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Comparative leaf anatomy and phylogeny of Syzygium Gaertn.

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Abstract

The leaf anatomy of 81 species of Syzygium was examined. General generic and subgeneric descriptions of Syzygium leaf anatomy are given. Four stomatal types (anisocytic, anomocytic, cyclo-staurocytic and paracytic) that occur exclusively or in combinations are recognised. Two major vascular systems are differentiated by the presence or absence of adaxial phloem partition. Phylogenetic inferences using maximum parsimony and Bayesian methods for separate and combined analyses of DNA (ETS and ITS) sequences and morphological (leaf anatomy and macromorphology) data were conducted. Results of the combined analyses gave slightly higher support value for clade than analyses based on DNA sequences. The subgenera Perikion, Sequestratum and Syzygium are strongly supported, but the subgenus Acmena is moderately supported in the Bayesian but not in the parsimony analysis of combined data sets. The relationships among subgenera are not fully resolved. All the leaf anatomical characters examined are homoplastic. We did not find any unique leaf anatomical characters allowing delimiting of the four subgenera in Syzygium. However, a combinations of non-unique leaf anatomical characters, including stomatal types, crystal types and frequency, and midrib vascular system (adaxial phloem partition) are diagnostic for subgeneric groups.

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Notes

  1. Wilkinson (1979) extended Metcalfe and Chalk’s (1950) stomata classification by differentiating actinocytic from cyclocytic types. The term cyclocytic, proposed by Stace (1965), is actually an extension of actinocytic stomata types that was originally proposed by Metcalfe and Chalk (1950). Wilkinson (1979) added that the subsidiary cells of actinocytic stomata are radially elongated; this implies that the radial diameters of the cells are bigger than their tangential width and that the subsidiary cells of cyclocytic are the opposite (therefore, the tendency to form narrow rings). In this study, we consider actinocytic and cyclocytic to be the same stomatotype and that they are probably variants of one another. The term cyclocytic was used here in Syzygium because of the tendency of these stomata towards cyclocytic form, in having subsidiary cells that vary from equal width and height to wider than high. Van Cotthem (1970) introduced the term staurocytic and defined it as "stoma surrounded by four (sometimes three or five) similar subsidiary cells with anticlinal walls arranged crosswise to the guard cells; subsidiary cells more or less radially elongated; the ‘cross’ randomly orientated to the long axis of the pore". Later, Wilkinson (1979) broadened the term by adding ‘the cell walls at the right angles to the long axis of the pore are variously oriented’ after she considered anomotetracytic stomata of Dilcher (1974) as a variant form of staurocytic stomata. Dilcher (1974) differentiated anomotetracytic from staurocytic in having subsidiary cells that are not arranged strictly crosswise, but irregular and variable in pattern. In this study, there was an intergrading characters of cyclocytic and staurocytic stomatal types, and hence the term cyclo-staurocytic was used.

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Acknowledgments

This work was largely funded by the Trinity College Dublin under the Trinity College Postgraduate Award. A special thanks to SYNTHESYS (European Union-funded Integrated Infrastructure Initiative grant) for funding research visits to the herbarium in Paris. Many thanks to Ursula King, who has contributed in collecting some of the leaf anatomy and molecular data. The following are thanked for their advice on the molecular analyses: Trevor Hodkinson, Mark Harrington, Ed Biffin, Peter van Welzen and Peter Hovenkamp. A big thanks to Liam Furlong for the graphics. We are very grateful to the Curators of KKU, L, P and BKF herbarium for providing material for our study. We are grateful to Pieter Baas for his advice and comments on the leaf anatomy data.

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Correspondence to Wuu Kuang Soh.

Appendices

Appendix 1

Samples used in the leaf anatomy study. The format follows species, distribution, collector’s name and number and herbarium duplicate. Abbreviation for geographical distribution follows: AUS Australia, BOR Borneo, CBD Cambodia, CHH Hainan, CHS China South East, IND India, JAW Jawa, LAO Lao PDR, MAL Peninsular Malaysia, NWC New Caledonia, NWG Papua New Guinea, PHI Philippines, SUM Sumatra, THA Thailand, VIE Vietnam.

Piliocalyx francisii Guillaumi: NWC—H.S. McKee 8185 (L). Syzygium abortivum (Gagnep.) Merr. & L.M.Perry: LAO—Thorel s.n. (P); THA—Thorel s.n. (P); VIE—Squire 106 (P), Vidal 795A (P). S. acuminatissimum DC.: CHS—Tsang 2714 (P); THA—Beusekom & Phengklai 842 (BKF), Kerr 8749 (TCD). S. aksornae P.Chantaranothai & J.Parn.: MLY—King 5780 (TCD);THA—Kerr 12238 (TCD). S. angkae (Craib) P.Chantaranothai & J.Parn.: THA—Fenelly 7 (TCD), H.B.G. Garrett 1120 (TCD); VIE—Martin M.A. 936 (P), Vidal 794A (P). S. antisepticum (Wight) S.N. Mitra: CBD—Martin 164 (P), Smitinand & Abbe 6489 (BKF); MLY—King 5433 (TCD); PHI—Hutchinson 7548 (L); THA—Fenelly 16 (TCD), Kerr 9799 (TCD), Kerr 9799 (TCD). S. apodophyllum (F.Muell.) B.Hyland: AUS—Hyland 9176 (L), Irvine 821 (L). S. araiocladum Merr. & L.M.Perry: VIE—Tsang 29081, Tsang 30349 (P). S. attenuatum (Miq.) Merr. & L.M.Perry: THA—Kerr 11785 (TCD), Phusomsaeng 245 (BKF), Ploenchit 291 (BKF). S. attopeuense (Gagnep.) Merr. & L.M.Perry: LAO—Tixier 2235708 (P); THA—Phengnaren et al. 95 (BKF); VIE—Rejamanek s.n. (P); Schmid s.n. (P). S. balsameum Wall. ex A.M. & J.M.Cowan: THA—Beusekom & Phengklai 2580 (BKF), Kerr 920 (TCD); VIE—Balansa 2878 (P). S. bankense (Hassk.) Merr. & L.M.Perry: BOR—Endert 1584 (L), S 41554 (L), SAN 86080 (L); JAW—Ploem s.n. (L); SUM—bb. 14399 (L); Kostermans 760 (L); Bogor cult. V.B116 (L). S. bicolor Merr. & Perry: NWG—Hartley 1200 (L), NGF 41971(L). S. boisianum (Gagnep.) Merr. & L.M.Perry: VIE—Petelot 6202 (P), Petelot 6274 (P), Tsang 27341 (P), Tsang 30728 (P). S. borneense (Miq.) Miq.: CBD—Martin 182 (P); LAO—Vidal 2223 (P); THA—Kerr 17298 (BKF); VIE—Tsang 29839 (L). S. bullockii (Hance) Merr. & L.M.Perry: CHH—Lei 1022 (P); VIE—J. & M.S. Clemens 3716 (P), Lecomte & Finet 883 (P), Pierre 1870 (P). S. campanulatum Korth.: THA—Emer END16 (KKU); THA—Kerr 16304 (BKF); THA—Chantaranothai & Kantachot 463 (KKU). S. canicortex B.Hyland: AUS—Hyland 10155 (L), Irvine 1694 (L). S. championii (Benth.) Merr. & L.M.Perry: VIE—Tsang 26910 (P), Tsang 27174 (P), Tsang 27222 (P). S. claviflorum (Roxb.) Wall ex Steudel: CBD—Chevalier 31723 (P); THA—Parnell, Chayamarit, Pooma, Simpson, Suddee & B. de Wilde 1851 (TCD); VIE—Balansa 2880 (L), Pierre s.n. (P), VN 1368 (Schmid) (P). S. corynanthum (F.Muell.) L.A.S.Johnson: AUS—Hyland 4121 R.F.K. (L), Hyland 9795 (L). S. cryptophlebium (F.Muell.) Craven & Biffin: AUS—Balgooy 1505 (L), Gray 678 (L), Hyland 8320 (L), Irvine 1284 (L), Smith & Pedley 11042 (L). S. cuminii (L.) Skeels: CBD—Petelot 3190 (P), Pierre 3190 (P); LAO—Tixier 1735609 (P), Vidal 2202 (P); VIE—Petelot 4679 (P), Petelot 6394 (P), Thorel s.n. (P). S. diospyrifolium (Wall. ex Duthie) S.N.Mitra: THA—Santisuk s.n. (BKF 100184) (BKF); VIE—Balansa 2865 (P), Chevalier 30093 (P). S. divaricatum (Merr. & L.M.Perry) Craven & Biffin: AUS—Hyland 3165 R.F.K. (L), Hyland 8800 (L). S. fastigiatum (Blume) Merr. & L.M.Perry: THA—K. & S. Larsen 32708 (TCD), Kerr 16843 (TCD), Kerr 18155 (TCD); VIE—Pierre s.n. (P). S. formosum (Wall.) Masam.: THA—Chantaranothai, Parnell, Simpson & Pooma 90/590 (TCD), Fennelly 13 (TCD); VIE—Vu Van Cuong 434 (P). S. francisii (Bailey) L.A.S.Johnson: AUS—Hyland 6677 (L), Smith 05150 (L). S. grande (Wight) Walp.: THA—Chataranothai, Parnell & Simpson 90/548 (TCD), Kerr 14000 (TCD), Parnell, Chayamarit, Pooma, Simpson, Suddee & B. de Wilde 1869 (TCD); VIE—Pierre s.n. (P). S. graveolens (F.M.Bailey) Craven & Biffin: AUS—Gray 2048 (L), Irvine 1447 (L). S. gustavioides (F.M.Bail.) B.Hyland: AUS—Hyland 3220 R.F.K. (L), Hyland 8777 (L). S. hancei Merr. & L.M.Perry: CBD—Middleton & Monyrak 623 (TCD); CHS—Tsang 26695 (P); THA—Chantaranothai, Parnell, Simpson & Sridit 90/225 (TCD); VIE—Petelot 2596 (A), Pierre s.n. (P), Tsang 27389 (P). S. harmandii (Gagnep.) Merr. & L.M.Perry: CBD—Hahn s.n. (P). S. hedraiophyllum (F.Muell.) Craven & Biffin: AUS—Hyland 9290 (L), Irvine 1681 (L). S. hemisphericum (Walp.) Alston: CBD—Diffon 509 (P), Magnen, Gourgand & Châtillon 7 (P); THA—Smitinand 10351 (BKF); VIE—Pierre s.n. (P). S. imitans Merr. & L.M.Perry: VIE—Tsang 26890 (P), Tsang 27232 (P), Tsang 30415 (P). S. jambos (L.) Alston: LAO—Spire 1025 (P); VIE—Balansa 2862 (P), Chevalier 30092 (P). S. jasminifolium (Ridl.) P.Chantaranothai & J.Parn.: MLY—FRI 17545 (L); THA—Sangkhachand, Phusomsaeng & Nimanong 1073 (BKF). S. khaoyaiense (P.Chantaranothai & J.Parn.) Craven & Biffin: THA—K. Larsen 10316 (BKF). S. kinabaluense (Stapf) Merr. & L.M.Perry: BOR—RSNB 194 (L), RSNB 4743 (L), RSNB 5884 (L), S 35823 (L), S 44469 (L), Smith 508 (L). S. levinei (Merr.) Merr.: VIE—Balansa 2887 (P), Balansa 2891 (P), D’Alleizette s.n. (L). S. lineatum (DC.) Merr. & L.M.Perry: CBD—Martin 1085 IREFC M37 (P), Martin 1676 (P); LAO—Harmand 252 (P); THA—Kerr 9283 (TCD). S. luehmannii (F.Muell.) L.A.S.Johnson: AUS—Hyland 9207 (L), Irvine 1639 (L); NWG—Brass 24853 (L). S. mackinnonianum (B.Hyland) Craven & Biffin: AUS—Hyland 11162 (L), Hyland 3310 R.F.K. (L). S. malaccense (L.) Merr. & L.M.Perry: LAO—Harmand 48 (P); VIE—Petelot 3387 (P), Thorel 311 (P). S. megacarpum (Craib) N.C.Rathakrishnan & N.C.Nair: LAO—Vidal 2577 (P); THA—Chantaranothai, Parnell & Simpson 90/432 (TCD), Fenelly 12 (TCD), Parnell, Chayamarit, Pooma, Simpson, Suddee & B. de Wilde 2032 (TCD). S. mulgraveanum (B.Hyland) Craven & Biffin: AUS—Hyland 8900 (L), Hyland 9248 (L). S. multibracteolatum (Merr.) Merr. & L.M.Perry: BOR—S 124475 (L), S 35667 (L), S 36624 (L), S 44292 (L). S. multipetalum Pancher ex Brongn. & Gris: AUS—Ingle I.71 (L). S. nervosum DC.: CHS—Tsang 26778 (P); THA—Maxwell s.n. (BKF 090782) (BKF); VIE—Balansa 2871 (P). S. nigrans (Gagnep.) Craven & Biffin: THA—Murataet, Phengklai, Mitsuta, Nagamasu & Nantasan 37145 (BKF); VIE—D’Alleizette s.n. (L), Pierre s.n. (P), Thorel s.n. (P). S. nummularium Airy Shaw: BOR—Richard 1981 (L), Richard 2417 (L), S 40942 (L). S. oblatum (Roxb.) Wall. Ex A.M. Cowan & Cowan: CBD—Magnen, Gourgand & Chatillon s.n. (P), Martin 1567 (P); THA—Collin 1368 (TCD), Geesink et al. (L), Parnell et al. 2044 (TCD); VIE—D’Alleizette s.n. (L), Martin 943 (P). S. odoratum DC.: VIE—J. & M.S. Clemens 3778 (P), J. & M.S. Clemens 4215 (P). S. pachysarcum (Gagnep.) Merr. & L.M.Perry: CBD—Bejaud 569 (P), Herbier Forestier du Cambodge 505 (P), Magnen, Gourgand & Châtillon 2 (P); VIE—Pierre s.n. (P). S. phengklaii (P.Chantaranothai & J.Parn.) Craven & Biffin: THA—Phengklai 4020 (BKF). S. pierrei (Gagnep.) Merr. & L.M.Perry: VIE—Pierrei s.n. (P). S. polyanthum (Wight) Walp.: CBD—Vidal 5010 (P); VIE—Tsang 30136 (L), Vu Van Cuong 1586. S. polycladum Merr. & L.M.Perry: BOR—Clemens 34208 (L), Clemens 40690A (L), Clemens 40692A (L), S 29020 (L). S. praecox (Roxb.) N.C.Rathakrishnan & N.C.Nair: THA—Kerr 17007 (TCD), Phusomaeng & Pinnin 318 (BKF); VIE—Schmid s.n. (P), Tsang 30757 (L). S. pterophorum Merr. & L.M.Perry: BOR—Clemens 29470 (L), Clemens 32012 (L), Clemens 33047 (L), Clemens 33047 (L). S. ripicola (Craib) Merr. & L.M.Perry: CBD—Bejaud 562 (P): VIE—Beusokom & Phengklai 106 (P), d’Alleizette s.n. (L), Schmid s.n. (P), Vu Van Cuong 278. S. sclerophyllum Thwaites: CBD—Dy Phon 1141 (P), Martin 806 (P), Stone B.C. 9264 (L), Vidal 4798 (P). S. siamense (Craib) P.Chantaranothai & J.Parn.: THA—Kerr 12565A (TCD), Kerr 598 (TCD); VIE—Bon 4191 (P), Chevalier 29923 (P). S. smithii Nied.: AUS—Hyland 11365 (L), Hyland 3134 R.F.K. (L). S. stapfianum (King) I.M.Turner: MLY—Wray-Smith KEP 79154 (L). S. sterrophyllum Merr. & L.M.Perry: CBD—Bansok 92 (BKF); CHS—Tsang 26735 (P); VIE—Balansa 1149 (P), Tsang 30189 (P). S. syzygioides (Miq.) Merr. & L.M.Perry: THA—Maxwell 85-123 (BKF); VIE—d’ Alleizette s.n. (L), Pierre s.n. (barcode P00589397) (P), Pierre s.n. (P). S. tenuirame (Miq.) Merr.: JAW—HB 834 & 843 (L); PHI—Bureau Science 34495 (Ramos & Pascasio) (L), Bureau Science 34709 (Ramos & Pascasio) (L); SUM—Teysman s.n. (L), Unknown s.n. (L). S. tephrodes (Hance) Merr. & L.M.Perry: CHH—Hendry 8086 (P), Lei 10 (P), Wang 33411 (P). S. tetragonum (Wight) Walp.: IN—J.D. Hooker s.n. (P); THA—Fenelly 5 (TCD); VIE—Petelot 6303 (P); VH 2934 (P). S. tetrapterum (Miq.) P.Chantaranothai & J.Parn.: JAW—Cultivated Bogor V B.70 (L); MLY—Mohd. Shah 2283 (L), SFN 38935 (L). S. thorelii (Gagnep.) Merr. & L.M.Perry: LAO—Thorel 3010 (P), Vidal 2786 (P), Vidal 2520 (P); THA—Kerr 20698 (TCD). S. tonkinense (Gagnep.) Merr. & L.M.Perry: VIE—Bon 2969 (P). S. tsoongii (Merr.) Merr. & L.M.Perry: CHH—How, F.C. 70528 (P); VIE—Balansa 1148 (P), Balansa 1148 (P), Lecomte & finet (P). S. unipunctatum (B.Hyland) Craven & Biffin: AUS—Gray 667 (L), Hyland 7357 (L). S. vestitum Merr. & L.M.Perry: LAO—Vidal 5696 (P); VIE—Petelot 6145 (P), Phengklai 10604. S. wilsonii (F.Muell.) B.Hyland: AUS—Dockrill 889 (L), Smith & Pedley 10193 (L). S. zeylanicum (L.) DC.: THA—Kerr 7083A (TCD), Kerr 15684 (TCD). S. zimmermannii (Warb.) Merr. & L.M.Perry: LAO—Spire 419 (P); THA—Kerr 20018 (BKF), Zimmermann 101 (L); VIE—Vidal 2521 (P).

Appendix 2

See Table 6.

Table 6 Source of plant material and GenBank Accession numbers for ITS and ETS nuclear DNA used in this study

Appendix 3

See Table 7.

Table 7 Data matrix of morphological data in the study

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Soh, W.K., Parnell, J. Comparative leaf anatomy and phylogeny of Syzygium Gaertn.. Plant Syst Evol 297, 1 (2011). https://doi.org/10.1007/s00606-011-0495-2

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