Taxonomic Revision of the Genus Pistacia L. (Anacardiaceae)

Pistacia is an economically important genus because it contains the pistachio crop, P. vera, which has edible seeds of considerable commercial importance whose value has increased over the last two decades reaching an annual value of about $2 billion (harvested crop). The taxonomic relationships among its species are controversial and not well understood due to the fact that they have no genetic barriers. The taxonomy of this genus is revised in detail through our research. It includes the following taxa: Pistacia atlantica Desf., P. chinensis Bunge subsp. chinensis, P. chinensis subsp. falcata (Bess. ex Martinelli) Rech. f., P. chinensis subsp. integerrima (J.L. Stew. ex Brandis) Rech. f., P. eurycarpa Yalt., P. khinjuk Stocks, P. lentiscus L. subsp. lentiscus, P. lentiscus subsp. emarginata (Engl.) AL-Saghir, P. mexicana Humb., Bonpl., & Kunth, P. X saportae Burnat, P. terebinthus L., P. vera L., and P. weinmannifolia Poiss. ex Franch. The genus is divided into two sections: section Pistacia and section Lentiscella. A key to the 14 taxa that have been recognized by this study is included. The new combination P. lentiscus subsp. emarginata (Engl.) AL-Saghir is made, and the names P. chinensis subsp. integerrima (J. L. Stew. ex Brandis) Rech. F., P. terebinthus L., and P. vera L. are lectotypified.


Introduction
Pistacia L. belongs to the family Anacardiaceae (cashew family), order Sapindales [1]. It contains nine species and five subspecies according to the current study.
Pistacia vera L. (cultivated pistachio) is by far the most economically important species in the genus. The value of P. vera fruits has increased over the last two decades reaching an annual value of about $2 billion (harvested crop) [2]. It has edible seeds and considerable commercial importance. Pistachios are utilized mostly in the shell, for fresh consumption; processed uses include candy, baked goods, and ice cream. They also have traditional, medicinal, and non-food uses such as toothache relief. The resin is used as a blood-clotting agent in Europe and the Middle East, while husks are used in India for dying and tanning. Pistachios have been reported as a remedy for scirrhus and sclerosis of the liver, abscesses, poor circulation, and other medical problems [3]. Currently, Iran, the United States, Turkey, and Syria are the main pistachio producers in the world, contributing over 90% of the world production [2].
Members of the genus are dioecious trees or shrubs with well-developed vertical resin canals. Leaves are alternate, deciduous or persistent, pinnately compound, but sometimes trifoliolate or unifoliolate, pari-or imparipinnate, membranaceous or leathery. Inflorescences are determinate and terminal or axillary. Flowers are almost always unisexual, radial, small, with well developed staminodes or carpellodes, and apetalous; sepals are usually 5, distinct to slightly connate; stamens are 4 -5, filaments are very short, usually glabrous, and usually distinct; pollen grains tricolporate or triporate; carpels are usually 3 and variously connate; ovary superior, with only 1 fertile and well developed carpel; gynoecium asymmetrical and unilocular with apical placentation, ovule 1; stigma capitate. Nectariferous disk present, usually intrastaminal. Fruit a flattened asymmetrical drupe, embryo curved; endosperm scanty or lacking.
Pistacia is believed to have originated in Central Asia [4][5][6][7]. Two centers of diversity have been described. One comprises the Mediterranean region of Southern Europe, Northern Africa, and the Middle East. The second comprises West and Central Asia [6][7][8][9]. The species of the genus occur naturally from North Africa to the Philippines and from Texas to Nicaragura.
Few systematic studies have been published on this important genus. The first complete classification of the genus was published by   [10]. Today, there are many questions about Zohary's taxonomic treatment, the status of many of his species, and the accuracy of dividing the genus into four sections. This disagreement is mainly because of little information being available on the phylogeny of the genus. Studies such as the one performed by  were hampered by the small sampling size, weak representation of the species, and unefficient methods. Consequently, the studies failed to resolve the relationships between species within the genus. Moreover, species of Pistacia easily form interspecific hybrids, suggesting close relationships, which limit the previous studies and make the actual level of speciation and relationships within the genus unclear [4]. A better understanding of these relationships is also needed to make the species more useful for plant improvement or genetic studies.
A comprehensive taxonomic revision, utilizing different types of data, is urgently needed for Pistacia in order to clarify the phylogenetic relationships between the species and to characterize the collective germplasm. This will provide a framework and guidelines for plant improvement and help to preserve the genetic resources of this important crop, especially since these genetic resources are under threat by extensive forest cutting in their native countries (especially in the Mediterranean countries, and Central and Western Asia).
Since  treatment, several new species have been added to Pistacia. Yaltirik (1967a, 1967b [13,14] classified Pistacia species in Turkey and described a new species, P. eurycarpa. This had been called P. atlantica var. kurdica by , a synonym. Zohary considered P. palaestina as a separate species, whereas Yaltirik (1967aYaltirik ( , 1967b retained it as a variety of P. terebinthus. Kokwaro described a new species from East Africa, P. aethiopica, in Kokwaro and Gillett (1980). Fifty-five binomials for Pistacia were found in the International Plant Names Index [15], only 14 were recognized by the authors (all those listed in this section). The hybrids will be further discussed in the taxonomic section of this study. Yi et al. (2008) [16] assessed the phylogeny of Pistacia using five molecular sets, sequences of nuclear ribosomal ITS, the third intron of the nuclear nitrate reductase gene (NIA-i3), and the plastid ndhF, trnL-F, and trnC-trnD. Their molecular data were largely consistent with our independently derived intrageneric classification based on morphology. They recognized the following species: P. atlantica, P. chinensis, P. integerrima, P. khinjuk, P. lentiscus, P. mexicana, P. palaestina, P. saportae, P. terebinthus, P. texana, P. vera, and P. weinmannifolia. Except for P. palaestina and P. texana, our study recognized these taxa (P. integerrima as a subspecies of P. chinensis), plus P. chinensis subsp. falcata, P. eurycarpa, and P. lentiscus subsp. emarginata. Pistacia was shown to be monophyletic in all analyses. The two accessions of P. vera formed a clade with P. khinjuk in all molecular data sets. Some of the ITS and NIA-i3 sequences of these two species were identical, suggesting a close relationship. Earlier molecular results also suggested a close relationship between them [4][5][6]17]. Pistacia palaestina was not well separated from P. terebinthus in either the plastid or the nuclear DNA data sets, and Yi et al. (2008, p. 245) stated that, "Pistacia palaestina may need to be merged into P. terebinthus." Close relationships between these two species were also suggested by the AFLP and the RAPD results [17][18][19]. These results are consistent with Engler (1936) [20] and Yaltirik (1967a), along with our classification, in considering P. palaestina to be a synonym of P. terebinthus. Pistacia mexicana and P. texana were not distinguishable in plastid restriction analyses [4]. The ITS data suggest that P. mexicana and P. texana are sister taxa; and the sequence divergence between these two species is low. Our morphological data indicate that there is too little variation to warrant the recognition of two species. Pistacia saportae was shown to be a hybrid between P. lentiscus (maternal) and P. terebinthus (paternal), as others had hypothesized (e.g., . Neighbor joining and parsimony analyses were performed on the morphological data for section Pistacia using PAUP 4.0 b10 [7,21]. Both analyses show that minutely puberulent; terminal leaflet 2.7 -7 cm long, 5 -20 mm wide, same size or smaller than laterals. Staminate panicles to 7(-11) cm long, often clustered, stout, branched from base, densely flowered, pubescent; flowers red. Pistillate panicles to 15 cm long, subterminal with leaves, stout, branched from base, minutely pubescent; flowers pinkish. Drupes many, red or reddish, 3 mm long, mesocarp fleshy, endocarp bony.
Phenology.-Flowering December, January, March to May; fruiting March to September.
Phenology.-Flowering March to May; fruiting April to October.
Common names.-Gulungoor, Gwun, Khinjuk, Shurumma (Afghanistan), Ushgai Buzgai (Baluchistan) [10]. Comments-Both Stearn (1957) [23] and Jarvis (2007) [24] emphasise the importance of the numbers that Linnaeus wrote on the sheets of many of the specimens in his herbarium for the typification of his names. "Such numbers almost always link these specimens with the corresponding account in the first edition of Species Plantarum" (Jarvis 2007: 43). Furthermore, "Stearn, from long study of the herbarium specimens and protologues over many years, reached the conclusion that the presence of such a number provided extremely strong evidence that the collection in question was in Linnaeus' possession by 1753" (Jarvis 2007:44 Bot. Jerusalem Ser. 5:209. 1952. TYPE: TUNISIA: Jebel Ichkeut, 1887, Letourneux (HOLOTYPE: C).
Phenology.-Flowering March to July; fruiting April to October.
Distribution.-Native to the Mediterranean basin, from Spain to Turkey, Croatia, and Bosnia, and Morocco to Saudi Arabla, Jordan, and Syria. Comments-Both Stearn (1957) and Jarvis (2007) strongly make the point that when choosing a lectotype for a Linnean name it is best to choose a specimen rather than an illustration. However, in this case it not possible to do so. None of the specimens of P. vera in Linnaeus' herbarium can be used to typify this name. No. 1170.1 (not annotated by Linnaeus) appears to have been added after 1753. No. 1170.2 (annotated "2 narbonensis Kh" [Linnaeus' student Martin Kahler] in Linnaeus' script) is a type of P. narbonensis. No. 1170.3 (annotated "Pistacia 3" in Linnaeus' script) is from George Clifford's herbarium (BM), but Hortus Cliffortianus (Linnaeus 1738) is not cited in his protologue; it is also annotated "an a P Terebinthus diversa? Non es vera" by J.E. Smith and indeed is P. terebinthus.
Phenology.-Flowering December to September; fruiting April and July to November.