plant diameters and large
Regarding the genitors, the smallest number of spine/ lengths of spines in any combination (both forms are
areoles was recorded in R. cajasensis and A. archibuin- suitable for new ornamental forms).
igiana species and it appears that this characteristic was The broad-sense heritability (Fig. 2) ranged
transmitted to the F1 progeny derived from these between 0.909 (plant diameter) and 0.948 (spine
crosses. length). All of the characters analysed, at least in terms
of this experience, have a strong genetic determinism,
being strongly influenced by genotype and to a lesser
The length of spines
degree, by the culture medium (greenhouse).
Very small spines presented the hybrids of the
following crosses: R. cajasensis 9 A. muscula, R.
Discussion
cajasensis 9 A. archibuinigiana and A. muscula 9 A.
vallegardensis (Table 3).
The ability of pollen to germinate is an important
The results showed that when R. cajasensis and A.
aspect in cross-pollination (Oyiga et al. 2010). In
archibuinigiana were used as the genitors, the length of
previous studies, the pollen germination ability of the
the spines was transmitted to the progeny with sufficient
parental plants used in this study was investigated and
fidelity and the hybrids progeny inherited the small
detected as being high (Mihalte et al. 2010). Even with
number of spines/areoles. A. fiebrigii and A. vallegard-
a high percentage of viable pollen, the cross-pollina-
ensis, both having longer spines than most of the studied
tion between Aylostera flavistyla and Rebutia senilis
species, passed this trait to their descendants.
did not succeed with using Aylostera flavistyla as
either the male or female parent. Thus, Aylostera
The variability and the heritability of the analysed flavistyla can be considered incompatible, as can
traits Hatiora (Boyle et al. 1994) and Schlumbergera (Boyle
1997). In addition, manual cross-pollination using
The obtained data showed the existence of a large wild Stenocereus stellatus failed between some
diversity, where the resulting variability was mani- domesticated and wild genotypes, suggesting a pollen
fested within the hybrid combinations (families) and incompatibility (Casas et al. 1999). The hybridisation
between the combinations. We also found a different experiments by Hentzschel and Hentzschel (2001) of
variation based on the characteristic that was analysed Sulcorebutia, Weingartia, Rebutia and Echinopsis
(Fig. 2). have produced the following results: most of the
The lowest coefficient of variability was recorded hybridisation failed between Sulcorebutia and Rebutia
for the number of spines/areoles (18.0%), whereas a padcayensis, even though the latter closely resembles
wide variability was recorded for the plant diameter Sulcorebutia and with several other Rebutia species.
(26.9%) and length of spines (38.4%). Therefore, the For other genera (Selenicereus and Hylocereus), inter-
CV% values indicate that it is possible to identify generic crosses appear to be a successful approach to
increase diversity. Tel-Zur et al. (2003) obtained
triploid, pentaploid, hexaploid and aneuploid hybrids
Length of the
0.948 in inter-generic crosses (Selenicereus and Hylocere-
22.40
spines us). However, Lichtenzveig et al. (2000) reported
Number of 0.943 viable hybrids from inter-generic and interspecific
spines/areolas 18.00
crosses between Selenicereus and Hylocereus.
0.909 High vigour, as observed for R. senilis 9 R.
Plant diameter
26.90 kupperiana var. spiniflorumand and A. buiningi-
0.00 5.00 10.00 15.00 20.00 25.00 30.00 ana 9 A. vallegardensis, is of considerable impor-
The variability The broad-sense heritability
tance to breeders, especially for the Rebutia genus,
Fig. 2 The variability and the broad-sense heritability of the which are generally small (Pilbeam 1997). For breed-
studied characteristics in the first-generation progeny (F1) ers, vigour correlates with increased photosynthetic

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Euphytica (2012) 184:369–376 375

area and improved root anchorage (Mondragon- due mainly to the influence of the female parent, but
Jacobo and Bordelon 1996). we do not exclude the possible effects of the male
McIntosh (2002) correlated vigour with the size of genitor and of course, those caused by the environ-
the plants for species of Ferocactus and showed that mental conditions, culture and interactions between
large plants grow more than small plants. However, in the genotype and ecotype.
terms of percent change in volume, the relationship The high genetic variability shown in the present
was the opposite: large plants grew less as a percent of research allows an efficient selection, but further
size than small plants. In addition, the number of investigation should be performed by examining the
flowers produced by a plant was significantly and levels of allozyme variation and the genetic structure
positively correlated with the size of the plant, but the (Figueredo et al. 2010).
flower abortion rates (Burd 1998) and the number of For most cross-pollinations, as was the case of the
seeds per fruit were not influenced by this factor. cactus species described here, the efficiency of
The study of the seminal progeny obtained from phenotypic selection is decisively affected by the size
hand-pollination showed that central spines lack in F1 of the heritability coefficient (Leite et al. 2006). Thus,
hybrids, as they do in their parents. For most crop the phenotypic selection for all of the studied charac-
cacti, the presence of spines is an inconvenience and ters in the populations represented by the F1 hybrids
significant efforts to develop new cultivars are focused can be efficient.
on spineless cultivars (Mondragon-Jacobo and Bord- Because the inheritance from genitors and the fixing
elon 1996). For ornamental cacti, as are the species of such characteristics was possible in the F1 hybrid
described here, the presence of spines is a positive descendants, studies of cacti germplasm to perform
element for their decorative traits. Peharec et al. artificial variability followed by artificial selection are
(2010) evaluated the spines of pot-grown Mammillar- absolutely justified and extremely useful to obtain new
ia plants and in vitro-regenerated shoots and found varieties. The obtained results are encouraging find-
that the pot-grown plants had 16–17 spines per areole, ings, which indicate that the studied characteristics are,
whereas the in vitro-grown shoots were normal but overall, under strong genetic control and that a
displayed a lower number of spines (11–12). Parra genotype with a given performance could be selected
et al. (2010) argued that genetic diversity should be and genetically improved. The narrow-sense heritabil-
conserved and should be promoted by artificial ity and the additive genetic variance have not been
selection, which, despite the high levels of gene flow, studied in this experience because these aspects are
moderate the genetic structure between wild and inappropriate for hybrids, owing to the genetic dis-
managed populations. equilibrium inherent in their origin (Gordon 1999).
A. fiebrigii var. densiseta 9 R. senilis, A. mus- The obtained results indicate that through artificial
cula 9 R. kupperiana var. spiniflorum and A. mus- hybridisation under a suitable choice of genitors,
cula 9 A. vallegardensis presented a large number of progeny with major features for selection that have
spines/areoles. The obtained results suggest the poly- genetically improved ornamental qualities can be
genic inheritance of this trait, whereas the genitors of produced, as was found for the crosses between A.
these inter-generic and interspecific combinations fiebrigii var. densiseta 9 R. senilis and A. buiningi-
were noted for their large number of spines/areoles. ana 9 A. vallegardensis.
With regard to breeding programmes, particular
emphasis should be placed on the mode of inheritance Acknowledgments This study was financed by the POSDRU/
89/1.5/S/62371 project (,,Postdoctoral School of Agriculture
of basic traits, such as the length of spines, number of
and Veterinary Medicine’’, Romania).
spines/areoles, fruit colour, size and shape (Mondrag-
on-Jacobo and Bordelon 1996).
The highest values of the analysed characteristics
were noted for A. fiebrigii var. densiseta 9 R. senilis References
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