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).