Phylogenetic analysis of the ()

Frederiksen, Signe Elisabeth; Seberg, Ole

Published in: Hereditas

DOI: 10.1111/j.1601-5223.1992.tb00198.x

Publication date: 1992

Document version Publisher's PDF, also known as Version of record

Citation for published version (APA): Frederiksen, S. E., & Seberg, O. (1992). Phylogenetic analysis of the Triticeae (Poaceae). Hereditas, 116(1-2), 15-19. https://doi.org/10.1111/j.1601-5223.1992.tb00198.x

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Phylogenetic analysis of the Triticeae ( Poaceae)

SIGNE FREDERIKSEN and OLE SEBERG

Botanical Laboratory, Copenhagen University, Copenhagen, Denmark

FKEDERIKSEN,S. and SEBERG,0. 1992. Phylogenetic analysis of the Triticeae (Poaceae). - Hereditas 116 15-19. Lund, Sweden. ISSN 0018-0661. Received August 2, 1991. Accepted December 24, 1991

A phylogenetic analysis, based on morphology, was made of the monogenomic genera of the Triticeae. Bruchypodiurn P. B. and Bromus L. were used as outgroups. No less than 1335 equally parsimonious trees were found (length 113, consistency index 0.33). The consensus tree does not support the monophyly of the Triticeae. Two well defined clades were found, a Hordeurn-clade and an Aegilops-clade. As the structure of the tree is only weakly supported, no taxonomic consequences are proposed.

Signe Frederiksen and Ole Seberg, Botanical Luboratory, Copenhagen Unruersiiy, Gothersgade 140, DK- I123 Copenhagen K, Denmark

A fundamental drawback of genome analysis is its Material and methods inability to reveal the phylogenetic relationships of the monogenomic groups, e.g., the genera defined Material from the following herbaria was studied: by having only a single genome. Even accepting BM, C, E, and K. The aim was to study 10-15 the basic principles of genome analysis, it is not different collections of each diploid species, but in possible to make a phylogenetic hypothesis taking a few cases less material was available. A few the diploid taxa into account (SEBERG1989). diploid species were, however, not available at all. Thus, the basic “building blocks” appear to be Data from Hordeum s. lat., Psathyrostachys, and largely unrelated, despite the general agreement Secale were obtained from N. Jacobsen, C. Baden, that the Triticeae is monophyletic ( MACFARLANEand G. Petersen, respectively. and WATSON 1982; WATSONet al. 1985; KEL- Diploid species representing genomically defined LOGG 1989; SEBERGet al. 1991). Unlike the genera (Table 2) were used as terminal taxa as the monogenomic taxa, the heterogenomic, polyploid genera were a priori supposed to be monophyletic taxa have a “known” history, as they are all pos- (KELLOGG1989). In cases where genera were tulated to be of allopolyploid origin. found to be morphologically heterogeneous and, BAUMet al. (1987) and KELLOGG(1989) have hence, probably non-monophyletic, they were split previously made phylogenetic hypotheses for the into smaller units. Triticeae. BAUM et al. (1987) used both the The Bromeae and the Brachypodieae were both monogenomic and the heterogenomic taxa in the used as outgroups, as they most probably are the cladistic analysis, and thus confounded the analy- closest relatives of the Triticeae ( MACFARLANE sis by including polyphyletic terminal taxa. KEL- and WATSON1982; WATSONet al. 1985; KEL- LOGG ( 1989) excluded the heterogenomic taxa LOGG 1989, 1992; SEBERGet al. 1991). Character from the phylogenetic analysis and added them as states found to be autapomorphies of terminal taxa reticulations on the final tree. Though KELLOGG’S were excluded, but a total of 31 morphological data matrix is a dear improvement in respect to characters were scored (Table 1). Most of them that of BAUMet al. (1987), both matrices suffer were binary, but a few have three or four states. from relying too heavily on the literature. All characters were treated as non-additive. 7 he present study follows the same basic Most character states were easily observed, but a scheme as KELLOGG’S(1989), but differs in taking few character states caused problems. On account more taxa into account and in a much more thor- of the occasionally incomplete material, the data ough study of herbarium specimens and live for each terminal taxon were compiled by using all . accessible collections. 16 s. FREDERIKSEN AND 0.SEBERG Hereditas 116 (1992)

Table 1. Characters and character states (-) Pseudoroegneria (S) 1. Longevity perennial/annual Lophopyrum (E) 2. Life form caespitose/stoloniferous 3. Shoots extravaginal/intravaginal Australopyrum (W) 4. Leaves auricles presentiauricles absent Erernopyrum (F) 5. Sheaths margins joined/not joined on vegetative Thinopyrum (J) shoots Agropyron (P) 6. Sheaths margins joinedinot joined on culm leaves (?) 7. Leaf blades folded/rolled Dasypyrum (V) 8. Spikelets homospiculate/heterospiculate (Hordeum- type)/heterospiculate (Hereronfhelium- Crithodium (A) type)/heterospiculate (Kiharopyrum-type) (G) 9. Spikelets embedded in rachis/more or less H et her ant hel iu m (a) protruding 10. Rachis disarticulating/tough Secale (R) Bromus (-) 11. Rachis disarticulating at every nodeinot so i 12. Rachis disarticulating above/below spikelets Taeniatherum (T) 13. Inflorescence short ( < 1/3 the spikelet length)/ Crithopsis (K) internodes long ( > 1/2 the spikelet length) Psathyrostachys (N) 14. Spikelets spikelets solitary/in pair/in triplets Critesion 1 (H) 15. Spikelets sessileilong pedicellate (infl. panicle)/lat- era1 subsessile, central sessile (Hordeum- Critesion 2 (H) type)/all subsessile (infl. spikelike raceme) Hordeurn (I) 16. Rachilla disatticulating/tough Amblyopyrum (Z) 17. Glumes ventricose/keeled/setaceous ( awnlike) Sitopsis 1 (6) 18. Glumes abaxial/lateral with respect to rachis Henrardia (0) 19. Glume-apex with 2-more lobesiwith I or without dents Patropyrum (D) 20. Glumes broadest in lower half-middleiin upper half Sitopsis 2 (B) 21. Glumes at least some awnediall awnless Orrhopygium (C) 22. Glume-apex nerves divergentinerves confluent Comopyrum (M) or nearly parallel Kiharapyrum (U) 23. Glumes 2-keeledil -keeled Chennapyrum (L) 24. Florets max. 2 per spikeletimore than 2 25. Lemma-apex with 2-5 lobes/with 1 or without dents Fig. 1. Consensus tree based on 1335 equally parsimo- nious trees. Genera and genome designations as in Table 26. Lemmas at least some awnediall awnless 1, except that Critesion 1 = C. murinum, Critesion 2 = 27. Lemmas keeled/ventricose C. bogdanii and C. brachyantherum, Sitopsis 1 = S. 28. Paled-apex bifidientire sharonensis, S. bicornis, and S. speltoides, and Sitopsis 29. Caryopsis adherentifree 2 = S. searsii and S. longissima. 30. Ovary with/without appendage 3 I. Chromosomes large, some telocentrics/large. only meta- NIG86. Accordingly, different permutations of the centrics/small input matrix were run and the strict consensus trees (Nelsen) made for each. In all runs, the consensus trees were similar.

The data-matrix shown in Table 2, based on the characters shown in Table 1, was used as input to Results HENNIG86 (FARRIS1988). Due to the size of the data-matrix only the heuristic algorithm (bb*) The individual trees were 113 steps long with a could be used in an attempt to find the shortest consistency index of 0.33. The consensus tree was, tree(s). The number (1335) of equally parsimo- as mentioned above, based on several different nious trees exceeded the storage ability of HEN- subsets of the 1335 equally parsimonious trees. It Herrdrtas 116 (1992) PHYLOGENY OF THE TRITICEAE 17

Table 2. OTU-Character matrix used as input to Hennig86. Genera, species and genome designations according to LOVE (1984). Concerning the characters 29 and 31 the following sources were consulted: KIMBERand FELDMAN( 1987); SCHULTZ-SCHAEFFER( 1956); CHENNAEVEERAIAH(1960); SCHULTZ-SCHAEFFERand JURASITS(1982); ENDOand GILL(1984); FREDERIKSEN (1986, 1991a,b); and SEBERG el al. (1991)

Taxon Character No. ~- 1-5 6-10 11-15 16-20 21-25 26-30 31

Brachypodium (-) pinnatum 12122 22122 --214 11221 22-22 I2222 3 silvaricum 11122 22122 --214 11221 22-22 12222 3 Bromus (-) porleri I1 121 12122 --212 11221 22-22 12221 ? kalmii I1 121 l2l22 --212 12221 22222 12221 ? gracillimus 21221 12122 --212 12221 22222 12221 ? japonicum 21221 12122 --212 11221 22-21 12221 2 remot @orus ?2121 1?122 --212 12221 22222 12221 ? Psarhyrostachys (N) ‘caespitose’ spp. 11211 2?121 11?31 1312- 1--12 12112 2 ‘stolonif.’ spp. 12?11 2?121 11?31 1312- 1--12 121 12 2 Critesion (H) murinum 21212 22222 21134 -1121 1--l2 12112 2 bogdanii 1222 2222? ?I 133 -312- 1--12 121 12 2 brachyanrherum 1222 22221 11133 -312- 1--12 12112 2 Hordeurn (I) uulgare ssp. spontaneum 1212 22221 11133 -1121 1--12 12112 2 Lophopyrum (E) elongatum 1212 22122 --21 I 11221 22-22 21212 2 Pseudoroegneria (S) libanotica -212 22 I22 --211 11221 22-22 222?2 2 tauri -212 2? I22 --21 I 11221 22-22 12222 ? sripifolia 1121? 2?122 --211 11221 22 - 22 222?2 2 srrigosa IIII? 22122 --211 11221 22 - 22 I22?2 ? spkata 11112 21122 --211 11221 12-22 122?2 2 Thinopyrum (J) bessarahieum 1212? 2?121 1121 I 11221 22-22 22222 2 Agropyron (P) pectiniforme 11211 21122 --Ill 12221 I2222 Illl2 2 Ausrralopyrum (W) uelurinum 11211 22122 --Ill 12221 22222 11212 2 retrofracrum 1 I21 I 22122 --Ill 12221 22222 12212 2 pectinatum 11211 22122 --I14 I222 1 22222 11212 2 Eremopyrum (F) disrans 2121 I 22121 11111 22221 12222 121 12 1 rririceum 2121 1 22 I22 --Ill 1222 1 12222 121 I2 1 Peridictyon (?) sanctum 11211 21122 --214 11221 22 - 22 12212 2 Festucopsis (G) serpentini 11221 22122 --214 11221 22 - 22 122?2 2 Crithopsis (K) delileana 21211 22121 11221 2322- 1--12 12212 2 Hereranthelium (Q) piliferum 21211 22321 21111 2322- 1 --22 121 12 2 Taeniarherum (T) capur -medusae 2121 I 22 I22 --I21 2312- 1--12 I2212 2 Henrardia (0) SPP. 2121 I 22111 12211 21121 22-12 22222 1 Dasypyrum (V) uillosum 21211 22121 11111 22221 12122 11222 2 Crirhodium (A) monococcum 2121 1 22121 11111 2221 1 221 -2 11222 2 Amblyopyron (Z) muticum 21111 22121 22211 21212 21-22 21212 2 Parropyrum (D) rauschii 2121 I 22111 12211 21221 22-22 12212 2 Kiharapyrum (U) umbellulatum 2121 I 22421 2-21 1 21212 1 1-21 12122 1 Comopyrum (M) comosum 2121 I 22121 2-21 I 21211 12-21 121 12 2 18 s FREDERIKSEN AND 0.SEBERC Herediras 116 (1992)

(Tuh/e 2, continued)

Taxon Character No

1-5 6- 10 11-15 16-20 21 --25 26-30 31

~ - Chennupyrum (L) uniuri.srurum 21212 2242 I 2-21 I 21211 12 21 21112 Orrhopjgium (C) raudarum 21211 22121 2-21 1 2121 I I2 21 21 I12 Siropsis (B) srursii 21211 2?121 2-211 21211 22 21 11122 longissima 21211 22121 2-21 1 21211 22 21 11112 .sharonrnsis 21212 22121 I121 I 2121 I 22 21 Ill12 hirornis 21212 22121 1121 I 21211 22 22 11112 .spelroides 21212 22121 --211 21221 22-21 I1212 Secule (R) ’annual’ spp. 21212 22121 11111 22221 12212 11222 ‘perennial’ ssp. I1212 22121 11111 22221 12212 11222

was 194 steps long and the consistency index was form a well defined clade within the with extremely low (CI = 0.19). In spite of the unre- simple starch grains as an autapomorphy (MAC- solved relationships between many of the terminal FARLANEand WATSON1982; WATSONet al. 1985; taxa, two well defined clades, the Hordeum -clade KELLOGG 1989). It has also been shown that and the Aegilops-clade, were consistently found. Pooideae is a monophyletic group sharing the fol- According to the consensus tree (Fig. I), lowing autapomorphies: large chromosomes, a ba- Brachypodium is the sister-group of a clade includ- sic chromosome number of 7, large linear hilum, ing both Bromus and the Triticeae. As the rela- lack of microhairs, and unvascularized lodicules tionships between Bromus and the Triticeae is (KELLOGGand CAMPBELL1987; SEBERGet al. unresolved, there is a possibility that the Triticeae 1991). It was proposed by SEBERGet al. (1991) is a non-monophyletic group. that the Brachypodieae is the sister group of the The Hordeum-clade (Fig. I), includes all termi- Triticeae while the Bromeae is the sister group of nal taxa with more than one spikelet per node the Brachypodieae plus the Triticeae. The hy- (char. 14). Moreover, the glumes of most taxa are pothesis was based on the view that spikelike in- setaceous (char. 17), a state otherwise only found florescences are more advanced than racemose in Heteranthelium. Psathyrostachys and Hordeum inflorescences, a point of view that gains support slat. are sister-groups sharing spikelets in triplets from outgroup comparison with the Pooideae as as a synapomorphy. The Hordeuni/Critesion-com- the outgroup. plex is a monophyletic group, united by the special In order to study the consequences of character arrangement and development of the spikelets. 15 and 31 they were split and recoded in accor- The Aegilops-clade (Fig. I), mostly includes the dance with this hypothesis, but it was found to diploid taxa of Aegilops slat. The clade is united have no influence on the consensus tree. by a combination of advanced character states: The two well defined clades found here were annuality, disarticulating rachis, tough rachilla, similar to clades found by KELLOGG(1989). Our and ventricose glumes. Apart from the taxa tradi- Hordeum -clade deviates from KELLOGG’Sby in- tionally included in Aegilops s.lat., Henrardia is cluding Psathyrostachys. The inclusion of Psathy- included in the clade, just as Amhlyopyrum, which rostachys within this clade is a good indication that in most modern Floras (e.g., BOR 1970; TZVELEVthe is relatively advanced and not primitive, 1976; MELDERIS1985) is retained as a genus of its as stated by BAUMet al. (1987). BAUMet al.’s own. (1987) use of Psathyrostachys as “outgroup” has previously been criticized by SEBERG( 1989). Our analysis does not support splitting of Hordeum into Discussion Hordeum sstr. and Critesion, as Critesion is found to be paraphyletic (Fig. 1). Our Aegilops-clade It has earlier been claimed that the Triticeae, the includes the same units as the corresponding clade Bromeae, and the Brachypodieae (the Triticanae) of KELLOGC(1989) although the tree topology is Hereditas 116 (1992) PHYLOGENY OF THE TRITICEAE 19 different. Thus, both Henrardia and Arnblyopyrurn BOISSIER,E. 1844. Diagnoses Plantarum Orientalium, I,? 73. - B. Hermann, Lipsia are part Of this 'lade' On account Of its very BOR, N. I. 1970. Gramineae. -In: Flora Iranica (ed K. H. deviating Henrardia is Often classi- RECHINGER),Akademische Druck u. Verlagsanstalt, Graz fied in its own subtribe, the Henrardiinae (cf. CHENNAVEERAIAH.M. S. 1960. Karyomorphologic and cytotaxo- 1984). nomic studies in Aegilops. - Acta fforti Gothoburgensis 23 T~~~~~~ 1976; ~6~~ The inclusion of 85-178 blyopyrum in the clade is in accordance with most ENDO,T. R. and GILL, B. s. 1984. The heterochromatin distribu- earlier authors (cf. BOI~SIER1844). Its relatively tion and genome evolution in diploid species of and Agropyron. - Can. J. Genet. Cytol. 26 669-678 primitive position is in accordance with and FARRIS,S, 1988, Hennig86 Reference. Version 1.5. - The Auhr MAJISU(1968), who regarded it as an ancient type FREDERIKSEN,S. 1986. Revision of Taeniatherum (Poaceae). - Nord. J. Bor. 6 389-397 be polyphyletic with s. speltoides, s. sharonensis, (poaceae), -Nard. J, B~~,11: 135-142 and S. bicornis as Sitopsis 1 in Fig. 1, and the FREDERIKSEN,S. 1991b. Taxonomic studies in Eremopyrum (Poaceae). - Nord. J. Bat. 11: 271-285 remaining 2 species, in Sitopsis 2. JONES, J. K. and MAJISU, B. N. 1968. The homology of Aegilops mutica chromosomes. - Can. J. Genet. Cytol. 10 620-626 Conclusion KELLOGG,E. A. 1989. Comments on genomic genera in the Triticeae (Poaceae). -Am. J. Bat. 76 796-805 This work was started as an attempt to make a KELLOGG,E. A. 1992. Restriction site variation in the chloroplast genomes of the monogenomic Triticeae. ~ Hereditas 116 phylogenetic hypothesis for the monogenomic gen- 43-47 era of the Triticeae, but the high level of homo- KELLOGG,E. A. and CAMPBELL, C. S. 1987. Phylogenetic analy- ses of Gramineae. - In: Grass Systematics and Euolution (eds plasy in the dataset, shown by the low consistency T. R. SODERSTROM,K. W. HILU,C. S. CAMPBELLand M.E. index, indicates a rather weakly supported struc- BARKWORTH),Smithsonian Institute Press, Washington DC, ture and, thus, no taxonomic consequences should London, P. 310-322 KIMBER,G. and FELDMAN,M. 1987. Wild Wheat. -Special yet be taken. Moreover, it has been impossible report 353, College of Agriculture, University of Missouri, Co- with the compiled data-matrix to support the lumbia monophyly of the tribe even if character LOVE,A. 1984. Conspectus Of the Triticeae. - Feddes Reperl. 95: 425 - 52 1 states were recoded. Despite these very negative MACFARLANE,T. D. and WATSON,L. 1982. The classification of conclusions we still believe it worthwhile to reflect Poaceae subfamily Pooideae. - Taxon 31: 178-203 MELOERIS,A. 1985. 12. Amblyopyrum Eig. -In: Flora of on the relationships of the Triticeae. Turkey. 9 (ed P. H. DAVIS),Edinburgh Unio. Press, Edinburgh, p. 232-233 SCHULZ-SCHAEFFER,J. 1956. Cytologische Untersuchungen in Acknowledgements. - We are grateful to our colleagues Dr. C. der Gattung 'ramus L. - '. Pflanzenzucht~35 297-320 Baden, Prof. N. Jacobsen and Dr. G. Petersen, Botanical Section, SCHULZ-SCHAEFFER,and JURASITS,p. 1982. Biosystematic the Royal Veterinary and Agricultural University, Copenhagen, investigations in the genus Agrwron. 1. Cytobichl studies of for information about Psathyrostachys, Hordeum and Secale. The 'pecies karyotypes. - Am. J. 'Ot. 49 940-953 Carlsberg Foundation is gratefully acknowledged for financial SEBERG, 0.1989. Genome phylogeny, and classifica- support. tion. - Syst. Euol. 166: 159-171 SEBERG,O., FREDERIKSEN,S., BADEN,C. and LINDE-LAURSEN, 1. 1991. Peridictyon, a new genus from the Balkan peninsula, and its relationship with Festucopsis (Poaceae). - Willdenowia References 21: 87-104 TZVELEV,N. N. 1976. Poaceae URSS. 1. - Nauk. Leningrad BAUM,B. R., ESTES,I. R. and GUPTA,P. K. 1987. Assessment of WATSON,L., CLIFFORD,H. T. and DALWITZ,M. J. 1985. The the genomic system of classification in the Triticeae. - Am. J. classification of Poaceae: subfamilies and supertribes. - Aust. Bot. 74: 1338-1395 J. Bat. 33: 433-484