Table 1.
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).