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. 2016 Dec 21;68(2):207–223. doi: 10.1093/jxb/erw432

Table 1.

Traits of photosynthetic pathway, leaf anatomy and life form in Salsoleae s.s. Trait 1: type of photosynthesis according to carbon isotope value; coding trait 2: C3 = 0, C4 = 1. Trait 2: function of bundle sheath (BS), Kranz-like (KLC) and Kranz cells (KC); coding trait 2: C3 type BS cells around peripheral VB (few or no organelles) = 0, KLC with increased number of organelles mostly in centripetal position, GDC only expressed in KLC cells, C3-C4 species = 1, C4 type Kranz cells = 2. Trait 3: Life form according to standard floras and our own observations in the field; coding trait 3: perennial l = 0, annual = 1. Trait 4: presence of sclerenchyma by replacement of major parts of the central water storage tissue; coding trait 4: no = 0, yes = 1. Trait 5: sites of major photosynthetic function; coding trait 5: predominantly in leaves and leaf-like structures (0), ± equally in leaves and stems (1), predominantly in stems due to reduction of leaves or their trans-formation into thorns (2). References for photosynthetic pathway and leaf anatomy see below table. Species are classified according to carbon isotope composition of leaf tissue as C3 or C4. Species are classified as C3, proto-kranz, C3-C4 intermediates, and C4 based on analyses of leaf anatomy, Trait 2 and C isotope composition, (see text).

Species of Salsoleae s.s. Isolate no. for molecular analysis Trait 1: Type of photosynthesis according to carbon isotope ratio Leaf anatomy; type names according to Voznesenskaya et al. (2013) Trait 2 Trait 3 Trait 4 Trait 5
Anabasis aphylla L. chen 2743/2017 C4 (1, 2, 12) salsoloid+H (1, 6, 8, this study) 2 0 0 2
Anabasis articulata (Forssk.) Moq. chen 2360 C4 (7) salsoloid+H (6, 8, 12, this study) 2 0 0 2
Anabasis brevifolia C.A. Mey. chen 2407 C4 (12) salsoloid+H (2, 11, this study) 2 0 0 1
Anabasis calcarea (Charif & Aellen) Bokhari & Wendelbo chen 1841 C4 (1) salsoloid+H (1, this study) 2 0 0 2
Anabasis ehrenbergii Schweinf. ex Boiss. chen 2403/2741 C4 (12) salsoloid+H (this study) 2 0 0 2
Anabasis setifera Moq. chen 2373 C4 (7) salsoloid+H (1, 2, 6, 12, this study) 2 0 0 1
Arthrophytum betpakdalense Korov. chen 0229 C4 ** salsoloid+H (this study) 2 0 0 1
Arthrophytum gracile Aellen chen 2603 C4 (1) salsoloid+H (this study) 2 0 0 2
Arthrophytum lehmannianum Bunge chen 2637 C4 (4) salsoloid+H (5, this study) 2 0 0 1
Cornulaca amblyacantha Bunge chen 0350 C4 ** salsoloid+H+S (this study) 2 0 1 1
Cornulaca monacantha Delile chen 0212 C4 (1, 12) salsoloid+H+S (2, this study) 2 0 1 1
Cornulaca setifera (DC.) Moq chen 0304 C4 (12) salsoloid+H+S (6, this study) 2 0 1 1
Cyathobasis fruticulosa (Bunge) Aellen chen 0082 C4 (12) salsoloid+H+S (this study) 2 0 1 2
Girgensohnia diptera Bunge chen 2639 C4 ** salsoloid+H+S (this study) 2 1 1 2
Girgensohnia minima E. Korov. chen 2601 C4 ** salsoloid+H+S (this study) 2 1 1 2
Girgensohnia oppositiflora (Pall.) Fenzl chen 0033 C4 (1, 12) salsoloid+H+S (2, 6, this study) 2 1 1 (1)2
Gyroptera gillettii Botsch chen 2819 C4 ** salsoloid+H (this study) 2 0 0 0
Halogeton alopecuroides (Delile) Moq. chen 0300 C4 (1, 7, 12) salsoloid+H (6, 8, 12, this study) 2 0 1 0
Halogeton arachnoideus Moq. chen 2605 C4 (1) salsoloid+H (this study) 2 1 0 0
Halogeton glomeratus (M. Bieb.) C.A. Mey. chen 0030 C4 (1) salsoloid+H (2) 2 1 0 0
Halogeton sativus (L.) Moq. chen 1229 C4 (1) salsoloid+H (8, this study) 2 1 0 0
Halothamnus bottae Jaub. & Spach chen 0351 C4 (12) salsoloid (7) 2 0 0 2
Halothamnus ferganensis Botsch. chen 0197 C4 ** salsoloid (7) 2 0 0 1
Halothamnus iliensis (Lipsky) Botsch. chen 2668 C4 (1, 12) salsoloid (7) 2 1 0 1
Halothamnus somalensis (N.E. Br.) Botsch. chen 2584 C4 ** salsoloid (7) 2 0 0 2
Haloxylon ammodendron (C.A. Mey.) Bunge chen 0035 C4 (1, 2, 12) salsoloid+H (11, this study) 2 0 0 2
Haloxylon persicum Bunge ex Boiss. chen 2815 C4 (7, 12) salsoloid+H (11) 2 0 0 2
Hammada articulata (Moq.) O. Bolos & Vigo chen 0196 C4 ** salsoloid+H (2, 6, this study)) 2 0 0 2
Hammada eriantha Botsch. chen 2813 C4 ** salsoloid+H (this study) 2 0 0 2
Hammada griffithii (Moq.) Iljin chen 2635 C4 (1, 12) salsoloid+H+S (this study) 2 0 1 2
Hammada negevensis Iljin & Zoh. chen 2814 C4 (7, 12) salsoloid+H (this study) 2 0 0 2
Hammada salicornica (Moq.) Iljin chen 2752 C4 (1, 7) salsoloid+H (2, 8, 12, this study) 2 0 0 2
Hammada schmittiana (Pomel) Botsch. chen 2629 C4 (7, 12) salsoloid+H (this study) 2 0 0 2
Hammada thomsonii (Bunge) Iljin chen 0178 C4 ** salsoloid+H+S (this study) 2 0 1 2
Horaninowia capitata Sukhor. chen 0188 C4 ** salsoloid+H+S (this study) 2 1 1 1
Horaninowia platyptera Charif & Aellen chen 2602 C4 (1) salsoloid+H+S (this study) 2 1 1 1
Horaninowia ulicina Fisch. & C.A. Mey. chen 2589 C4 (1) salsoloid+H+S (15, this study) 2 1 1 1
Iljinia regelii (Bunge) Korovin chen 0182 C4 (4) salsoloid+H (11, this study) 2 0 0 0
Lagenantha cycloptera (Stapf) M.G. Gilbert & Friis chen 2809 C4 ** salsoloid+H (this study) 2 0 0 0
Noaea minuta Boiss. & Bal. chen 0079 C4 (12) salsoloid+S (this study) 2 1 1 0
Noaea mucronata (Forssk.) Asch. & Schweinf. chen 0019 C4 (1, 2, 7) salsoloid+S (6, 9, this study) 2 0 1 (1)2
Nucularia perrinii Batt. chen 2627 C4 ** salsoloid+H (8, this study) 2 0 0 0
Rhaphidophyton regelii (Bunge) Iljin chen 0075 C3 (4) kranz-like salsoloid+S (this study) 1 0 1 0
Salsola abrotanoides Bunge chen 2996 C3 (4, 6, 9) sympegmoid (11, this study) 0 0 0 0
Salsola acutifolia (Bunge) Botsch. chen 2640 C4 (1, 12) salsoloid+H (this study) 2 1 0 0
Salsola arbusculiformis Drob. chen 0176 C3 (1, 2, 6, 8, 11) kranz-like sympegmoid (13, 16, this study) 1 0 0 0
Salsola botschantzevii Kurbanov chen 2630 C3 (9) proto-kranz sympegmoid (this study) 0 0 0 0
Salsola cyrenaica (Maire & Weiller) Brullo chen 0354 C4 (9) salsoloid+H (3, this study) 2 0 0 0
Salsola deschaseauxiana Litard. & Maire chen 2758 ( = 2641) C3 (9) kranz-like salsoloid (this study) 1 0 0 0
Salsola divaricata Masson ex Link chen 2779 C3 (6, 9) kranz-like salsoloid (14, this study) 1 0 0 0
Salsola drobovii Botsch. chen 0175 C3 (4, 6, 9) proto-kranz sympegmoid (this study)*** 0 0 0 0
Salsola florida (M. Bieb.) Poir. chen 2811 C4 (1, 12) salsoloid+H (2, 6, this study) 2 1 0 0
Salsola foliosa (L.) Schrad. chen 0103 C4 (1) salsoloid+H (11, this study) 2 1 0 0
Salsola grandis Freitag, Vural & N. Adιgüzel chen 0105 C4 ** salsoloid+H (4, this study) 2 1 0 0
Salsola gymnomaschala Maire chen 0355 C3 (9) kranz-like salsoloid (this study) 1 0 0 0
Salsola junatovii Botsch. not included C3 (9) proto-kranz sympegmoid (this study) 0 0 0 0
Salsola kerneri (Woł.) Botsch. chen 2642 C4 (1, 6) salsoloid+H (this study) 2 0 0 0
Salsola laricifolia Turcz. ex Litv. chen 1355 C3 (6, 9, 10, 11) kranz-like salsoloid (14, 15, 16, this study) 1 0 0 0
Salsola lipschitzii Botsch. not included C3 (9) proto-kranz sympegmoid (this study) 0 0 0 0
Salsola melitensis Botsch. chen 2644 C4 (9) salsoloid+H (this study) 2 0 0 0
Salsola montana Litv. chen 2591 C3 (1, 2, 5, 6, 9) proto-kranz sympegmoid (14) 0 0 0 0
Salsola oppositifolia Desf. chen 0099 C4 (1, 6, 9, 12) salsoloid+H (8, this study) 2 0 0 0
Salsola oreophila Botsch. chen 2847 C3 (5, 9) sympegmoid (10, this study) 0 0 0 0
Salsola pachyphylla Botsch. chen 2762 C3 (5, 6) sympegmoid (11, this study)) 0 0 0 0
Salsola rosmarinus (Ehrenb. ex Boiss.) Akhani chen 0303 C4 (1, 7) salsoloid+H (2, 6, this study) 2 0 0 0
Salsola schweinfurthii Solms-Laub. chen 2827 C4 (1, 6, 7, 12) salsoloid+H (this study) 2 0 0 0
Salsola soda L. chen 2834 C4 (1, 7) salsoloid+H (9, this study) 2 1 0 0
Salsola stocksii Boiss. chen 2646 C4 (1) salsoloid+H (2) 2 0 0 1
Salsola tianschanica Botsch. not included C3 (9) sympegmoid (this study) 0 0 0 0
Salsola tunetana Brullo chen 2647 C4 ** salsoloid+H (this study) 2 0 0 0
Salsola verticillata Schousboe chen 2648 C3 (this study)* kranz-like salsoloid (this study) 1 0 0 0
Salsola webbii Moq. chen 2828 C3 (1, 6, 9, 12) sympegmoid (2, 8, 14, this study) 0 0 0 0
Salsola zygophylla Batt. & Trab. chen 2756 C4 (1, 6, 12) salsoloid+H (this study) 2 0 0 0
Salsola zygophylloides (Aellen & Townsend) Akhani chen 2593 C4 ** salsoloid+H (this study) 2 0 0 0
Sevada schimperi Moq. chen 2590 C4 (3) salsoloid+H (this study) 2 0 0 0
Sympegma regelii Bunge chen 383a/2766 C3 (4, 11) sympegmoid (2, 9, 16, this study) 0 0 0 0
Salsola genistoides Juss. ex Poir. (outgroup) chen 1155/1362 C3 (1, 9) sympegmoid (11, this study) 0 0 0 2

References for C 3 versus C 4 type carbon isotope ratio: 1 = Akhani et al. (1997), 2 = Akhani and Ghasemkhani (2007), 3 = Carolin et al. (1975), 4 = Freitag and Stichler (2000), 5 = P’yankov et al. (1997), 6 = Pyankov et al. (2001), 7 = Shomer-Ilan et al. (1981), 8 = Voznesenskaya et al. (2001), 9 = Voznesenskaya et al. (2013), 10 = Wen and Zhang (2011), 11 = Wen and Zhang (2015), 12 = Winter (1981).

References for leaf anatomy: 1 = Bokhari and Wendelbo (1978), 2 = Carolin et al. (1975), 3 = Freitag and Duman (2000), 4 = Freitag et al. (1999), 5 = Freitag and Stichler (2000), 6 = Khatib (1959), 7 = Kothe-Heinrich (1993), 8 = Maire (1962), 9 = Monteil (1906), 10 = P’yankov et al. (1997), 11 = Pyankov et al. (2001), 12 = Volkens (1887), 13 = Voznesenskaya et al. (2001), 14 = Voznesenskaya et al. (2013), 15 = Wen and Zhang (2011), 16 = Wen and Zhang (2015).

*In Voznesenskaya et al. (2013) this species was mentioned to have the C4 pathway. However, samples for the carbon isotope value were taken from a wrongly identified specimen [D. Podlech 44954 (P)]. The correct identification for this specimen is Salsola oppositifolia, which indeed is a C4 species.

** C4 metabolism deduced from leaf anatomy, no carbon isotope values available.

*** Classified as sympegmoid in Freitag and Duman (2000), Pyankov et al. (2001) and Khatib (1959).