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Euphytica

, Volume 184, Issue 3, pp 369–376 | Cite as

The plant size and the spine characteristics of the first generation progeny obtained through the cross-pollination of different genotypes of Cactaceae

  • Lucica MihalteEmail author
  • Radu E. Sestras
Article

Abstract

The main characteristics (plant diameter, number of spine/areoles and length of spines) of 16 cactus hybrids were analysed and the genetic variability and broad-sense heritability was studied. The descendants were obtained through a cyclic cross-pollination pattern, with the parental forms chosen based on aesthetic considerations. Cross-pollination among Rebutia senilis × Aylostera muscula, Rebutia tarvitaensis × Aylostera muscula, Aylostera flavistyla × Rebutia senilis, Rebutia senilis × Aylostera flavistyla, Aylostera muscula × Aylostera albiflora and Rebutia senilis × Aylostera albiflora did not succeed, whereas all of the other hand-pollinated crosses succeeded and produced viable seeds. The highest values of the analysed characters were observed in the progeny of A. fiebrigii var. densiseta × R. senilis and A. buiningiana × A. vallegardensis and the artificial selection to identify plants with special decorative traits was extremely efficient among them. In the F1 population of the studied crosses, a large genetic diversity was found within hybrid combinations (families), between combinations and a different variation was recorded among the analysed traits. The broad-sense heritability ranged between 0.909 (plant diameter) and 0.948 (spines length). All of the characters analysed, in the present experience, have a strong genetic determinism, being greatly influenced by the genotype and to a lesser extent, by the cultivation conditions (greenhouse).

Keywords

Cactaceae F1 hybrids Interspecific hybridisation Inter-generic hybridisation Genetic diversity 

Introduction

The Cactaceae family (order Caryophyllales) includes plants with perennial photosynthetic succulent stems, spines produced on modified axillary buds (termed areoles) and colourful flowers with numerous stamens.

The multiple uses and the ability of cacti to thrive in the arid and semiarid environments that other species are unable to tolerate make it of interest to breeders and molecular biologist seeking to develop crops for areas typically unsuitable for conventional agriculture (Nobel 2002). A primary breeding goal should be the expansion of the production area for cacti by developing cold-tolerant cultivars because the current high-yielding fruit, vegetable and forage varieties do not survive between temperatures of −5 and −8°C (Loik and Nobel 1991; Parish and Felker 1995; Wang et al. 1998).

The genetic diversity in cultivated cacti is limited by the small number of progenitors and the loss of genetic variation during cultivation (Nobel 2002) and most of the domesticated cacti grown for fruit or ornamental flowers apparently originated from a relatively narrow germplasm base. In the case of Eastern cactus, over 100 distinct clones have been described, but Meier (1995) proposed that all are probably the descendants of three plants (two Hatiora gaertneri and one H. rosea).

Cacti are threatened by the loss and degradation of their habitat and illegal collection (Oldfield 1997; Boyle and Anderson 2002); the most important factor causing the loss of biodiversity is intensive land use (Zak et al. 2004). The “Red List” of threatened species of the International Union for the Conservation of Nature (IUCN) provides a categorised list of species based on their relative risk of extinction at a global scale; the list includes at least 104 cacti species (7% of all species) as vulnerable to extinction (IUCN 2008).

The majority of the studies regarding cacti hybridisation have been restricted to the Opuntioideae subfamily and little is known about the role of hybridisation on Cactoideae, a more diverse subfamily (Machado 2008). Therefore, in the present research, we chose species from the Aylostera and Rebutia genera and therefore, the aim of this study was to identify potential genitors for breeding programs and to improve the genetic diversity, which will permit an efficient selection of new cultivars.

Materials and methods

Plant material and growth conditions

The Cactaceae species used in the present research were grown in the greenhouse complex at the “Alexandru Borza” Botanical Garden of Cluj-Napoca, Romania. This Cactaceae collection comprises more than 4100 specimens belonging to 115 genera from the 241 total known according to the Backeberg system (1968–1977).

Based on aesthetic considerations (shape of plant, flower diameter and colour of flowers), we chose 19 genotypes as the genitors for the interspecific and inter-generic hybridisations (Table 1).
Table 1

The main traits of the parental genotypes

Species

Plant shapea

No. spines/areoles and length of spines

Flower diameter (cm)

Flower 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

aAll of the values represented the arithmetic mean

The hybrid seeds were sown in small pots in a mixture, composed of three parts of sterilised fibrous soil, one part peat moss and one part washed sand (Hewitt 1993) and were grown in the Botanical Garden Cluj-Napoca, Romania. The seeds were free of chemicals and fertiliser. In December, the minimum temperature dropped to 5°C and the maximum temperature reached 23.48°C in July.

Experimental design and statistical analyses

Using a cyclic hybridisation pattern, 14 interspecific combinations (between two species of the same genus) and 16 inter-generic combinations (between two plants belonging to two different genera) was achieved.

To isolate a cross-pollinated flower from the possibility of contamination by the pollen from other plants and to distinguish the differences between hybrid and non-hybrid fruits, each flower was insulated individually with sticky paper and different colours of thread were used for each flower (Mondragon-Jacobo and Bordelon 1996).

A total of ten plants were pollinated for each combination and every plant contained approximately ten flowers. Hybrid seeds were obtained from 12 interspecific and 12 inter-generic combinations and ten seeds were sown/pot. Viable F1 progeny were obtained in 16 hybrid families and the plants were analysed in the first year of vegetative growth (Fig. 1). The low proportion of seed germination can be explained by the different growth forms of cacti: columnar cacti have a higher rate of seed germination than globular cacti (Ortega-Baes et al. 2010). Aylostera and Rebutia species are globular cacti and it is also possible that their seeds experience a dormancy period (Mihalte et al. 2010).
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)

The experiment was structured following a completely randomised (CR) design with three replications for each analysed trait (plant diameter, number of spine/areoles and length of spines). The differences in the characteristics of the progeny were analysed statistically using ANOVA, where the mean of the experiment was the control and the coefficient of variability (CV%) for traits was computed. The data are presented as the means and standard deviations for each cyclic hybridisation.

Genetic parameters

The main characteristics of the F1 hybrids inform the interspecific and inter-generic hybridisation were calculated and are discussed in terms of the coefficients of variability within each hybrid family. The uniformity of the traits was computed based on the following coefficients: CV% < 10%-low variability; 10% < CV% < 20%-medium variability and CV% > 20%-high variability (Reed et al. 2002; Sestras et al. 2009).

To determine the genetic proportion in the phenotypic expression of the studied characteristics, the coefficient of heritability was also calculated, where the individual of the F1 of a cross was the observational unit. The broad-sense heritability was noted and computed by a classical model, H2 = σG2/σP2, where σG2 is the genotypic variance and σP2 is the phenotypic variance (Holland et al. 2003; Piepho and Möhring 2007; Sestras et al. 2008).

Results

The cross-pollination of parental forms

The cross-pollinations among Rebutia senilis × Aylostera muscula, Rebutia tarvitaensis × Aylostera muscula, Aylostera flavistyla × Rebutia senilis, Rebutia senilis × Aylostera flavistyla, Aylostera muscula × Aylostera albiflora, Rebutia senilis × Aylostera albiflora were unsuccessful (Table 2). All of the other artificial hybridisations were successful and produced viable seeds; however, a viable F1 generation was obtained in only 16 hybrid combinations. The parental genotype, Aylostera fiebrigii, has been reported to present a small capacity of germination when it has been used for studying the germination percentages of different cacti species (Mihalte et al. 2009).
Table 2

Hybrid combinations and results of hybridisations

No.

Mother genotype (♀)

Father genotype (♂)

Results of hybridization (fruits and seeds)

Viable F1 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

The plant diameter

The plant diameters of the progeny were variable (Table 3), with the average of the F1 hybrids in the studied families varying significantly compared with the control.
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 (cm)

CV%

No. of spines/ areolas

CV%

The length of spines (mm)

CV%

1.

R. cajasensis × R. senilis

2.6 ± 0.1

8.4

14.5 ± 6.2°°°

8.9

20.0 ± 4.2*

11.3

2.

R. senilis × 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 × R. spegazziana

1.8 ± 0.8°°

11.9

22.5 ± 1.8

5.7

17.2 ± 1.4

9.8

4.

A. buiningiana × A. vallegardensis

3.3 ± 0.8**

23.0

15.5 ± 5.2°°°

13.4

20.6 ± 4.8*

9.4

5.

A. muscula × A. vallegardensis

3.2 ± 0.7**

13.3

23.5 ± 2.8**

5.5

9.6 ± 6.3°°

17.7

6.

A. fiebrigii × A. vallegardensis

2.5 ± 0.0

19.0

20.5 ± 0.2

6.3

26.2 ± 10.4***

13.8

7.

A. muscula × A. buiningiana

2.6 ± 0.1

8.6

22.5 ± 1.8

5.7

9.8 ± 6.0°°

13.6

8.

A. spinosissima × A. albiflora

3.6 ± 1.1***

8.2

23.3 ± 2.6**

11.8

15.5 ± 0.3

13.6

9.

R. cajasensis × 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 × R. senilis

2.4 ± 0.2

11.3

27.8 ± 7.1***

6.2

27.1 ± 11.3***

11.3

11.

A. muscula × 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 × R. kupperiana var. spiniflorum

2.2 ± 0.3

24.7

21.5 ± 0.8

6.0

12.8 ± 3.0

23.8

13.

R. cajasensis × A. archibuinigiana

2.1 ± 0.4

12.3

17.5 ± 3.2°°°

11.9

8.5 ± 7.4°°°

37.5

14.

R. senilis × A. archibuinigiana

1.9 ± 0.6°

28.2

19.8 ± 0.9

8.6

14.4 ± 1.4

18.7

15.

R. donaldiana × A. buiningiana

2.4 ± 0.1

17.7

20.8 ± 0.1

10.7

18.2 ± 2.4

28.8

16.

R. cajasensis × 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)

High values of plant diameter, suggesting high vigour, presented in the hybrids of the following combinations: R. senilis × R. kupperiana var. spiniflorum, A. buiningiana × A. vallegardensis, A. muscula × A. vallegardensis. In general, the hybrids derived from the interspecific combinations were more vigorous than the hybrids from the inter-generic combinations.

The following different variations of characteristics in the F1 populations were noted: a low variability among the hybrids of R. cajasensis × R. senilis and R. senilis × R. kupperiana var. spiniflorum; a large variability for the A. narvaecensis × R. kupperiana var. spiniflorum and R. senilis × A. archibuinigiana hybrid family and a medium variability for the remainder of the hybrid combinations.

The number of spines/areoles

The variability of the number of the spines/areoles in the F1 hybrids was quite small; only the combinations A. buiningiana × A. vallegardensis and R. cajasensis × A. archibuinigiana presented hybrids with a medium variability of this trait (Table 3).

Compared with the mean of experience (21.0), the number of spines/areoles in the F1 hybrids showed positive values for the following crosses: A. fiebrigii var. densiseta × R. senilis, A. muscula × R. kupperiana var. spiniflorum, A. muscula × A. vallegardensis and A. spinosissima × A. albiflora. Of all of the hybrid combinations, the lowest number of spines/areoles was recorded for the hybrids derived from R. cajasensis × R. senilis and A. buiningiana × A. vallegardensis. Regarding the genitors, the smallest number of spine/areoles was recorded in R. cajasensis and A. archibuinigiana species and it appears that this characteristic was transmitted to the F1 progeny derived from these crosses.

The length of spines

Very small spines presented the hybrids of the following crosses: R. cajasensis × A. muscula, R. cajasensis × A. archibuinigiana and A. muscula × A. vallegardensis (Table 3).

The results showed that when R. cajasensis and A. archibuinigiana were used as the genitors, the length of the spines was transmitted to the progeny with sufficient fidelity and the hybrids progeny inherited the small number of spines/areoles. A. fiebrigii and A. vallegardensis, both having longer spines than most of the studied species, passed this trait to their descendants.

The variability and the heritability of the analysed traits

The obtained data showed the existence of a large diversity, where the resulting variability was manifested within the hybrid combinations (families) and between the combinations. We also found a different variation based on the characteristic that was analysed (Fig. 2).
Fig. 2

The variability and the broad-sense heritability of the studied characteristics in the first-generation progeny (F1)

The lowest coefficient of variability was recorded for the number of spines/areoles (18.0%), whereas a wide variability was recorded for the plant diameter (26.9%) and length of spines (38.4%). Therefore, the CV% values indicate that it is possible to identify hybrids with small plant diameters and small lengths of spines and with large plant diameters and large lengths of spines in any combination (both forms are suitable for new ornamental forms).

The broad-sense heritability (Fig. 2) ranged between 0.909 (plant diameter) and 0.948 (spine 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 degree, by the culture medium (greenhouse).

Discussion

The ability of pollen to germinate is an important aspect in cross-pollination (Oyiga et al. 2010). In previous studies, the pollen germination ability of the parental plants used in this study was investigated and detected as being high (Mihalte et al. 2010). Even with a high percentage of viable pollen, the cross-pollination between Aylostera flavistyla and Rebutia senilis did not succeed with using Aylostera flavistyla as either the male or female parent. Thus, Aylostera flavistyla can be considered incompatible, as can Hatiora (Boyle et al. 1994) and Schlumbergera (Boyle 1997). In addition, manual cross-pollination using wild Stenocereus stellatus failed between some domesticated and wild genotypes, suggesting a pollen incompatibility (Casas et al. 1999). The hybridisation experiments by Hentzschel and Hentzschel (2001) of Sulcorebutia, Weingartia, Rebutia and Echinopsis have produced the following results: most of the hybridisation failed between Sulcorebutia and Rebutia padcayensis, even though the latter closely resembles Sulcorebutia and with several other Rebutia species. For other genera (Selenicereus and Hylocereus), inter-generic crosses appear to be a successful approach to increase diversity. Tel-Zur et al. (2003) obtained triploid, pentaploid, hexaploid and aneuploid hybrids in inter-generic crosses (Selenicereus and Hylocereus). However, Lichtenzveig et al. (2000) reported viable hybrids from inter-generic and interspecific crosses between Selenicereus and Hylocereus.

High vigour, as observed for R. senilis × R. kupperiana var. spiniflorumand and A. buiningiana × A. vallegardensis, is of considerable importance to breeders, especially for the Rebutia genus, which are generally small (Pilbeam 1997). For breeders, vigour correlates with increased photosynthetic area and improved root anchorage (Mondragon-Jacobo and Bordelon 1996).

McIntosh (2002) correlated vigour with the size of the plants for species of Ferocactus and showed that large plants grow more than small plants. However, in terms of percent change in volume, the relationship was the opposite: large plants grew less as a percent of size than small plants. In addition, the number of flowers produced by a plant was significantly and positively correlated with the size of the plant, but the flower abortion rates (Burd 1998) and the number of seeds per fruit were not influenced by this factor.

The study of the seminal progeny obtained from hand-pollination showed that central spines lack in F1 hybrids, as they do in their parents. For most crop cacti, the presence of spines is an inconvenience and significant efforts to develop new cultivars are focused on spineless cultivars (Mondragon-Jacobo and Bordelon 1996). For ornamental cacti, as are the species described here, the presence of spines is a positive element for their decorative traits. Peharec et al. (2010) evaluated the spines of pot-grown Mammillaria plants and in vitro-regenerated shoots and found that the pot-grown plants had 16–17 spines per areole, whereas the in vitro-grown shoots were normal but displayed a lower number of spines (11–12). Parra et al. (2010) argued that genetic diversity should be conserved and should be promoted by artificial selection, which, despite the high levels of gene flow, moderate the genetic structure between wild and managed populations.

A. fiebrigii var. densiseta × R. senilis, A. muscula × R. kupperiana var. spiniflorum and A. muscula × A. vallegardensis presented a large number of spines/areoles. The obtained results suggest the polygenic inheritance of this trait, whereas the genitors of these inter-generic and interspecific combinations were noted for their large number of spines/areoles. With regard to breeding programmes, particular emphasis should be placed on the mode of inheritance of basic traits, such as the length of spines, number of spines/areoles, fruit colour, size and shape (Mondragon-Jacobo and Bordelon 1996).

The highest values of the analysed characteristics were noted for A. fiebrigii var. densiseta × R. senilis and A. buiningiana × A. vallegardensis and the artificial selection to identify plants with special decorative traits was extremely effective for these combinations. It is possible that these results may be due mainly to the influence of the female parent, but we do not exclude the possible effects of the male genitor and of course, those caused by the environmental conditions, culture and interactions between the genotype and ecotype.

The high genetic variability shown in the present research allows an efficient selection, but further investigation should be performed by examining the levels of allozyme variation and the genetic structure (Figueredo et al. 2010).

For most cross-pollinations, as was the case of the cactus species described here, the efficiency of phenotypic selection is decisively affected by the size of the heritability coefficient (Leite et al. 2006). Thus, the phenotypic selection for all of the studied characters in the populations represented by the F1 hybrids can be efficient.

Because the inheritance from genitors and the fixing of such characteristics was possible in the F1 hybrid descendants, studies of cacti germplasm to perform artificial variability followed by artificial selection are absolutely justified and extremely useful to obtain new varieties. The obtained results are encouraging findings, which indicate that the studied characteristics are, overall, under strong genetic control and that a genotype with a given performance could be selected and genetically improved. The narrow-sense heritability and the additive genetic variance have not been studied in this experience because these aspects are inappropriate for hybrids, owing to the genetic disequilibrium inherent in their origin (Gordon 1999).

The obtained results indicate that through artificial hybridisation under a suitable choice of genitors, progeny with major features for selection that have genetically improved ornamental qualities can be produced, as was found for the crosses between A. fiebrigii var. densiseta × R. senilis and A. buiningiana × A. vallegardensis.

Notes

Acknowledgments

This study was financed by the POSDRU/89/1.5/S/62371 project („Postdoctoral School of Agriculture and Veterinary Medicine”, Romania).

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Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Genetics and Plant BreedingUniversity of Agricultural Science and Veterinary MedicineCluj-NapocaRomania

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