Pollen morphology and fertility of wild Atlas pistachio (Pistacia atlantica Desf., Anacardiaceae)

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1 Grana ISSN: (Print) (Online) Journal homepage: Pollen morphology and fertility of wild Atlas pistachio (Pistacia atlantica Desf., Anacardiaceae) Safia Belhadj, Arezki Derridj, Laure Civeyrel, Charles Gers, Thierry Aigouy, Thierry Otto & Thierry Gauquelin To cite this article: Safia Belhadj, Arezki Derridj, Laure Civeyrel, Charles Gers, Thierry Aigouy, Thierry Otto & Thierry Gauquelin (7) Pollen morphology and fertility of wild Atlas pistachio (Pistacia atlantica Desf., Anacardiaceae), Grana, 46:3, 148-6, DOI:./17313 To link to this article: Published online: 2 Nov 7. Submit your article to this journal Article views: View related articles Citing articles: 2 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 12 December 17, At: 2:9

2 Grana, 7; 46: Pollen morphology and fertility of wild Atlas pistachio (Pistacia atlantica Desf., Anacardiaceae) 6 SAFIA BELHADJ 1, AREZKI DERRIDJ 2, LAURE CIVEYREL 3, CHARLES GERS 3, THIERRY AIGOUY 4, THIERRY OTTO & THIERRY GAUQUELIN Institut d Agropastoralisme, Centre Universitaire de Djelfa, Ain Chih, Djelfa, Algeria, 2 Laboratoire de Biosystématique Végétale, Faculté des Sciences Biologiques et Agronomiques, Université Mouloud Mammeri, Tizi-Ouzou, Algeria, 3 UMR 24, Laboratoire d Ecologie Fonctionnelle, Bat. IV R3, Université Paul Sabatier, Toulouse, France, 4 Laboratoire des Mécanismes et des Transferts en Géologie, Service de Microscopie Electronique et de Microsonde Electronique, Université Paul Sabatier et INP, Toulouse, France, Laboratoire d Ecologie Fonctionnelle, UMR 24, Université Paul Sabatier, Marvig, Toulouse, France, and 6 Institut Méditerranéen d Ecologie et de Paléoécologie, UMR CNRS 6116, Université de Provence, Marseille, France. Abstract Pollen morphology and fertility in different populations of Pistacia atlantica from Algeria have been examined by light and scanning electron microscopy. Characteristics such as the shape and size of the pollen grains, the number of apertures, and the exine surface were recorded for each site for comparison. The pollen grains of Pistacia atlantica are consistently spheroidal to prolate spheroidal and pantoaperturate. The exine ornamentation is reticulate. Significant differences in pollen size and number of apertures were observed between the different sites. The fertility of pollen from different sites was estimated using the acetocarmine staining method and show that mean percentage of fertile pollen is high but varied among the sites with highest value (99.7%) at the Berriane site and lowest value (9.9%) at the Messaad site. Keywords: Pollen morphology, Pistacia atlantica, variation, aperture number, pollen fertility Intense germ plasm erosion is underway in the semiarid, arid and Saharian areas due to human activities (Quezel & Santa, 1963). Initiatives have been taken to conserve and propagate pre-saharian and Saharian genetic resources. The Atlas pistachio (Pistacia atlantica Desf.) is one of the species considered in this initiative, but very little information is available about the ecological adaptation of this species. Due to the lack of information, intraspecific variation is poorly understood and there is also limited knowledge about distribution of characters within the wide-ranging populations. Pistacia atlantica (Anacardiaceae) is a dioecious tree, widely distributed in Algeria from the Mitidja plains to the Saharian regions (Monjauze, 19). This drought-tolerant tree, with an extensive root system, has been the subject of several studies aimed at selecting ecotypes best-adapted to present weather and soil conditions. In addition to its ecological use in reforestation programmes and land preservation it has the advantage of being a good root stock and a good pollinator for the economic important Pistacia vera (Crossa-Raynaud, 1984; Isfendiyaroglu et al., 1; Ozeker et al., 6). The pollen morphology of the genus Pistacia has previously been described and illustrated in several studies (Erdtman, 192; Haddad, 1969; Alyafi, 1979; Diez, 1987; El-Oqlah, 1996). However, very few palynological studies have focused on the morphology and structure of the pollen from the Algerian Atlas pistachio. Pollen morphology from two different populations from Algeria was studied by Alyafi (1979), who also made a general comparison with pollen from populations in other countries Correspondence: Safia Belhadj, Institut d Agropastoralisme, Centre Universitaire de Djelfa, B.P.3117 Poste Ain Chih, Djelfa, Algeria. belhadjsafia@yahoo.fr (Received February 7; accepted 12 June 7) 1 ISSN print/issn online # 7 Taylor & Francis DOI:./17313 Grana gra d 24//7 18::28 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) 21897

3 Grana gra d 24//7 18:: The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) Pistacia atlantica pollen morphology 149 Table I. Main climatic features of the selected experimental sites. Sites Latitude Longitude Altitude (m) Q 3 Climate type Berriane (Be) 32 19N 3 469E Saharian fresh El Hamel (E) 3 99N 4 49E Arid mild Messaad (M) N 3 369E Arid fresh Ain Oussera (Ao) 3 29N 2 9E Arid fresh Aflou (Af) 34 99N 2 9E 9 3. Semi-arid cold Djelfa (Dj) N 3 9E Semi-arid fresh 6 Q 3 : Emberger quotient (aridity quotient). Source of climatic data: National Meteorology Office of Algeria. 2 3 Pollination is one of the most important factors in the Pistacia species; male trees tend to shed pollen before female flowers are receptive. In the case of insufficient pollination, blank nuts form, a situation that creates two kinds of problems: an economic problem (1), since the yield is reduced in P. vera (Ozeker et al., 6); and a physiological problem (2) for the regeneration processes, since the amount of germinating seeds is reduced in such plants. When natural pollination is not sufficient, artificial pollination can be applied as a substitute (Isfendiyaroglu et al., 1) and all Pistacia species can pollinate and fertilize each other. From the point of view of agriculture, as well as pollination biology, it is extremely important to control the fertilisation capacity and the quality of temporarily stored pollen (Nepi & Franchi, ). As Pistacia atlantica, is used as a pollinator for P. vera, it is critical to estimate pollen fertility in this species. Therefore, this study investigated in detail the pollen morphology, particularly in relation to pollen fertility, grain size, apertures and exine ornamentation of six different wild Pistacia atlantica populations using light (LM) and scanning electron microscopy (SEM). This paper is the first contribution to the description of the pollen morphology of Algerian Pistacia atlantica grown under different climatic conditions and is intended to serve as a reference study along with previous studies to clarify variations within this species. Material and methods The investigations were carried out on pollen samples from six different origins (Table I, Figure 1) obtained from living specimens in wild populations in Algeria, selected such as to cover a wide climatic variation. The flower clusters were sampled from a minimum of five male trees at the beginning of the flowering period. The flower clusters were isolated and dried in laboratory conditions; and the pollen grains were then collected and kept at 4C for one month. The pollen grains were prepared for light (LM) and scanning microscopy (SEM) by standard acetolysis (Erdtman, 192). For LM, the pollen was mounted in unstained glycerine jelly. The values given are based on the measurements of 2 pollen grains from each site. Morphological observations, including shape, size (long diameter, D and short Figure 1. Position of sampling sites and their climatic zones (According to Stewart, 1974). 1

4 Grana gra d 24//7 18::33 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) S. Belhadj et al. 2 3 diameter, d), D/d ratio and number of apertures ( measurements in total) were made using a Zeiss light microscope (). The acetolyzed pollen grains were conserved in absolute ethanol until used for SEM studies. Measurements for D and d, as well as for the D/d ratio, were made according to Erdtman s (192) and Alyafi s (1979) methods, measuring the longest diameter (D) and the shortest diameter (d). For SEM observations, non-acetolyzed and acetolyzed pollen grains were placed directly on stubs and coated with carbon. Four stubs were prepared for each site, two for each acetolyzed and non-acetolyzed pollen grains, to give 24 stubs in total. The detailed exine surface ornamentation, pollen shape and aperture characteristics were examined using a JEOL. JSM-63 LV- Japan SEM and micrographs were digitally recorded at different magnifications. The pollen terminology in general follows Punt et al. (1999). The acetocarmine staining method (Wodehouse, 193; Shaheen, 4) was applied to determine the presence of cytoplasm in intact pollen grains and the counts were used as an approximation for pollen viability. Twenty slides were prepared for each site. Each slide was divided into areas of 1 cm 2 and randomly divided onto four areas. On each of the four areas, three fields were randomly selected and fertile and sterile pollen grains were then recorded in each field using a compound microscope at x magnification (1 4 fields in total). The data were subjected to one-way ANOVA and the mean separation was made with the Tukey test to determine whether the differences were significant or not, using Statistix analytical software (version 1., 1996). Results Pollen shape and size The pollen grains were relatively uniform in shape (spheroidal or prolate spheroidal) (Figures 2, 3, ), of medium size ( mm) and pantoaperturate (Table II). The mean D and d values recorded for the grains were statistically significant (Table II). D varied from to mm with a mean value of 37.2 mm and d values ranging between mm, with a mean value of 33.7 mm. The lowest D and d mean values (3.7 and 31.2 mm, respectively) were at the Djelfa (Dj) site and the highest at the Berriane (Be) site (39.2 and 3.4 mm, respectively). The mean value of the D/d ratio, was around 1.11 at all the sites; the highest mean value (1.14) recorded was for the Dj site and the lowest (1.9) was for the Ain Oussera (Ao), Messaad (M) and Aflou (Af) sites, that gave Figure 2. A C. SEM micrographs of non-acetolyzed pollen of Pistacia atlantica from different populations. (A) Messaad; (B) Berriane; (C) El Hamel. Scale bars 2 mm (A C). the spheroidal or prolate spheroidal shape (Table II). For the D/d ratio no significant differences between the six sites were observed in this study. For D the lowest values were from the Af, and Dj sites (no significant differences between these two) and the highest values were from Be that was significantly different from the Af and Dj sites, but 1 1

5 Pistacia atlantica pollen morphology Figure 3. A C. SEM micrographs of acetolyzed pollen of Pistacia atlantica from different populations. (A) El Hamel;(B) Messaad;(C) Berriane. Scale bars 2 mm(a); mm(b, C). not significantly different from the values of the El Hamel (E), Ao and M sites. The same pattern is seen for the d values: Be and Ao sites showed the highest values (no significant differences between the two). The Dj site showed the lowest value but was not Table II. Minimum, maximum and average values of long diameter (D), short diameter (d), D/d ratio, aperture number and pollen fertility. D/d ratio Aperture number Pollen fertility (%) Mean SD (***) Mean SD (***) Mean SD (***) Long diameter (D) Short diameter (d) Mean SD (**) Mean SD (***) (Min-Max) (mm) (Min-Max) (Min-Max) (Min-Max) (Min-Max) (mm) Site Berriane (Be) 39.16a 3. (3 46) 3.36a 2.46 ( 39) 1.11a. (1 1.33) 6.8ab.9 (4 8) 99.7 a.43 (98.7 ) El Hamel (E) 37.92ab 4.69 ( ) 34.24ab 3.94 (28 46) 1.11a.7 (1 1.27) 6.28ab 1.2 (4 9) 97.7 bc 1.14 (9.8 ) Messaad (M) 37.44ab 3.96 (33 44) 34.ab 2.14 ( 39) 1.9a.9 (1 1.2).b.91 (4 7) 9.9 c 2.72 ( ) Ain Oussera (Ao) 37.32ab 3.39 (33 48) 34.28a 2.2 (28 39) 1.9a.6 (1 1.2) 6.a.87 (4 8) 98.8 ab 1. (9.7 ) Aflou (Af) 3.88b 2.16 (33 41) 32.96ab 2.6 (28 37) 1.9a.7 (1 1.21) 6.a.96 ( 9) 99.4 ab.6 (97.9 ) Djelfa (Dj) 3.72b 2.3 ( 39) 31.24b 2.73 (24 3) 1.14a.11 (1 1.) 6.44a.6 ( 8) 98.4 ab 1. (94.1 ) Mean ( ) (24 46) (1 1.) (4 9) (89.4 ) Mean separation within columns, by Tukey test (** pv.1, *** pv.1). Values with same letters are not significantly different. a,b,c, Grana gra d 24//7 18::36 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) 21897

6 Grana gra d 24//7 18::41 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) S. Belhadj et al. 2 3 significantly different from the E, M and Af sites (no significant differences between these sites; Table II). The largest sized pollen (D and d) was found in the most arid site (Be) (Saharian climate type) followed by E, M and Ao sites (Arid climate type) and the smallest for the Dj and Af sites, located in the semiarid climate type (Tables I, II). Pollen aperture number Pollen from different sites showed a variation in aperture number from four to nine with a mean value around six pores (6.). The apertures were spread over the surface giving the pantoporate type. Pollen from the Af, Dj and Ao sites (no significant differences between the sites) had the highest aperture number (respectively, 6.; 6.44 and 6.), while pollen grains from the M site (no significant difference to the E and Be sites), have a significantly smaller number of pores (.) (Table II). Exine The surface of the pollen grains has a reticulate exine sculpturing. The reticulum has brochi of different size and the lumina have more or less rounded depressions giving a foveolate structure (Figure 4). Pollen fertility The statistical analysis showed significant differences between sites in terms of fertility. Pollen fertility was high at all sites ranging between a minimum rate of 89.4% and a maximum rate of % (Table II). Colourless pollen grain is indicator of aborted pollen (Figure ). The Be site had the highest pollen fertility (99.7%), followed by the Af (99.4%), Ao (98.8%) and Dj (98.4%) sites (no significant differences with the latter and among them). The E site fertility (97.7%) was not significantly different from the M site (9.9%), and although it was near the previous group, was significantly lower than the Be site. Pollen size is negatively correlated to the aridity as well as to the altitude of the sites (Figures 6, 7); the size decreases linearly with the increasing aridity and altitude. On the other hand, pollen fertility is positively correlated to the aperture number; the higher the number of apertures, the higher the pollen fertility (Figure 8) Figure 4. SEM micrographs of exine ornamentations of Pistacia atlantica pollen grains. A, B. Non-acetolyzed pollen: (A) El Hamel; (B) Djelfa. C, D. Acetolyzed pollen: (C) Berriane; (D) Messaad. Scale bars 2 1 mm (A D). 1

7 Grana gra d 24//7 18::46 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) Pistacia atlantica pollen morphology 3 6 Figure 7. Relationship between the average pollen size (D and d) and the altitude for each site (see Table I); (r D.82; r d.94) Figure. LM micrographs of Pistacia atlantica pollen grains (). A. Fertile pollen grains stained with acetocarmine. B. Fertile (fp) and sterile (sp) pollen. Discussion Pollen grains from all sites showed uniformity in shape and exine sculpturing, while pollen grains showed variability in size, aperture number and fertility between the different sites. This is in accordance with descriptions of pollen grains from other Pistacia species (Erdtman, 192; Zavada & Dilcher, 1986; El-Oqlah, 1996; Ozeker et al., 6). Pistacia pollen shape is variable, with Erdtman (192) describing Pistacia pollen grains as spheroidal or oblate, while Alyafi (1979) and Zavada & Dilcher (1986) reported a spherical shape. However, a tendency to spheroidal shape is stated for P. atlantica pollen grains by Erdtman (192) and El-Oqlah (1996). This is in accordance with our study. Variation in P. atlantica pollen size is also seen in our study, and although our D-d values were higher than those given by Alyafi (1979), they were in general agreement with those of Erdtman (192), (Table III). The characteristics of the pollen of P. atlantica from the Dj site (Table II) resemble those of the Turkish and Jordanian material studied by Alyafi (1979), (Table III). As far as pollen apertures are concerned, the aperture number is reported to be a plastic feature in the genus Pistacia and it may also vary within the same taxon (Erdtman, 192; Haddad, 1969; Alyafi, 1979; El-Oqlah, 1996), (Table III). This is in accordance with our results, where the number of Figure 6. Relationship between the average pollen size (D and d) and the Emberger quotient (Q 3 ) for each site (see Table I); (r D.96; r d.81). Figure 8. Relationship between the average pollen aperture number and the pollen fertility for each site (see Table I); (r+.77). 1

8 Grana gra d 24//7 18::3 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) S. Belhadj et al. Table III. Characteristics of Pistacia atlantica pollen. Comparison of data from different sources. Author Taxon Long diameter (mm) Mean (Min-Max) Short diameter (mm) Mean (Min-Max) Aperture number Mean (Min-Max) Pollen shape Origin Alyafi (1979) Pistacia atlantica ( 28) (18 24).88 ( 7) Spherical Messaad (Algeria) ( 26) (18 24) 6.16 (4 7) Ain Safra (Algeria) 29.1 (2 3) (24 ) 4.76 (4 ) Jordan 29.6 (26 33) (23 ) 4.84 (4 6) Turkey 23. ( 28) 21. (19 24).4 (4 7) to Tunisia Pistacia atlantica (2 34) 26. (23 ) 6.66 ( 9) Iraq var. kurdica Zoh. (Sensu P.eurycarpa Yaltirik) Pistacia atlantica. (18 24).6 (18 24) 4.68 (4 6) subspherical Russia var. latifolia Zoh. (Sensu P.mutica Fischer & C.A. Meyer) Erdtman (192) Pistacia atlantica 33 / (6 7) spheroidal to prolate spheroidal / Our results (mean values) Pistacia atlantica var. atlantica apertures varied from four to nine per pollen grain in P. atlantica populations. Concerning the exine sculpturing, Alyafi (1979) reported a reticulate ornamentation in Pistacia pollen. Pistacia vera showed different exine structures associated with different varieties (Davarynejad et al., 199). According to El-Oqlah (1996), the exine has a tectate infrastructure with smooth reticulate ornamentations. Zavada & Dilcher (1986) reported a perforate tectum with a columellate infrastructure. In P. atlantica, the ornamentations were micro reticulate or foveolate (Alyafi, 1979), and a similar feature was noted in our study. The external characters of pollen, such as size, number of pores and sculpturing of the exine, are widely used for identification purposes and the number of pores on periporate pollen has been used as a diagnostic character for taxonomic purposes in several families such as the Caryophyllaceae, Plantaginaceae and Chenopodiaceae (Mc Andrews & Swanson, 1967). Davarynejad et al. (199), in their study, used pollen morphology as an indicator for the identification of male pistachio trees for P. vera varieties. However, it is recognized that these characters are more or less variable, particularly as a result of the effects of climate on the pollen-forming plant (Kurtz & Liverman, 198) and several studies have attempted to demonstrate the relationship between pollen characteristics and various climatic factors. Species with many pores tend to have larger pollen grains than species with few pores. This increase in size may be caused by an increased adaptation to different systems of animal pollination ( ) (24 46) 6. (4 9) spheroidal Algeria as well as the level of polyploidy that may be manifested by larger grains as the ploidy level increases. Mineral nutrition as well as the genetic factors may also cause variation in pollen size. In addition a correlation with climatic factors has been postulated for the genus Ilex, in which the pollen size increases both with latitude and altitude (Lobreau- Callen, 197). In our study, there is a trend towards a larger size of pollen grains from the semi-arid sites to the more arid sites and which is also negatively correlated to the site altitude. This is not in accordance with Kurtz and Liverman (198) who reported the occurrence of smaller pollen grains caused by aridity. Another perspective is given by Dömnez and Pinar (1), who reported a trend towards greater pollen size from the less to the more specialized taxa in Iris species, supporting the general idea that pollen size increases with evolution. The pollen of angiosperms for instance, has evolved towards an increasing number of apertures that offers a potential selective advantage because it increases the likelihood of contact between the germination site and the stigmatic surface (Dajoz et al., 1991). Pollen fertility, as well, may provide additional information of taxonomic importance when correlated with morphological traits and may help to determine whether a plant species is successfully adapted to certain ecological conditions (Qureshi et al., 2). Crane et al. (1974) reported that pollen fertility could vary between species, types and years. This variation may be due to different ecological conditions between the different sampling regions as has been suggested for Pistacia species (Ozeker et al.,

9 Grana gra d 24//7 18::3 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) Pistacia atlantica pollen morphology ). In our study we used the acetocarmine method as a measure for viable grains. The acetocarmine staining shows the presence or absence of cytoplasm in the pollen grains. It may overestimate pollen fertility since pollen containing cytoplasm may be non-fertile (Dafni & Firmage, ). However, the measurements are useful in separating the various populations studied for applied artificial pollination and indicate high pollen fertility at all the sites. This is positively correlated with the aperture number, whereas no correlations are seen between the inferred pollen fertility, pollen size, and climatic conditions (Data not shown). This is in contrast to the study by Till-Bottraud et al. (1994) that reported a negative correlation between pollen fertility and aperture number in some angiosperm species. Conclusions The present investigation shows that pollen morphology of the Algerian representatives of Atlas pistachio is comparatively homogenous. Indeed, the surface pattern of the pollen from all sites showed homogeneity. Nevertheless, variation among populations was seen mainly in the diameters of the grains and the aperture number as well as in the fertility. The acetocarmine test showed high number of pollen grains containing cytoplasm of this species across the contrasting habitats, which may be used as an indication of high viability of pollen at all sites studied. Thus the pollen from all sites may be considered as functional in artificial pollination. Three different groups can be distinguished, based on pollen size, according to the aridity quotient Q 3 : Dj and Af sites (semi-arid group); E, M and Ao sites (arid group) and Be site (Saharian group). Three different groups are also separated according to their altitude: the group from 7 8 m altitude (E, Be, M and Ao sites), the group at 9 m altitude (Af site) and the group at m altitude (Dj site). While two groups are distinguished according to their pollen fertility: M site (less than 96%) and E, Dj, Ao, Af and Be sites (with more than 97%). These results show a potential use of pollen characteristics at least in some infra-specific systematic and pollination studies in Pistacia atlantica. Acknowledgements We thank the staff of the Ecolab UMR 24 CNRS/ UPS/INP, Toulouse and especially Dr. O. Roux and Dr. E. Van Campo for their technical assistance and co-operation. We would like also to thank N. Myers, MD, USA and J. Woodley, independent contractors, for the English correction of this article. References Alyafi, J. (1979). Approches systématiques et écologiques du genre Pistacia dans la région méditerranéenne. Marseille: Fac. Sci. Techn. St-Jerome, Univ. Aix-Marseille III. 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10 Grana gra d 24//7 18::4 The Charlesworth Group, Huddersfield +44() Rev 7.1n/W (Jan 3) S. Belhadj et al. Shaheen, M. A. (4). Evaluation of date palm males pollen viability and ultrastructure. In L. G. Albrigo & V. Galán Saúco (Eds), Citrus and other Subtropical and Tropical fruit crops: Issues, advances and opportunities Proc. 26 th Int. Hortic. Congr. Toronto 2. Leuven: ISHS. Acta Hort Stewart, P. (1974). Un nouveau climagramme pour l Algérie et son application au barrage vert. Bull. Soc. Hist. Nat. Afrique Nd, 6, Till-Bottraud, I., Lawrence Venable, D., Dajoz, I. & Gouyon, P. H. (1994). Selection on pollen morphology: A game theory model. Am. Nat., 144, Wodehouse, R. P. (193). Pollen grains. New York/London: Hafner Publ. Co. Zavada, M. S. & Dilcher, D. L. (1986). Comparative pollen morphology and its relationship to phylogeny of pollen in the Hamamelidae. Ann. Mo. Bot. Gard., 73,