Pollen morphology and ultrastructure of Quercus with focus on Group Ilex (=Quercus subgenus Heterobalanus (Oerst.) Menitsky): implications for oak systematics and evolution

Abstract

It has been suggested that pollen ornamentation can be used to distinguish infrageneric groups in Quercus. Here, we document pollen morphology of nearly all species of Quercus Group Ilex and show that they share distinctive microrugulate pollen ornamentation. Furthermore, pollen ultrastructure of all six infrageneric groups of Quercus was studied comparatively and evaluated using a phylogenetic framework for Fagaceae. Characteristics of the foot layer, such as its thickness and continuity, and the ratio foot layer to tectum are not stable within infrageneric groups of Quercus. The foot layer in derived groups (Groups Cerris, Quercus, Lobatae) is irregular, discontinuous and thin (type 2 foot layer). Members of Groups Cyclobalanopsis and Ilex either have a regular, continuous, and comparatively thick foot layer (type 1), or a type 2 foot layer. Only Group Protobalanus consistently has a type 1 foot layer and is similar to Trigonobalanus and Colombobalanus among trigonobalanoids, and to castanoids. Because (I) all except for one species of Castanea and Nothofagus have a type 1 foot layer and (II) basal groups in Quercus may have a type 1 foot layer, we suggest that this is the ancestral state in Fagaceae, and that the type 2 foot layer of Fagus is derived.

Keywords:

• Quercus Group Ilex
• evolution
• pollen ornamentation
• foot layer

Acknowledgements

The authors want to thank the staff of the herbarium Edinburgh and Berkeley for providing male flowers. This work was supported by a grant of the Swedish Research Council to TD and by a RFBR grant #12-04-01740, МК-3156.2014.4 to MVT.

Specimens investigated

Group Ilex: Quercus acrodonta, G. Forrest 16522 (E); Q. alnifolia, P. H. Davis s. n. (E), Foggie 215 (E), A. Foggie s. n. (E); Q. aquifolioides, G. Forrest 100026 (E); Q. aucheri, P. H. Davis 8007 (ISTO), E. Özhatay 19257 (ISTO); Q. baloot, J. E. T. Aitchison 262:128:25:87 (S), S. A. Bowes Lyon 616 (E), W. Koelz 8222 (E); Q. baronii, G. H. Yang 58623 (PE), Forestry School of Mei County, Shaanxi Province 05104572 (NF); Q. coccifera, F. S. Meyers, J. E. Dinsmore B7123/3123 (S), J. E. Dinsmore 9122, B3122 (S), J. E. Dinsmore 7124C (S), H. Lenander 23-4-1936 (S), G. Een 22-4-1952 (S), P. H. Davis 7959 (ISTO), E. Özhatay 19820 (ISTO), E. Wall 9-5-1933 (S), G. Erdtman 8.5.49 (S), Valbonne 1891 (S), Lorch 1953 (S); Q. cocciferoides, Handel-Mazzetti 3632 (E), P. Simeon Ten. 45 (E), P. Simeon Ten. 246 (E); Q. dilatata, A. Andersson 4–1915 (E), Duthie 12949 (E); Q. engleriana, E. H. Wilson 3633 (E); Q. franchetii, A. Henry 9298A (E), T. Smitinand, I. Alsterlund 6781_24519 (E); Q. gilliana, G. Forrest 2056 (E), Handel-Mazzetti 1556 (E); Q. guyavifolia, D. Chamberlain et al. 004 (E); Q. ilex, A. Uggla 20-4-1936 (S), Anisits 30-5-1911 (S), I. Segelberg 19-5-1964 (S), ISTF 17026 (ISTF), H. Lenander 18-5-1933 (S), Torrelodones 1949 (S), Firenze 1873 (S), de Wilde & Dorgelo 2592 (S), J. H. Vijk s. n. (S); Q. kingiana, C. C. Hosseus 300_282 (E); Q. lanata, F. G. Dickason 8435 (E), Kumrun s.n. (E), H. B. Garrett 1175 (S); Q. leucotrichophora, J. D. A. Stainton 207 (E); Q. lodicosa, G. Forrest 26611 (E); Q. longispica, G. Forrest 21318 (E); Q. monimotricha, E. H. Wilson 3626 (E); Q. pannosa, ACE 506 (E); Q. phillyreoides, Det. O. Schwarz 27-4-1911 (S), M. Takeoka s. n. 26/4/1976 and 4/5/1977 (S), Murata & Koyama s. n. 25/4/1965; Q. rehderiana, J. F. Rock 24264 (E), E. E. Maire s. n. (E); Q. semecarpifolia, J. E. T. Aitchison 394 (S), Parkinson 4363 (S); Q. senescens, D. Chamberlainet al. 159a (E), F. Ducloux 1265 (E); Q. spathulata (syn. Q. dolicholepis A. Camus), G. Forrest 12397 (E), E. H. Wilson 3625 (E); Q. spinosa, E. H. Wilson 1493 (E).

Group Cerris: Quercus acutissima, J. F. Rock 2451 (E), S. K. Lau 3173 (E); Q. brantii, H. E. Wright et al. 6323 (E), O. Polunin, Khudairi 16 (S); Q. castaneifolia, P. Sintensis 1485a (E); Q. cerris, Jerusalem Botanical Garden, M. J. E. Coode, B. M. G. Jones 6426 (ISTO), N. Lundqvist 14364 (S); Q. libani, R. Wheeler Haines 18-7-1961 (E); Q. ithaburensis subsp. macrolepis, K. H. Rechinger 22299 (S); Q. suber, Fernanes & Sousa 1590, 5/5/1947, E. Wall 5 (S), H. Lenander 9-5-1928 (S); Q. variabilis, E. Dahlström 5-4-1947 (S).

Group Quercus: Quercus arizonica, E. Palmer 77 (UC); Q. brandegei, H. S. Gentry 4361 (UC); Q. bumelioides, R. L. Rodgriquez 346 (UC), A. Smith s. n. 19/02/1940 (UC); Q. dentata, E. E. Maire 1475_1913 (E); Q. douglasii, P. S. Woolsey & G. M. Tucker 1898 (UC); Q. fabri, Kingdon Ward 5094 (E), Xiao Bai Zhong 3393 (E); Q. faginea, P. H. Davis 50823 (E); Q. frainetto, F. Schultz 917 (S), Pancic 14-4-1985 (S), Wierzbicki 917 (S); Q. garryana, J. P. Tracy 6008 (UC), J. P. Tracy 15915 (UC); Q. griffithii, F. G. Dickason 7385 (E); Q. infectoria subsp. veneris, Jerusalem Botanical Garden, Q. kelloggii, J. P. Tracy 4895; Q. macranthera, ISTO 29084 11/6/1974 (ISTO), A. H. & V. F. Brotherus 775 (S), Kozlowski (S), P. Sintensis 4197 (S); Q. michauxii, fresh material, Gainesville USA; Q. petraea, Sochi Botanical Garden, E. Rastan 1880 (S), B. Wallnöfer 13566 (E); Q. pontica, E. K. Balls 412 (E); Q. pyrenaica, O. Cyren 4-6-1928 (S), G. Lidman 1806 (S); Q. robur, Jerusalem Botanical Garden, J. Vetter 8-5-1932 (S), T. Symonowiczówna (S); Q. tuberculata, A. Carter & J. Reese 4566 (UC), T. T. Marshall. Jr. 118; Q. virginiana, E. J. Palmer 9199 (S).

Group Lobatae: Quercus canbyi, R. M. King 4543 (UC), Q. humboldtii, J. L. Zarucchi, G. McPherson, J. Koldán 7293 (UC), Q. laevis, fresh material, Gainesville USA; Quercus nigra, fresh material, Gainesville USA.

Group Cyclobalanopsis: Quercus acuta, C. Wilford s. n. (S); Q. augustinii, F. Ducloux 993 (E), G. Forrest 24033 (E), G. Forrest 26600 (E); Q. championii, T. Ying 0243 (E); Q. fleuryi, W. T. Tsang 26676 (E); Q. glauca, H. Togasi 1040 (S); Q. helferiana, J. F. Rock 2662 (E); Q. longinux, fresh material, Sochi Botanical Garden

Group Protobalanus: Quercus chrysolepis, A. D. E. Elmer 4539 (E), Lewis S. Rose 41236 (S), H. E. & S. T. Parks 24129 (S); Q. tomentella, Blanche 317 (E), E. K. Balls 11863 (S); Q. vaccinifolia, E. K. Balls 11107 (S), A. A. Heller 6980 (E), A. A. Heller 10938 (E).