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Gentianaceae: Systematics and Natural History

Posted on: Thursday, 2 December 2004, 03:00 CST

Gentianaceae: Systematics and Natural History.-Lena Struwe and Victor A. Albert (eds.) 2002. Cambridge University Press, Cambridge, CB2 2RU, UK. x + 652 pp. ISBN 0-521-80999-1. Hardback. 95 ($130).

We are witnessing a revolution in plant systematics brought on by the flourishing of molecular pliylogenetics principally based on DNA sequence data. Over the last decade, thousands of molecular phylogenies have been published for all types of organisms including almost all major groups of plants, addressing overall relationships among major groups or detailed relationships in specific lineages (Pagel, 1999). In addition to studies on the evolution of genes, genomes, and the origin of biodiversity, recent advances have led to the assembly of the general "tree of life" and to the compilation of phylogenetic trees into hierarchical systems, i.e., classifications. Such practice is done at or above the level of family, e.g., the work of the Angiosperm Phylogeny Group (APG, 2003). Gentianaceae: Systematics and Natural History combines molecular and morphological data to revise the outdated classification of a family established more than a century ago. Evolutionary trends in morphology, anatomy, palynology, and phytochemistry are reconsidered in the light of molecular phylogeny.

The first chapter, coauthored by the editors, is a concise overview of the Gentianaceae: its taxonomic history, circumscription, diagnostic characters, affinities and distribution. Based on a review of phylogenetic studies at the family level or above, family Gentianaceae of GiIg (1895) is modified to include Anthocleista, Fagraea and Potalia (formerly Loganiaceae), and Saccifolium (formerly recognized as a monotypic family), but excluding subfamily Menyanthoideae, which has been confirmed as a family of Asterales by several recent phylogenetic studies. Gentianaceae so defined upholds an increased morphological heterogeneity and, as the authors indicate, lacks a general characterization, but its monophyly is well supported by DNA data and potentially by some cryptic phytochemical features. The authors attempt to characterize the newly defined Gentianaceae, but the description of several general morphological gestalts seems rather ineffective in this regard, although highlighting some evolutionary problems in the family. It would have been useful, particularly for those who do not know much about the Gentianaceae, if the authors had presented a comparison with closely related families of the order Gentianales. Statistical descriptions of diversity in terms of the number of species and genera are also presented for major clades and partitions of the continents. Although a general description of diversity and its geographic distribution is necessary, the figures can be misleading, particularly concerning the number of genera in a clade or a region, because generic delimitations of some clades are highly controversial.

Chapter 2, coauthored by Struwe et al., is the most significant part of the book, in terms of both length (it covers nearly half of the volume) and scientific importance, presenting a new classification integrating molecular phylogeny with morphology. Since GiIg (1895), the classification of Gentianaceae has been somewhat overlooked, and revision of the classification was "a work waiting to be done." Phylogenetic relationships inferred from two plastid fragments, the trnL(UAA) intron and matK gene, were used as the backbone of the new classification. The molecular phylogenies were produced mainly with previously published data with a few additions of taxa. This chapter primarily provides detailed descriptions of the tribes, subtribes, and genera, with morphological evolution and biogeography discussed in the context of molecular phylogenies. Although providing an adequate guideline for classification, discussion on phylogenetics per se falls short and is sketchy in the book. It would have been better to justify the new classification with a thorough discussion of the phylogenetics of the family. Nevertheless, the inferred phylogenies are congruent with those published earlier (Thiv et al., 1999), and in full agreement with our recent results based on both plastid and nuclear DNA sequences in terms of tribal and subtribal relationships (Yuan et al., 2003). The phylogenetic assumption of the classification, at least at the tribe and subtribe levels, seems solid and well supported.

The tribe Saccifolieae is newly established by Struwe et al. in this chapter to accommodate a basal clade consisting of several small genera that were previously placed elsewhere both inside and outside Gentianaceae. The recognition of this small tribe significantly enlarges the morphological breadth of Gentianaceae, such as saccate leaves and heterostyly, and has great importance in understanding the origin and early differentiation of Gentianaceae.

The tribe Exaceae, although not new, is newly shaped in Chapter 2 to include the Madagascan endemics Tachiadenus and Gentianothamnus. Dr. Klackenberg, author of this tribe, has devoted study to this tribe since his doctoral thesis, a monograph on the genus Exacum. His descriptions of morphological, anatomical, and karyological variations, as well as phylogenetic relationships among genera of the tribe, are by far the most detailed and sophisticated of the tribes presented in the book. His suggestions of a close affinity between the saprophytic genus Cotylanthera and Exacum based on morphology (anthers opening by apical pores and finely perforated endothecial walls), and close relationship between Gentianothammus and Tachiadenus, are all confirmed by our recent molecular studies (Yuan et al., 2003). Meanwhile, he suggested gondwanan tectonic history as the cause of the vicariant distribution pattern of the deep branching clades of Gentianaceae, within the tribe Exaceae, and even the genus Exacum. He further hypothesized that the genus Exacum may have existed over 80 million years before present (Mya). These speculations are, however, not corroborated by molecular dating, because divergence of the order Gentianales is estimated at not beyond the Late Cretaceous (< 90 Mya) and divergence of the family Gentianaceae at around 50 Mya (Wikstrm et al., 2001; Yuan et al., 2003).

Following molecular phylogenetic results (Thiv et al., 1999), the tribe Chironicac is newly defined in this chapter to accommodate Gilg's (1895) subtribes Erythraeinae and Chironiinae. The tribe is further divided into three subtribes that seem to show biogeographic importance. Excepting the delimitation of some genera such as Centaurium the proposed circumscription of tribe and subdivision into subtribes is supported by independent studies (Mansion, 2001). The suggested biogeographic histories of the tribe and the subtribes concur with molecular dating (Wikstrm et al., 2001; Mansion, 2001). Descriptions and discussion of this tribe fall short, but subsequent publications by the authors provide a useful addition (Thiv and Kadereit, 2002; Thiv, 2003).

The classification of the tribe Helieae presented in this chapter, rooted in the thorough studies of the doctoral thesis of Struwe (1999), has greatly clarified the long-lasting taxonomic and nomenclatural confusion regarding the genera of the group. The genera of this tribe used to be placed in three different tribes by GiIg (1895) based mainly on the superficial similarity of pollen morphology. Although the importance of pollen characters to infratribal classification of Helieae was confirmed, molecular phylogenetic results have shown that pollen types, viz. monads, tetrads, and polyads, are superficially homoplasious, and involve substantial difference. For example, tetrad and polyad pollen were the diagnostic character of Gilg's (1895) Helieae, thus genera such as Coutoubea, Deianira, Schultesia, Symphyllophyton, and Xestaea, all producing tetrads, were included in Helieae by GiIg, whereas molecular results revealed them to be members of Chironieae. Enlightened by molecular studies, further palynological observations on these genera confirmed that the tetrads of these genera were in fact significantly different from those of typical Helieae, such as Adenolisianthus, Helia, Tetrapollinia. The circumscription of the tribe Helieae and the genera therein are better balanced between palynological data and other morphological data. The genera in the Helieae of the new classification are small and much divided except genus Macrocarpaea (Grant, 2003), which is not relevant to some other tribes, such as Gentianeae.

The tribe Potalieae, although the name per se and its Gcntianaceae attribution is not new, is newly shaped in this chapter to comprise three subtribes. Molecular data, strongly supporting the Centianaceac affiliation of the subtribes, conflict with morphological data including pollen and seed micromorphology revealed in this book, which deserve further studies. The morphological descriptions and evolutionary considerations seem relevant and detailed. Nevertheless, the biogeographic suggestions are not convincing. For example, it is hard to believe that the current distribution of Potalia elegans in the white-sand of the Guayana Shield is relictual dating from gondwanan continuity between South Ameri\ca, Africa, and Madagascar as the authors suggest (p. 206). It is equally hard to believe that the repeated disjunct pantropical patterns shown in the subtribe Potaliinae and the species and subspecies of the genus Emcosfema were due to 'a common vicariance event' (pp. 219-220). A common vicariant origin of the patterns would suggest unrealistically old ages for the subtribe and the genus (or even the subspecies of Enicostema axillare), and also a dramatic slow down of evolution in the annual or perennial herb genus Emcosfema, or dramatic speed up of evolution in the woody mostly tree subtribe Potaliinae consisting of Anthocliesta, Fagraea, and Potalia. The repeated disjunctive patterns shown in the subtribe are not likely to have a common cause.

The tribe Gentianeae consists of mostly temperate gentians that are better known and studied. The tribe Gentianeae of the new system presented in this chapter is principally congruent with subtribe Gentianinae of Gilg (1895) with the inclusion of Bartonia and Obolaria and exclusion of Ixanthus. Two evolutionary lineages, readily revealed in the tribe Gentianeae by both morphological and molecular studies, are properly accommodated as two subtribes in the new system, Gentianinae and Swertiinae. Except for the extremely heterogeneous genus Swertia, and to a lesser extent Gentianella and Lomatogonium, most recent authors of Gentianaceae tend to agree on the circumscriptions and relationships among the most genera of the tribe. Swertia as currently defined is highly polyphyletic containing at least 14 lineages with regards to other genera of the subtribe as revealed by a recent phylogenetic studies with extensively sampling of species worldwide and multiple molecular markers of both nuclear and plastid genomes (Chassot, 2003). Further taxonomic and nomenclatural adjustments are necessary and anticipated. Although biogcography is still inconclusive, the diversification pattern of the tribe across the entire northern hemisphere does offer a good case to study the extensive floristic links between the Eurasian and American continents.

In general, the new classification has revealed significant taxonomic clarity, and has improved our understanding of the general relationships within the Gentianaceae. It will serve as a good platform for further studies at lower taxonomic levels, yet we still have to decide on a good genus concept that can be applied to all tribes of the family. Apart from the less understood polyphyletic genera (e.g., Centauruim, Gentianella, Lomatogonium, Swertia) that clearly need further taxonomic consideration, the generic concept of the current classification is not fully comparable among some monophyletically defined genera across the tribes. The tropical, particularly the Neotropical genera of the tribe Helieae, are considerably smaller than the temperate genera such as Gentiana of the tribe Gentianeae. In the case of Gentiana, morphological variation among its sections is almost comparable to the variation among the genera of the tribe Helieae.

Mszros et al. (Chapter 3) present a cladistic analysis of 84 mostly morphological characters of 41 representative genera. Although this attempt could have provided an interesting comparison with phylogenies based on molecular data, the result was somewhat disappointing because the morphological tree was hardly resolved. As discussed in detail by the authors, the lack of resolution of the morphological tree may be due to insufficient sampling of taxa and informative characters. The large amount (24.4%!) of missing data may also have contributed to poor resolution. In addition, there is room to further optimize character state interpretation. For example, the arbitrary demarcation of haploid chromosome numbers as a three-state character is obviously unjustified, without considering the cytogenetic background of the haploid numbers. Nevertheless, as stated in the descriptions given in Chapter 2, the higher level taxa (tribes and subtribes) defined according to molecular phylogeny often lack synapomorphies. Phylogenetic inferences from morphological characters are probably compromised by a high frequency of homoplasious evolution. Further exploitation by improving character understanding and expanding taxon and character sampling remains necessary for a better evaluation of morphological evolution.

Nilsson (Chapter 4) presents a thorough review of the palynology of Gentianaceae, which includes a number of new observations illustrated with many impressive SEM photographs of various members of the !family, particularly Neotropical taxa. Palynological characters were the most important criteria for the classification of GiIg (1895), and thus a better understanding of palynology of Gentianaceae is crucial for its taxonomy. Palynology of Gentianaceae is a life-long target of Nilsson's research. As the subject of his doctorate thesis, he made the first comprehensive observation on palynology of Gentianaceae (Nilsson, 1967). The study presented in this book is his last contribution as he regrettably passed away at the time the book was published. This review clearly documents that although palynology cannot provide an overall phylogenetic resolution, it can serve for 'local' diagnosis of relationships among a few genera. The review reevaluates the phylogenetic significance of pollen characters, and discusses in depth the evolution of different pollen types in the light of molecular phylogenies. Undoubtedly it will be an important resource for future studies of Gentianaceae, and a good reference for other families as well. A minor disappointment concerns the way in which the palynological data are presented. In addition to the dedicated Chapter 4, there are substantial parallel descriptions and discussions on palynology following each tribe in Chapter 2, which are somewhat repetitive, and complicated to cite.

Bouman et al. give an excellent survey of seed micromorphology, development, structure, and dispersal. seed coat micromorphology is systematically described and illustrated with nice SEM photographs. High diversity of seed coat micromorphology is revealed, mostly characterizing the tribe, subtribe, or generic circumscriptions of the new classification. The only significant conflict concerns the subtribe Potaliinae. Similar to pollen morphology, seed morphology of the subtribe Potaliinae is shown to resemble that of the Loganiaceae rather than other members of the Gentianaceae. The authors claim that the new classification was followed in their descriptions. However, a minor discrepancy occurs regarding the genus Megacodon. It is widely accepted as a distinct genus, but it is still considered as a part of Gentiana in this chapter (p. 505). Nevertheless, this chapter provides an additional line of data for the taxonomy of Gentianaceae. Its methodology and terminology also provide wonderful references for wide applications to the studies of other plant families.

In their review of phytochemistry and pharmacology in the final chapter, Jensen and Schripsema uncover interesting patterns of distribution of four types of secondary chemicals (secoiridoids, xanthones, the C-glucoxanthone mangiferin, C-glucoflavones) in different tribes. Although the secoiridoids are found in almost all members of Gentianaceae studied, thus representing a plesiomorphic state, xanthones, C-glucoxanthone mangiferin, and C-glucoflavones seem not to occur in basal clades of the family, with the latter two limited to the tribe Gentianeae. The oxidation pattern of the xanthones also deserves phylogenetic consideration, but, as the authors recognize, sampling of species is still insufficient and taxonomically unbalanced among the tribes. So far, less than 10% of the Gentianaceae have been chemically analyzed, mostly members of the temperate Gentianeae. Sampling of more species representing all lineages of the family is needed for a full understanding of biosynthesis, metabolism, biological function, and phylogenetic implications of those characteristic chemicals.

Overall, this book contains a wealth of information about phylogeny, morphology, palynology, phytochemistry, and biogeography of the Gentianaceae. It provides a comprehensive classification of tribes and subtribes, reflecting the progress of taxonomy in the light of molecular phylogenetics. It is also a good example of how research on a family can achieve a better and comprehensive understanding of the taxa under study. Some minor flaws deserve mentioning. For example, in the description of the tribe Saccifolieae, anthers are described as 'without apically elongated connectives' (p. 57), which contradicts the key to tribes and the descriptions of genera therein. The biogeographical considerations of the tribes of Gentianaceae are neither fully consistent, nor convincing enough. Whereas the distribution pattern of the tribe Chironiinae is considered to be the result of postgondwanan dispersals, tribes Exaceae and Helieae are considered to reflect gondwanan breakup. A key to genera is not available for any tribe or subtribes, and there are substantial citations of unpublished data and personal observations. The palynological data are split into two parts, and those palynological descriptions given within each tribe do not integrate well with other descriptions of the tribes and the genera therein. It is true that a systematic treatment of the family was needed, but any urgency in publishing the book should not have led to a poor presentation of some results. Nevertheless, the book is an important source of information for Gentianaceae, and useful for students and researchers of both Gentianaceae and other plants and is complemented by a well-presented and informative web site, Gentian Research Network, led by Dr. Struwe: http:// www.rci.rutgers.edu/~struwe/gentnet/.

Macrocarpaca lenne. A) habit of flowering stem; B) leaves; C) interpetiolar ridge; D) co\rolla viewed from front; E) flower and floral buds; F) cross-section of corolla; G) mature dehisced capsules; H) wood anatomy of cross-section of main trunk. A-H from pickles, photos and specimens of J. R. Grant & Struwe 01-4013. (Drawing by Bobbi Angell; reprinted with permission from Harvard Papers in Botany 8(1):71, 2003.)

REFERENCES

APG. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141:399-436.

Chassot, P. 2003. Molecular phylogenetic, karyological and palynological studies in subtribe Swertiinae (Gentianaceae). PhD Dissertation. Universit de Neuchtel, Neuchtel, Switzerland.

Gilg, E. 1895. Gentianaceae. Pages 50-108 in Die natrlichen Pflanzenfamilien 4(2) (A. Engler and K. Prantl, eds.). Engelmann, Leipzig.

Grant, J. 2003. Systematics, biogcography, and natural history of the Neotropical Moon-gentians (Macrocarpaea: Gentianaceae). PhD Dissertation. Universit de Neuchtel, Neuchtel, Switzerland.

Mansion, G. 2001. Phylogenetic relationships within the subtribe Chironiinae (Gentianaceae), with a particular focus on the evolutionary trends and biogeographic patterns of the genus Centaurium Hill s. 1. PhD Dissertation. Universit de Neuchtel, Neuchtel, Switzerland.

Nilsson, S. 1967. Pollen morphological studies in the GentianaceaeGentianinae. Grana Palynol. 7:46-145.

Pagel, M. 1999. Inferring historical patterns of biological evolution. Nature 401:877-884.

Struwe, L. 1999. Morphological and molecular phylogenetic studies in Neotropical Gentianaceae. PhD Dissertation. Stockholm University, Stockholm.

Thiv, M. 2003. A taxonomic revision of Canscora, Cracosna, Duplipetala, Hoppea, Microrphium, Phyllocydus and Schinziella (Gentianaceae-Canscorinae). Blumea 48:1-46.

Thiv, M., and J. W. Kadcreit. 2002. A morphological cladistic analysis of Gentianaceae-Canscorinae and the evolution of anisomorphic Androeda in the subtribe. Syst. Bot. 27:780-788.

Thiv, M., L. Struwe, V. A. Albert, and J. W. Kadereit. 1999. The phylogenetic relationships of Saccifolium bandcirae Maguire and Pires (Gentianaceae) reconsidered. Harvard Pap. Bot. 4:519-526.

Wikstrm, N., V. Savolainen, and M. W. Chase. 2001. Evolution of the angiosperme: Calibrating the family tree. Proc. R. Soc. Lond. B 268:2211-2220.

Yuan, Y-M., S. Wohlhauser, M. Mller, P. Chassot, G. Mansion, J. Grant, P. Kupfer, and J. Klackenberg. 2003. Monophyly and relationships of the tribe Exaceae (Gentianaceae) inferred from nuclear ribosomal and chloroplast DNA sequences. MoI. Phylogenet. Evol. 28:500-517.

Yong-Ming Yuan and Jason R. Grant, Institut de Botanique, Universit de Neuchtel, Cil-2007, Switzerland

Copyright Society of Systematic Biologists Oct 2004

Source: Systematic Biology

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