Effect of gibberellic acid on germination of seeds of five species of cacti from the Chihuahuan Desert, northern Mexico.
We determined the effect of three concentrations of gibberellic
acid on germination and photoblastic behavior of five species of
Opuntioideae from the Mapimi Biosphere Reserve, southern Chihuahuan
Desert, Durango, Mexico. For Cylindropuntia imbricata, addition of high
concentrations (1,500 ppm) of gibberellic acid gave a 30% germination
similar to the control; for Opuntia rastrera, medium concentrations
(1,000 ppm) gave <40% germination; and for O. microdasys, low
concentrations (500 ppm) gave 35% germination. High concentrations
restricted germination. Opuntia macrocentra and Cylindropuntia
leptocaulis did not differ significantly from the control. Opuntia
macrocentra required light for germination; addition of gibberellic acid
did not substitute for light. For all species, light increased
germination and the effect of gibberellic acid is species dependent,
rarely better than the control. Species we studied did not seem to have
physical dormancy and may have had physiological dormancy that was
unaffected by gibberellic acid.
Determinamos la respuesta fotoblastica y el efecto de tres concentraciones de acido giberelico en la germinacion de cinco especies de Opuntioideae de la Reserva de la Biosfera de Mapimi en el desierto Chihuahuense, Mexico. Para Cylindropuntia imbricata con la adicion de una concentration alta (1,500 ppm) se obtuvo una germinacioin de 30% similar al control; para Opuntia rastrera, con una concentracion media (1,000 ppm) se obtuvo una germinacion <40%; y para O. microdasys, con una concentracion baja (500 ppm) se obtuvo una germinacion de 35% y una concentracion media inhibio la germinacion. Opuntia macrocentra y Cylindropuntia leptocaulis no difirieron significativamente del control. Opuntia macrocentra requirio luz para su germinacion y la adicion de acido giberelico no sustituyo el requerimiento de luz. Para todas las especies estudiadas, la luz incremento la germinacion y el efecto del acido giberelico es dependiente de la especie, y en pocas ocasiones mejor que el control. las especies estudiadas no parecieron presentar latencia fiisica y posiblemente tuvieron latencia fisiologica que no fue afectada por el acido giberelico.
Gibberellins (Physiological aspects)
Cactus (Physiological aspects)
Aguilar, Karla Ma.
Mandujano, Maria C.
|Publication:||Name: Southwestern Naturalist Publisher: Southwestern Association of Naturalists Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2011 Southwestern Association of Naturalists ISSN: 0038-4909|
|Issue:||Date: Sept, 2011 Source Volume: 56 Source Issue: 3|
|Topic:||Event Code: 310 Science & research|
|Geographic:||Geographic Scope: United States Geographic Code: 1USA United States|
In some Cactaceae, recruitment is particularly difficult, either
because of low germination (Rojas-Arechiga and Vazquez-Yanes, 2000) or
inadequate establishment of seedlings (Steenbergh and Lowe, 1969; Nobel,
1984; Godinez-Alvarez and Valiente-Banuet, 1998). Therefore, detecting
mechanisms that promote germination have important implications;
especially, with regard to propagation of species for conservation and
Physiological dormancy in seeds of some plants depends on the ratio of levels of growth inhibitor (abscisic acid) and growth promoter (gibberellic acid). This has been tested in species such as Albizia grandibracteata, where three concentrations of gibberellic acid promoted germination with respect to the control (Tigabu and Oden, 2001). In seeds of Arbutus andrachne, a treatment with 250 or 500 mg/L of gibberellic acid resulted in >80% germination (Karam and Al-Salem, 2001). For plants inhabiting arid environments, some research has been done to promote germination with gibberellic acid (Ismail, 1990; Maiti et al., 1996). Plants in arid environments tend to have mechanisms that defer germination as an adaptive response to unpredictable environmental conditions (Jurado and Moles, 2003).
Results from studies of effects of gibberellic acid on seeds of cactaceae are scarce and diverse. The first studies with gibberellic acid in Cactaceae were by Alcorn and Kurtz (1959) and McDonough (1964) who demonstrated that concentrations of 500 and 1,000 ppm increased germination of seeds of Carnegiea gigantea and Stenocereus thurberi under light and dark treatments in a temperature range close to optimum. since then, experiments with other species of Cactaceae have had contrasting results (Table 1). Particularly for species of Opuntia, the difficulty of germinating seeds has been recognized since the 1960s, so several pretreatments have been used to increase germination (Pilcher, 1970; Potter et al., 1984; Trujillo-Argueta and Gonzalez-Espinosa, 1991; Mandujano et al., 1997, 2005; Pendley, 2001). Results are varied, but even acid and mechanical scarification treatments have not promoted better germination for species such as Opuntia rastrera (Mandujano et al., 2005), which probably is associated with lack of physical dormancy that has been seen in other species of Opuntia (Orozco-Segovia et al., 2007). It also has been suggested that the best way to achieve better germination is by means of an after ripening period, which suggests presence of non-deep, physiological dormancy (Baskin and Baskin, 1998; Mandujano et al., 1997). This dormancy can be overcome during dry storage (Orozco-Segovia et al., 2007). The diminished capacity in production of amylase in the aleurone from seeds apparently is due to a decrease in expression of the [alpha]-amylase genes. This reduction is associated with a decrease in the response to gibberellic acid (Bernal-Lugo et al., 1999). Deno (1994) suggested that species of Opuntia need gibberellic acid to germinate, although available data do not seem to support this idea (Table 1).
Gibberellic acid is widely used to promote germination by photoblastic seeds in the dark (Lewak and Khan, 1977). Its effect has been shown for many species that belong to several families of plants (Baskin and Baskin, 1998). Again, results for cactaceae are as diverse as the number of species used in trials (Brencher et al., 1978; Zimmer and Buttner, 1982; Arias and Lemus, 1984; Trejo Hernandez and Garza Castillo, 1993; Zimmer, 1998; Rojas-Arechiga et al., 2001; Ortega-Baes and Rojas-Arechiga, 2007; Rojas-Arechiga, 2008).
We determined the effect of giberellic acid on germination with seeds undergoing an ageing process in five species of Opuntioideae that occur sympatrically in the southern chihuahuan Desert. We also studied photoblastic behavior in all species to determine the effect of addition of gibberellic acid at three concentrations under light and dark conditions. Species studied were Cylindropuntia leptocaulis, C. imbricata, Opuntia rastrera, O. macrocentra, and O. microdasys. In 1996, we collected seeds from ripe fruits of these five species in the Mapimi Biosphere Reserve in the chihuahuan Desert of Durango, Mexico (26[degrees]29-52'N, 103[degrees]32-58'W; mean annual precipitation, 227 mm; mean annual temperature, 21[degrees]C; Montana and Breimer, 1988). Seeds were extracted from fruits and pulp residues were removed from seeds, which were then air dried at room temperature and stored in paper bags at room temperature until onset of the experiment (9 years after harvest). This period corresponds to prior experiments with O. rastrera, demonstrating that seeds do not germinate unless they undergo an after-ripening period of [greater than or equal to]1 year. Percentages of germination remain high (45% in 12L:12D photoperiod and a constant 25[degrees]C temperature) even after 12 years in storage (Aguilar-Morales, 2005); thus, seeds remain viable for a long time. seeds were sown in Petri dishes with 1% agar and we added three concentrations of gibberellic acid (500, 1,000, and 1,500 ppm) and a control (no addition of gibberellic acid). We used four replicates of 25 seeds/Petri dish/treatment. Four replicates each containing 25 seeds/Petri dish were used to test for photoblastism, each Petri dish was wrapped within two layers of aluminum foil and kept in total darkness until the end of the experiment. Experimental units were placed in a germination chamber (Conviron CMP3000; Controlled Environments Limited, Winnipeg, Manitoba, Canada) at 25[degrees]C and a 12L:12D photoperiod. The experiment was followed daily for 4 months and we considered a seed to be germinated once the radicle appeared.
Results were analyzed adjusting a generalized-linear model on the number of germinated seeds with JMP version 6.0, assuming a binomial error distribution (Crawley, 2002). Total percentages of germination were contrasted among species. In addition, separate analyses for each species were fitted as we detected great variation in germination between species in response to addition of gibberellic acid.
Mean proportions of seeds that germinated differed among species ([chi square] = 70.64, df = 4, P < 0.001; Fig. 1a). The greatest proportions of germinated seeds were for O. rastrera and the lowest for O. macrocentra. The only difference was the low proportion of germination by seeds of O. macrocentra; all other species did not differ in germination (P > 0.05). In the photoblastic experiment, we detected consistent significant effects of light ([chi square] = 174.37, df = 4, P < 0.001; Fig. 1b) for all species implying that they germinate at higher proportions under light conditions. The significant species-light interaction ([chi square] = 20.87, df = 4, P < 0.001) only suggests high variation among species that require light. We detected neither a significant effect of concentration of gibberellic acid ([chi square] < 0.01, df = 3, P > 0.999) nor a light-gibberellic acid concentration ([chi square] = 0.04, df = 3, P > 0.998), meaning that under both light conditions germination of seeds behaved similarly. There was, however, a significant effect of gibberellic acid by species ([chi square] = 55.48, df = 12, P < 0.001) suggesting different responses of species to concentrations of gibberellic acid (Figs. 2 and 3). Opuntia macrocentra exhibited no germination under dark conditions suggesting strict photoblastic behavior for seeds of this species.
[FIGURE 1 OMITTED]
The concentration of gibberellic acid seems to have species-specific responses (Figs. 2 and 3) and was significant for only two species (C. imbricata: [chi square] = 18.47, df = 3, P < 0.01; O. microdasys: [chi square] = 34.65, df = 3, P < 0.01) under light conditions and for three species under dark conditions (O. imbricata: [chi square] = 7.88, df = 3, P = 0.048; O. rastrera: [chi square] = 12.23, df = 3, P = 0.066; O. microdasys: [chi square] = 29.42, df = 3, P < 0.001). A similar pattern for both light treatments was detected for C. imbricata and O. microdasys (Figs. 2 and 3). For these two species, low and high concentrations increased germination with respect to the control, and for O. microdasys, concentrations of gibberellic acid of 1,000 ppm inhibited a proportion of seeds germinating in dark conditions. However, low concentrations of gibberellic acid significantly promoted higher germination in O. microdasys ([chi square] = 14.07, df = 1, P < 0.01) for both light treatments. The highest concentration significantly increased germination in C. imbricata ([chi square] = 8.33, df = 1, P < 0.01) under light conditions, as compared to the control. The addition of gibberellic acid in C. leptocaulis, O. rastrera, and O. macrocentra had no apparent effect on germination with respect to the control (P > 0.05 for the three cases; Fig. 2), except for O. rastrera under dark conditions (Fig. 3). Even under control conditions, O. macrocentra had low overall germination. The proportion of germination for the five species was low (<0.5), which is consistent with other species of Opuntia (Pilcher, 1970; Trujillo-Argueta and Gonzalez-Espinosa, 1991; Pendley, 2001). In particular, the low proportion of seeds of O. macrocentra that germinated also was detected for 1-year-old seeds (Mandujano et al., 2007b), so viability can be discarded partially as a factor responsible for the low rate of germination. Although viability of seeds was not quantified in our study and may be confounding our results, and the interpretation of our results cannot be entirely ascribed to our treatments, standard assays for testing viability of seeds (e.g., tetrazolium) may not be reliable in seeds that have deep dormancy because of low levels of respiration. In addition, seeds of Opuntia have high viability (Gimeno and Vila, 2002; Orozco-Segovia et al., 2007), so we assume that much of the differences we observed may be due to our treatments. Opuntia macrocentra probably is facing a more serious problem than other species of Opuntioideae, as recruitment is mainly through seeds that have low percentages of germination, and germination does not seem to be enhanced by gibberellic acid. The first factor partially could explain the absence of seedlings in long-term demographic studies (Mandujano et al., 2007a). Our results are also the first reports of germination of seeds within Cylindropuntia; these two species seem to behave like Opuntia. The addition of gibberellic acid in the Opuntioideae we studied had contrasting results. Only a high concentration of gibberellic acid affected seeds of C. imbricata. Within Opuntia, only one of the species responded to addition of gibberellic acid. Opuntia rastrera and O. macrocentra did not respond to addition of gibberellic acid under light conditions and only O. rastrera showed a positive effect of gibberellic acid under dark conditions. Positive responses were detected for O. microdasys at low concentrations. Lack of effects of gibberellic acid in some concentrations, especially in O. macrocentra, compared to the control are consistent with results of other species of Opuntia (Williams and Arias, 1978; Olvera-Carrillo, 2001), but contrast with results for O. joconostle (Sanchez-Venegas, 1997). This may be due to O. joconostle (and other species of Cactaceae where gibberellic acid enhanced germination) previously being imbibed in distilled water, which could be confounding the effect of gibberellic acid. In general, results of other studies suggest that the increase in percentage of germination with gibberellic acid may be promoted by the previous treatment of the seeds (i.e., scarification or imbibition), rather than the effect of gibberellic acid. Our results led us to conclude that there is no clear pattern of the effect of gibberellic acid on germination of seeds within Cactaceae. In a previous study with seeds of O. rastrera, the only mechanism that overcame dormancy was an after ripening period, neither mechanical scarification nor acid scarification gave better results than ageing (Mandujano et al., 2005), which is consistent with what Orozco-Segovia et al. (2007) have suggested about the lack of physical dormancy in the Opuntia. Results obtained here and in other studies of Opuntia (Mandujano et al., 1995; Orozco-Segovia et al., 2007) suggest that these species do not have physical dormancy, although the trait would be favored in arid environments. The best way to promote germination could be an after-ripening period (for some species), which would be consistent with seeds of Opuntioideae being able to form persistent seed banks (Mandujano et al., 1997; Montiel and Montana, 2003).
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
The common belief that gibberellic acid is a promoter of germination may not hold for Cactaceae. Instead, treatments that trigger germination may be more related to environmental cues than to biological attributes.
Financial support was provided by Secretaria de Medio Ambiente y Recursos Naturales Consejo Nacional de Ciencia y Tecnologia 0350 to MCM and Consejo Nacional de Ciencia y Tecnologia 83790 and a sabbatical leave grant to JG. This paper was completed while on sabbatical leave at New Mexico State University with B. Milligan, we greatly appreciate the discussions and space in his laboratory.
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Submitted 4 September 2008. Accepted 15 April 2011.
Associate Editor was David B. Wester.
MARIANA ROJAS-ARECHIGA, KARLA MA. AGUILAR, JORDAN GOLUBOV, AND MARIA C. MANDUJANO *
Instituto de Ecologia, Departamento Ecologia de la Biodiversidad, Universidad Nacional Autonoma de Mexico, Apartado Postal 70-275, Ciudad Universitaria, 04510 Mexico, Distrito Federal, Mexico (MRA, KMA, MCM)
Universidad Autonoma Metropolitana, Departamento El Hombre y Su Ambiente, Calzada Del Hueso 1100, Colonia Villa Quietud, Coyoacan, 04960, Mexico Distrito Federal, Mexico (JG)
* Correspondent: firstname.lastname@example.org
TABLE 1--Studies of Cactaceae in which germination has been assessed using different treatments with gibberellic acid. Taxon Treatment Astrophytum capricorne, Scarification plus gibberellic Leuchtenbergia principis, acid at 0.1% Echinocactus grusonii Opuntia joconostle Imbibition during 30 min in a 40-ppm solution of gibberellic acid Sclerocactus mariposensis Scarification plus imbibition for 18 h plus gibberellic acid at 0.5% Myrtillocactus geometrizans, 500 and 2,000 ppm of Mammillaria ritteriana gibberellic acid Arequipa erectocylindrica, 500 and 1,000 ppm of Eulychnia longispina, gibberellic acid Eulychnia castanea Cereus Soaking seeds for 30 min in 100-200 ppm of gibberellic acid Cereus griseus 0.001M gibberellic acid Rebutia minuscula, 500, 1,000, and 1,500 ppm Pachycereus hollianus of gibberellic acid Oreocereus maximus, 500, 1,000, and 2,000 ppm Oreocereus celsianus, of gibberellic acid Notocactus leninghausii, Epiphyllum anguliger Opuntia tomentosa 1,000 ppm of gibberellic acid Notocactus submammulosus 10-100 mg/L of gibberellic acid Trichocereus terscheckii 500 and 1,000 ppm of gibberellic acid Opuntia rastrera, Opuntia 200 ppm of gibberellic microdasys, Opuntia acid macrocentra Mammillaria haageana, 500 and 1,000 ppm Mammillaria mystax, of gibberellic acid Mammillaria supertexta, Mammillaria carnea Effect of gibberellic Taxon acid Source Astrophytum capricorne, Positive De la Rosa-Ibarra Garcia Leuchtenbergia principis, response and Garcia (1994) Echinocactus grusonii Opuntia joconostle Positive Sanchez-Venegas (1977) response Sclerocactus mariposensis Positive Moreno et al. (1992) response Myrtillocactus geometrizans, Positive zimmer and Buttner (1982) Mammillaria ritteriana response Arequipa erectocylindrica, Positive zimmer and Buttner (1982) Eulychnia longispina, response Eulychnia castanea Cereus Positive Krulik (1981) response Cereus griseus Negative Williams and Arias (1978) response Rebutia minuscula, Negative Brencher et al. (1978) Pachycereus hollianus response Oreocereus maximus, Negative zimmer and Buttner (1982) Oreocereus celsianus, response Notocactus leninghausii, Epiphyllum anguliger Opuntia tomentosa No response Olvera-Carrillo (2001) Notocactus submammulosus No response Shimomura et al. (2000) Trichocereus terscheckii No response Ortega-Baes and Rojas- Areichiga (2007) Opuntia rastrera, Opuntia No response Mandujano et al. (2007b) microdasys, Opuntia macrocentra Mammillaria haageana, No response Rojas-Arechiga (2008) Mammillaria mystax, Mammillaria supertexta, Mammillaria carnea
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