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Home , Barleria cristata, Bignoniaceae, Bignonia capreolata, Catalpa bignonioides, Crescentia alata, Dolichandrone

beni-suef university journal of basic and applied sciences 3 (2014) 172e177

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Full Length Article Morphological of Juss.

* Usama K. Abdel-Hameed

Ain Shams University, Faculty of Science, Department, Abassia, Cairo, Egypt article info abstract

Article history: The most recent classification of Bignoniaceae recognized seven tribes, Phylogenetic and Received 7 April 2014 monographic studies focusing on within Bignoniaceae had revised tribal and generic Received in revised form boundaries and numbers for several groups, the portions of the that remain 22 September 2014 most poorly known are the African and Asian groups. The goal of the present study is to Accepted 23 September 2014 identify the primary lineages of Bignoniaceae in Egypt based on macromorphological traits. Available online 4 November 2014 A total of 25 species of Bignoniaceae in Egypt was included in this study (Table 1), along with cristata as outgroup. Parsimony analyses were conducted using the program Keywords: NONA 1.6, preparation of data set matrices and phylogenetic editing were achieved in WinClada Software. The obtained cladogram showed that within the studied taxa of Phylogeny Bignoniaceae there was support for eight lineages. The present study revealed that the two studied species of showed a strong support for as well as and Monophyletic genera . It was revealed that , and are not monophyletic Bignoniaceae genera. Copyright 2014, Beni-Suef University. Production and hosting by Elsevier B.V. All rights reserved.

recognized seven of the eight tribes proposed by Gentry 1. Introduction (1980): Bignonieae, Coleeae, Crescentieae, Eccremocarpeae, Oroxyleae, Tecomeae, and Tourrettieae. Bignoniaceae Juss. is a family of , or and Phylogenetic and monographic studies focusing on clades rarely herbs (Watson and Dallwitze, 1992). The family includes within Bignoniaceae have revised tribal and generic bound- 82 genera and 827 species (Lohmann and Ulloa, 2007) and it is aries and species numbers for several groups, including distributed in the tropics and forms an important part of the Coleeae (Zjhra et al., 2004), Bignonieae (Lohmann, 2006), vegetation (Shashina, 1989), while a few of the species are (Chen et al., 2005), Crescentieae/Tabebuia s.l. found in the temperate and sub-tropical regions. (Grose and Olmstead, 2007a, b), and (Li, 2008). Taking Bignoniaceae belong in (Angiosperm Phylogeny these recent studies into account, along with the two-volume Group II, 2003; Olmstead et al., 1993), The taxonomic history monograph of neotropical Bignoniaceae (Gentry, 1980, 1992), of the family was described in detail by Gentry (1980) and the portions of the family that remain most poorly known are summarized by Spangler and Olmstead (1999). The most the African and Asian groups, which account for approxi- recent classification of Bignoniaceae by Fischer et al. (2004) mately 29 genera and 115 species (Lohmann and Ulloa, 2007).

* Tel.: þ20 122 3616259. E-mail addresses: [email protected], [email protected]. Peer review under the responsibility of Beni-Suef University. http://dx.doi.org/10.1016/j.bjbas.2014.09.001 2314-8535/Copyright 2014, Beni-Suef University. Production and hosting by Elsevier B.V. All rights reserved. beni-suef university journal of basic and applied sciences 3 (2014) 172e177 173

Table 1 e The studied taxa of Bignoniaceae with related senso Schumann (1895) and outgroup . No. Taxa Tribe senso Schumann (1895) 1. paniculatum (L.) Humboldt, Bondpland and Kunth var. Bignonieae paniculatum 2. B. capreolata L. (¼B. crucigera L., Anisostichus capreolata Bur., Doxantha capreolata Miers.) 3. B. jasminoides Hort. (¼Tecoma jasminoides Lindl, jasminoides Schum.) 4. B. magnifica Bull. (¼Arrabidaea magnifica Steen., magnifica (Steen.) Dugand) 5. B. purpurea Lodd. 6. B. venusta Ker., (¼ ignea (vell.) Presl., P. venusta (Ker.) Miers., Tecoma venusta Lem.) 7. grandiflora Loisel (¼C. chinensis Voss, Bignonia chinensis Lam., B. Tecomeae grandiflora Thunb., Tecoma chinensis Koch, T. grandiflora Loisel. Amat.) 8. Walt. (¼C. catalpa (L.) Karst., C. syringaefolia Sims., Bignonia catalpa L.) 9. cujete L. (¼Crescentia ovate Burm.) Crescentieae 10. Doxantha unguis-cati Mier em. Rehder (¼D. unguis Miers., Bignonia unguis-cati Bignonieae L., B. tweediana Lindl., Batocydia unguis Mart., Macfadyena unguis-cati (L.) A.Gentry., M. dentate Bur. & K. Sch.) 11. acutifolia Humb. & Bonpl. (¼J. ovalifolia R. Br., J. mimosifolia D. Don) Tecomeae 12. Kigelia africana (Lamk) Bth. In Hook. (¼K. aethiopicum (Fenzl.) Dandy, K. Crescentieae pinnata (Jacq.) DC., Crescentia pinnata Jacq., Bignonia Africana Lamk., Tecoma Africana G. Don) 13. K. moosa Sprague 14. Markhamia hildebrandtii (Baker) Sprague (¼M. lutea K. Schum., Tecomeae hildebrandtii Baker) 15. M. platycalyx Sprague (¼Dolichandrone platycalyx Baker) 16. hortensis L.F. (¼M. dubiosa Span., Bignonia suberosa Roxb., B. Bignonieae cicutaria Mart., Nevrilis suberosa Rafin.) 17. Parmentiera alata Miers. (¼ H.B.K., C. trifoliate Blanco, Otophora Crescentieae paradoxa Bl.) 18. P. cerifera Seem. 19. campanulata P. Beauv. (¼S. tulipifera G. Don, S. danckelmaniana Tecomeae Buttn., Bignonia tulipifera Schymach. & Thonn.) 20. S. niolotica Seem. 21. Tabebuia guayacan (Seem.) Hemsl. (¼Tecoma guayacan Seem.) 22. T. pentaphylla (L.) Hemsl. (¼Bignonis pentaphylla L., B. pallida Lindl., (Bertol.) DC., T. Pallida (Lindl.) Miers., Couralia rosea Donn.-Sm., Tecoma rosea Bertol., T. pentaphylla Juss., T. evania Donn.-Sm.) 23. (Thunb.) Lindl. (¼Tecomaria capensis (Thunb.) Spach., T. krebsii Klotzsch, T. petersri Klotzsch, Bignonia capensis Thunb., Ducoudraea capensis Bur.) 24. T. shirensis Baker (¼Tecomaria chirensis K. Schum., Tecoma whytei G.H. Wright., T. nyikensis Baker) 25. T. stans (L.) H.B. & K. (¼Bignonia stans L., Stenolobium stans (L.) Seem.) 26. Barleria cristata L. e 2 1753 (APNI) (Outgroup) Family

Previous phylogenetic studies have provided an outline The goal of the present study is to identify the primary of relationships in the family (Bignonieae: Lohmann, 2006; lineages of Bignoniaceae in Egypt based on macro- Coleeae: Zjhra et al., 2004; Crescentieae and the Tabebuia morphological traits. Testing hypotheses of generic mono- alliance: Grose and Olmstead, 2007a) However, these studies phyly was largely beyond the scope of this study. A good have lacked much detail due to limited sampling for many understanding of major lineages and relationships among lineages (Olmstead et al., 2009). The study by Spangler and them provides a basis for subsequent studies on the Olmstead (1999) suggested that tribes Bignonieae, Coleeae comparative biology of Bignoniaceae. So, these results serve and Crescentieae were monophyletic, while Tecomeae were as basis to frame future studies of clades where additional not. Coleeae and Crescentieae, once considered to be a work is needed. single tribe on the basis of shared traits including fleshy indehiscent (e.g., Bentham and Hooker, 1876), were found not to belong together, confirming Gentry's (1976) 2. Materials and methods decision to keep them separate. In each of these studies, greater taxon sampling and additional sequence data pro- A total of 25 species of Bignoniaceae in Egypt was included in vide more detail on the phylogeny of those clades. this study (Table 1), along with Barleria cristata as outgroup. 174 beni-suef university journal of basic and applied sciences 3 (2014) 172e177

Identification was confirmed according to Bailey (1949), sessile (C. cujete) or winged (P. alata and P. cerifera). compo- Parrotta (2001) and Ross (2005). The taxa were further sition; simple (B. cristata, C. bignonioides and C. cujete), bifoliate (4 matched against dried specimens in the Herbaria of Ain taxa), trifoliate (Amphilophium paniculatum and P. cerifera), Shams University (CAIA) and Cairo University (CAI). Macro- palmate (T. guayacan and T. pentaphylla), imparipinnate (12 taxa), morphological attributes were extracted from fresh and her- bifoliate& trifoliate (Bignonia venusta), bipinnate & tripinnate barium specimens. The voucher specimens of the species (Millingtonia hortensis), simple, bifolaite and trifoliate (P. alata). collected have been deposited at (CAIA). Terminal leaflet; absent (B. cristata, C. bignonioides and C. cujete), Parsimony analyses were conducted on data sets of normal (17 taxa), in the form of simple in Bignonia mag- morphological traits using the program NONA 1.6 (Goloboff, nifica and B. purpurea, triforked tendril (4 taxa). Petiolule; absent 1993), preparation of data set matrices and only in six taxa. Lamina margin; entire (17 taxa), serrate or editing were achieved in WinClada Software (Nixon, 1999). All dentate (8 taxa), sinuate (M. hortensis). Lamina apex; acuminate phylogenetic analyses were conducted using heuristic searches. (19 taxa), acute (6 taxa), obtuse (P. cerifera). Lamina shape; ovate (6 taxa), obovate (B. magnifica), oblong ( T.a guayacan), lanceolate (9 taxa), cordate (A. paniculatum and C. 3. Results bignonioides), spathulate (C. cujete), elliptic (5 taxa). Inflorescence; spike (B. cristata), solitary (4 taxa), cymose (5 taxa), racemose (4 3.1. Macromorphological traits taxa), panicle (8 taxa), corymbose (Spathodea campanulata and S. niolotica), mixed (Tecoma capensis and T. shirensis). Calyx shape; The macromorphological characters of all the studied taxa in tubular (4 taxa), campanulate (12 taxa), cubular (4 taxa), spath- addition to their states and taxa versus characters data matrix like (5 taxa), bilabiate (P. alata). Calyx limb; toothed (6 taxa), were summarized in (Tables 2 and 3). The most informative and lobed (9 taxa), 2-parted (C. bignonioides and C. cujete), 3-lobed diagnostic morphological characters were: texture varied (Kigelia moosa, Markhamia hildebrandtii and M. platycalyx), cleft (4 between hairy in eight taxa, glabrous (13 taxa), rough in Par- taxa), frilled (A. paniculatum). Corolla shape; funnel (8 taxa), mentiera alata and P. cerifera,glandular(Markhamia platycalyx, tubular (5 taxa), campanulate (8 taxa), trumpet-shaped (Dox- Tabebuia guayacan and T. pentaphylla). The habit; (14 taxa) antha unguis-cati, K. africana and K. moosa), bell-shaped (Jacaranda or tree in the remainings. Strength; erect (17 taxa), climbing in acutifolia and M. platycalyx). Bilipped corolla; present only in the rest. Duration; evergreen (20 taxa) or in the others. seven studied taxa. Fertile ; four (24 taxa), two (C. Leaf arrangement; opposite (21 taxa), whorled ( bignonioides), four/five (T. capensis). ; absent (5 taxa), and P. alata), Opposite/Whorled (Catalpa bignonioides, Kigelia one (20 taxa), three (C. bignonioides). character; long in africana and Spathodea niolotica). Leaf ; petiolate (23 taxa), four or rudimentary in the remainings. Filament; exerted in

Table 2 e Morphological characters, their states and codes of taxa under investigation. Character Character state and its (code) 1. Plant texture Hairy (0) Glabrous (1) Rough (2) Glandular (3) 2. Habit Shrub (0) Tree (1) 3. Strength Erect (0) Climbing (1) 4. Duration Evergreen (0) Deciduous (1) 5. Leaf arrangement Opposite (0) Whorled (1) Opposite/Whorled (2) 6. Leaf petiole Petiolate (0) Sessile (1) Winged (2) 7. Leaf composition Simple (0) Bifoliate (1) Trifoliate (2) Palmate (3) Imparipinnate (4) Bifoliate þ Trifoliate (5) Bipinnate þ Tripinnate (6) Simple þ Bifolaite þ Trifoliate (7) 8. Terminal leaflet Absent (0) Normal (1) Simple tendril (2) Triforked tendril (3) 9. Petiolule Absent (0) Present (1) 10. Lamina margin Entire (0) Serrate or Dentate (1) Sinuate (2) 11. Lamina apex Acuminate (0) Acute (1) Obtuse (2) 12. Lamina shape Ovate (0) Obovate (1) Oblong (2) Lanceolate (3) Cordate (4) Spathulate (5) Elliptic (6) 13. Inflorescence Spike (0) Solitary (1) Cymose (2) Racemose (3) Panicle (4) Corymbose (5) Mixed (6) 14. Calyx shape Tubular (0) Campanulate (1) Cubular (2) Spath-like (3) Bilabiate (4) 15. Calyx limb Toothed (0) Lobed (1) 2-parted (2) 3-lobed (3) Cleft (4) frilled (5) 16. Corolla shape Funnel (0)Tubular (1) Campanulate (2) Trumpet-shaped (3) Bell-shaped (4) 17. Bilipped corolla Absent (0) Present (1) 18. Fertile stamens no. Four (0) Two (1) Four-five (2) 19. Staminodes no. Absent (0) One (1) Three (2) 20. Staminode character Absent (0) Rudimentary (1) Long (2) 21. Filament elongation Included (0) Exerted (1) 22. 2-celled (0) 1-celled (1) 23. shape Ellipsoide (0) Linear (1) Oblong (2) Globular (3) Cylindrical (4) Lanceolate (5) 24. Fruit (0) (1) 25. wing Absent (0) Present (1) beni-suef university journal of basic and applied sciences 3 (2014) 172e177 175

Table 3 e Data matrix of 25 Morphological characters and their states (91) of the studied taxa. TC 12345678910111213141516171819202122232425 10000002310043151100000201 21010001310122101101100101 31010004100033111001100201 41010001200112102001100101 50010004210132200001100101 61010005310032201001110101 71011004111134112001100201 81101200000144022012100201 91100110000051022001101310 101010001311031113001100201 111101006110034104001200301 121100204111064113100001410 130000004110164133001111410 141100004110004332001100101 153100004111064334000000101 160100006112034201001110111 172100127100001442101211310 182000022111261340001110410 190101004110065342001100501 200100204110005342001110501 213101003110022010001100201 223101003110033210001100201 231010004111006110121110101 240010004111006110100000201 251000004111033110101100101 260000000000000000000000000

seven taxa or included in the rest. Ovary; 1-celled in four taxa or Bignoniaceae, there is support for monophyly of lineages 2-celled in the remainings. Fruit shape; ellipsoide (B. cristata), (IIeVIII) together through the synapomorphic characters viz. linear (8 taxa), oblong (4 taxa), globular (C. cujete and P. alata), leaf composition, the nature of the terminal leaflet and the cylindrical (K. africana, K. moosa and P. cerifera), lanceolate (S. presence of the petiolule. In addition, there is a support for a campanulata and S. niolotica), flat (B. purpurea), elongated (Campsis sisteregroup relationship between these lineages and lineage grandiflora, C. bignonioides and Doxantha unguis-cati), ovate (A. I. In phylogenetic context, eight clades in Bignoniaceae are paniculatum), orbicular (J. acutifolia). Fruit type; berry in five taxa recognized based on the analyses of chloroplast sequences or capsule in the rest. Seed wing; present only in 20 studied taxa. (Olmstead et al., 2009). C. bignonioides and C. cujet are contained in lineage I 3.2. Cladistic analysis (Bootstrap value ¼ 50) owing to a synapomorphic character; three-lobed calyx limb. On the other hand, Jianhua (2008) and The obtained cladogram (Fig. 1) shows that within the studied Olmstead et al. (2009) confirmed the isolation of Catalpa in one taxa of Bignoniaceae there is support for eight lineages viz. lineage and Crescentia in another. lineage I (C. bignonioides and Crescentia cujet), lineage II (A. In lineage II, the basal position of A. paniculatum is sup- paniculatum, Doxantha unguis-cati, B. capreolata and B. magnifica), ported, as is the monophyly of Doxantha unguis-cati, B. capreo- lineage III (T. guayacan and T. pentaphylla), lineage IV (B. pur- lata and B. magnifica as a group. The two latter studied species purea and B. venusta), Lineage V (, T. capensis and T. of Bignonia are closely related than Doxantha unguis-cati. shirensis), lineage VI (J. acutifolia and M. hortensis), lineage VII These two species and Amphilophium are contained in (M. hildebrandtii, P. alata and S. niolotica) and the last lineage one lineage (Bignonieae) according to Olmstead et al. (2009). A. comprises (M. platycalyx, S. campanulata, P. cerifera, K. africana paniculatum is marked with autapomorphic character; frilled and K. moosa). Bignonia jasminoides occupied the basal position calyx limb. There is a sisteregroup relationship between for lineages (VeVII) and the basal position of C. grandiflora in lineage II and the subsequent lineages that show a monophyly relation to lineages VI, VII and VIII is supported. owing to synapomorphic character viz. leaf composition. Lineage III that includes the two studied species of Tabebuia shows a strong support for monophyly (BS ¼ 75) as well as B. 4. Discussion purpurea and B. venusta that included within lineage IV. In phylogenetic context, the present study revealed that genus The comprising all Bignoniaceae receives 100% boot- Bignonia is not monophyletic taxa. B. venusta is marked with strap support, expressing strong support for the monophyly of possess of bipinnate and tripinnate as autapomorphic the family. Among the obtained eight lineages of character. A detailed phylogenetic study of Bignonieae that 176 beni-suef university journal of basic and applied sciences 3 (2014) 172e177

Fig. 1 e Cladogram based on morphological traits of Bignoniaceae comprising eight lineages.

sampled one-third of all species indicated that the majority of synapomorphic character. M. hortensis is marked with the the traditionally recognized genera are not monophyletic autapomorphic character sinuate leaf margin. According to (Lohmann, 2006). Olmstead et al. (2009), these genera were included in distinct The basal position of B. jasminoides in relation to lineages V, three lineages. VI, VII and VIII is supported, as is the monophyly of these M. hildebrandtii occupied the basal position to P. alata and corresponding lineages. The three studied species of Tecoma S. niolotica that have a close relationship. This lineage is a are included within lineage V. The basal position of Tecoma sister to lineage VIII through the synapomorphic characters stans is supported as is the monophyly of T. capensis and T. of calyx traits. Within lineage VIII, the basal position of M. shirensis (BS ¼ 72) through the presence of mixed inflorescence platycalyx ia supported, as is the monophyly of S. campanulata, as synapomorphic character. T. capensis is marked with P. cerifera, K. africana and K. moosa as a group, the fruit shape autapomorphic character; four or five fertile stamens. The as synapomorphic character marked this monophyletic present study revealed that Tecoma is monophyletic genus, group. It is revealed that Markhamia, Parmentiera and Spatho- this is not comparable to Olmstead et al. (2009) where para- dea are not monophyletic genera while Kigelia is mono- phyly of this group is confirmed, expressing that the studied phyletic genus. According to Olmstead et al. (2009), Kigelia, genus clearly merit additional study using more criteria and Parmentiera and Spathodea are contained in one clade (Paleo- more species. tropical clade). C. grandiflora rooted three lineages VI, VII and VIII as a group, the monophyly of these lineages is supported. There is a sisteregroup relationship between lineage VI and the 5. Conclusion remaining two lineages. The monophyly of lineage VI including J. acutifolia and M. hortensis is supported owing to the It is concluded that Bignoniaceae are monophyletic family presence of simple, bifoliate and trifoliate leaves as comprising eight lineages, the two studied species of Tabebuia beni-suef university journal of basic and applied sciences 3 (2014) 172e177 177

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