| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
2Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK; 3Department of Botany, University of Reading, Reading, RG6 2AS, UK; and 4The New York Botanical Garden, Bronx, New York 10458-5126
Received for publication June 24, 1997. Accepted for publication January 11, 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: atpB • Cneoraceae; Harrisonia; Ptaeroxylaceae; Rutaceae; Simaroubaceae • rbcL
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
155 genera with 1600 species, mostly tropical and subtropical in distribution. The family is usually placed in Rutales (Takhtajan, 1987
, 1997
; Dahlgren, 1989
; Thorne, 1992
) or in Sapindales (Cronquist, 1993
) because they, like other families in the order, are usually woody plants with typically compound, estipulate leaves, seldom more than two ovules per carpel, a nectary disk (sometimes modified into a gynophore), usually no more than twice as many stamens as sepals or petals, and a superior ovary.
Within the order, Rutaceae are grouped with Simaroubaceae, Meliaceae, Cneoraceae, and Ptaeroxylaceae (the latter included in Sapindaceae by Cronquist), primarily because of the absence of resin ducts in the bark, wood rays, and leaf veins and the presence of triterpenoid compounds (Cronquist, 1988
). Rutaceae are distinguished from these families, however, by glandular-punctate leaves, the production of limonoids, and the usual presence in parenchyma and pericarp of secretory cavities containing aromatic ethereal oils. A study of rbcL data from members of the Sapindales complex (Gadek et al., 1996
) supported the inclusion of Rutaceae within Sapindales and the family's distinction from, but close association with, Simaroubaceae, Meliaceae, Cneoraceae, and Ptaeroxylaceae.
In the only systematic treatment of Rutaceae, Engler (1896
, 1931)
recognized seven subfamilies: Rhabdodendroideae, Aurantioideae (=Citroideae), Flindersioideae, Spathelioideae, Dictyolomatoideae, Rutoideae, and Toddalioideae. He defined these subfamilies primarily by characters of the gynoecium, especially fruit type. Although in modern classifications (Takhtajan, 1987
; Dahlgren, 1989
; Thorne, 1992
; Cronquist, 1993
), Rhabdodendroideae have been excluded from Rutaceae, the other six subfamilies (not always with the same circumscriptions) have been retained. Takhtajan (1987)
recognized the six subfamilies. Thorne (1992)
combined Toddalioideae with Rutoideae, making five subfamilies. Dahlgren (1989)
and Cronquist (1993)
did not mention subfamilies, but Cronquist did include Flindersiaceae as a synonym of Rutaceae. Hutchinson (1973)
listed four subfamilies: Rutoideae (including Flindersia), Toddalioideae, Rhabdodendroideae, and Aurantioideae (=Citroideae) but did not mention Spathelia (Spathelioideae) or Dictyoloma (Dictyolomatoideae). He mentioned Chloroxylon (as Chloroxlum), the other genus of Flindersioideae, only in a paragraph of useful products of Meliaceae. A conspectus of the subfamilies and tribes is given in Appendix 1.
In recent classifications, Engler's monogeneric Rhabdodendroideae have been recognized as a family, Rhabdodendraceae, and placed within Rosales (Cronquist, 1988
, 1993
; Dahlgren, 1989
) or Rutales (Takhtajan, 1987
; Thorne, 1992
). Prance (1968
, 1972)
surveyed morphological and anatomical characters and concluded that Rhabdodendron would be best recognized as a separate family within Centrospermae (=Caryophyllales). Analysis of rbcL sequence data by Gadek et al. (1996)
described Rhabdodendron as sister to the caryophyllid clade (including Droseraceae and Nepenthaceae), as was also found by Fay et al. (1997)
. A chemical study of Rhabdodendron macrophyllum (Wolter-Filho et al., 1985
) revealed no metabolites typical of Rutaceae, such as alkaloids and limonoids, compounds characteristic of many members of Sapindales; however, the presence of ellagitannins indicated its placement in Rosales. Rhabdodendron is excluded from this analysis.
Engler defined Citroideae (33 genera and 210 species native to the Old World tropics) by the syncarpous ovary with one or two, sometimes several, ovules per carpel and by the indehiscent, fleshy fruit, often (in Citrinae) with pulp vescicles, but sometimes (in Aegle) with a hard shell. Citroideae have always been included in Rutaceae but divided into several of tribes; Engler (1931)
recognized a single tribe, Tanaka (1932)
eight, and Swingle and Reece (1967)
two.
Engler assigned to Flindersioideae two genera, Flindersia and Chloroxylon, both native to the Old World tropics. They are characterized by a syncarpous ovary with two to several ovules per carpel and by a loculicidal (in Chloroxylon) or septifragal (in Flindersia) capsule with winged seeds. Affinities of these two genera have been uncertain, but because of the similarity of their fruits and seeds to those of Cedrela, early botanists (de Candolle, 1824
, 1878
; Bentham and Hooker, 1862
) included them in Meliaceae. Because of their glandular-punctate leaves, Engler (1877
, 1931)
placed both in Rutaceae, in which Flindersia was recognized by its recent monographer (Hartley, 1969
). Characters of these two genera do not clearly indicate in which family, Meliaceae or Rutaceae, they should be placed, and they also have been recognized as a separate family, Flindersiaceae (Airy-Shaw, 1965
; Takhtajan, 1983
).
Dictyolomatoideae, consisting only of the South American genus, Dictyoloma, are characterized by an apocarpous ovary, several ovules per carpel, a fruit in which each carpel dehisces along its ventral suture with a separating endocarp, and winged seeds. Spathelioideae also consist of a single genus, Spathelia (native to the West Indies and South America), defined by a syncarpous ovary, one or two ovules per carpel, and an indehiscent winged fruit. Although originally described in Rutaceae, Dictyoloma was placed by Planchon (1846)
with Spathelia in Simaroubaceae as tribe Spathelieae, characterized by appendaged staminal filaments. Bentham and Hooker (1862)
agreed with their exclusion from Rutaceae and also placed them in Simaroubaceae. Engler (1874
, 1877
) maintained Dictyoloma in Simaroubaceae, but later (1896, 1931) treated it and Spathelia as members of their own monogeneric subfamilies of Rutaceae.
Rutoideae, largest of the subfamilies (100 genera and 1204 species of temperate and tropical regions worldwide), are defined by generally having two ovules per carpel in a dehiscent fruit (except in Pitavia and some Acronychia). In the characteristic fruit, each carpel dehisces along the ventral suture, leaving no persistent axis, with a separating, cartilaginous endocarp. A fruit with similar dehiscence and endocarp is otherwise found only in Dictyoloma.
Engler defined Toddalioideae (21 genera and 152 species also native to tropical and temperate regions worldwide) by an indehiscent drupe or samara developing from a syncarpous ovary with one or two ovules per carpel. Although always included in the family, Toddalioideae were submerged in Rutoideae by Thorne (1992)
.
Although the ordinal position of Rutaceae seems certain, recent studies have cast some doubt on Engler's subfamilial classification and indicated the inclusion in it of additional genera. On the basis of phytochemical data, Da Silva et al. (1988)
suggested the elimination of Toddalioideae and assignment of the genera to several groups in the Rutoideae. More recently, rbcL data have indicated a relationship between Rutaceae and Harrisonia (Simaroubaceae), Cneoraceae, and Pteroxylaceae (Fernando, Gadek, and Quinn, 1995
; Gadek et al., 1996
).
This study of rbcL and atpB sequence variation in a broader sample of Rutaceae assesses molecular support for the subfamilial circumscriptions and monophyly of Rutaceae and should help to focus future studies of the family, leading to a better understanding of its phylogeny.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Fresh (1–2.0 g) or dried (0.1–0.2 g) leaf material was ground into a fine paste and incubated according to the shortened 2X CTAB procedure of Doyle and Doyle (1987)
. Proteins were removed with SEVAG (24:1, chloroform:isoamyl alcohol), followed by an equilibrium density-dependent centrifugation in CsCl2-ethidium bromide (1.55 g/mL). After dialysis the purified DNAs were stored at -80°C at the RBG(KEW) DNA bank. Better yields of DNA were obtained from fresh leaves than from leaves dried in silica.
Amplification and sequencing
Gene amplification was performed using the polymerase chain reaction (PCR) of Saiki et al. (1987)
with the oligonucleotide primers described by Olmstead et al. (1992)
for the rbcL gene and Hoot, Culham, and Crane (1995)
for the atpB gene. Slight modifications to the reaction conditions (e.g., the annealing temperatures, MgCl2 concentration) were sometimes necessary depending upon the exact nature of the primers and template used. Amplified products were cleaned using Promega Magic mini columns following protocols provided by the manufacturer. Cleaned products were then directly sequenced using the AmpliTaq DNA Polymerase Cycle Sequencing Ready Reaction Kit (Applied Biosystem, Warrington, Cheshire). Unincorporated dye terminators were removed by using Centrisep spin columns (Princeton Separations, Adelphia, New Jersey) or by precipitation with 1:25 3mol/L NaoAc:100% ETOH then 100% ETOH. Samples were run on an Applied Biosystems (Inc.) 373A DNA Sequencer, and data were collected on a Macintosh platform. Raw sequencing data were edited and assembled using Sequencher (Gene Codes Corporation, Ann Arbor, Michigan).
Selection of taxa
Species representing all subfamilies and tribes of Rutaceae and families that have been suggested as possible relatives [Anacardiaceae, Burseraceae, Cneoraceae, Meliaceae, Ptaeroxylaceae, and Simaroubaceae s. str. (Fernando and Quinn, 1995
)] were included in both the rbcL and the atpB data sets. The same genera were included in both analyses except that Flindersia and Harrisonia were not used in the atpB analysis because of a lack of material.
Phylogenetic analysis
Each data set was first analyzed with PAUP version 3.1.1 (Swofford, 1993
) using heuristic search methods. For all data sets, 100 replicates of random taxon entries were performed using TREE BISECTION RECONNECTION (TBR), MULPARS, and STEEPEST DESCENT, with all characters and character states weighted equally and unordered (Fitch parsimony; Fitch, 1971
). All trees from the replicates were then swapped to completion, all shortest trees were saved, and a strict consensus tree was computed. Relative support for clades identified by rbcL and atpB analyses was assessed with bootstrap (BS) methods.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
Overall levels of support
To assess support, we compared the internal support of the separate analyses to that of the combined analysis using total bootstrap indices (Table 1). The combined analysis has higher bootstrap values than found for either of the individual trees.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Outgroup relationships
As stated in the introduction, most systematists have assumed a close association between Rutaceae and other families of Sapindales, and most have found Rutaceae to be most similar to Meliaceae and Simaroubaceae. Rutaceae, Meliaceae, Simaroubaceae, and Burseraceae all have bitegmic and crassinucellate ovules, but only Rutaceae and Meliaceae have a clearly differentiated seed coat (Corner, 1976
). Corner (1976)
noted a fibrous exotegmen in the seeds of Meliaceae but not in the structureless and hence uniform seeds of Simaroubaceae, Burseraceae, and (with limited sampling) Rutaceae and therefore did not consider Rutaceae and Meliaceae to be closely related. Boesewinkel (1980)
, however, found a fibrous exotegmen in some species of Rutaceae, a finding that supports a relationship with Meliaceae. In a recent study of the morphology and anatomy of the gynoecium in Rutaceae and Simaroubaceae, Ramp (1988)
questioned the separation of these two families and suggested that Simaroubaceae represent an unnatural group of which some groups are derived from different subgroups of Rutaceae. Several studies of the distribution within Rutales of alkaloids, coumarins, chromones, and limonoids strongly support a close association among Rutaceae, Cneoraceae, Ptaeroxylaceae, Meliaceae, and Simaroubaceae (see papers in Waterman and Grundon, 1983
). In a recent study of rbcL sequence data from several families of the Sapindales, Gadek et al. (1996)
proposed that members of Simaroubaceae were a sister group of Rutaceae. Our combined analysis of sequence data showed that Simaroubaceae/Meliaceae were strongly supported as the sister group of Rutaceae.
Circumscription of Rutaceae
Our independent and combined analyses indicate that Rutaceae are paraphyletic because Harrisonia (based on rbcL data), Cneorum, and Ptaeroxylon are excluded. Thorne (1992)
suggested removing Harrisonia from Simaroubaceae, in which it had been placed previously (Jussieu, 1825
; Planchon, 1846
; Bentham and Hooker, 1862
; Engler, 1931
), and placing it, with Spathelia, in Spathelioideae. Taylor's (1983)
information on the distribution of secondary metabolites indicated a relationship of these two genera and Cneorum and Ptaeroxylon. Both limonoids and chromones occur in Harrisonia, a rare combination of compounds otherwise known only in Cneorum and Spathelia. Ptaeroxylon lacks limonoids but possesses chromones of the ptaeroxylon group that are otherwise restricted to Harrisonia, Spathelia, and Cneorum. Taylor (1983)
considered this evidence to indicate that Harrisonia and Spathelia occupy a "rather unclear junction area" between Rutaceae, Cneoraceae, and Ptaeroxylaceae. Rather than occupying such a "junction," Harrisonia (as well as Cneorum and Ptaeroxylon) occupies a position within Rutaceae. Comparative morphological and anatomical studies of these genera are needed to assess this broader concept of the family.
Circumscription of the subfamilies within Rutaceae
Citroideae (=Aurantioideae)
In both independent and combined analyses, all genera of Citroideae (except Luvunga) form a strongly supported clade. A survey of the cytological literature (Stace, Armstrong, and James, 1993
) showed that the chromosome numbers for the Citroideae were taxonomically informative, largely constant, and in agreement with the classification of Swingle and Reece (1967)
. Studies of alkaloids (Waterman, 1975
) and flavonoids (Grieve and Scora, 1980
) also strongly support the conclusions of Swingle and Reece. Because Luvunga was not included in any of these studies, its position cannot be assessed. The anomalous pairing in our analyses of Luvunga with Zanthoxylum of Rutoideae is unexplained. With this single exception, the Citroideae appear to be a well-defined, natural group.
Flindersioideae
Our analysis based on rbcL data indicated that this subfamily is not monophyletic; Flindersia appears to be more closely related to Lunasia (Rutoideae), whereas Chloroxylon is sister to Ruta (Rutoideae). As stated in the introduction, Flindersia and Chloroxylon have been placed in Meliaceae (in the tribe Cedreleae) because of similarities in fruits, in Rutaceae because of the presence of schizogenous cavities in the leaves, cotyledons, and perianth or in a separate family because of their overall intermediate nature. Pollen morphology led Erdtman (1986)
to recognize Chloroxylon and Flindersia as rutaceous rather than meliaceous. Wood anatomical studies (Harrar, 1937
) indicated placement of Flindersia intermediate between Rutaceae and Meliaceae. The secondary xylem of Chloroxylon also possesses features of both Meliaceae and Rutaceae (Pennington and Styles, 1975
). Flindersia was retained in Rutaceae by Hartley (1969)
largely on the basis of chemical evidence of alkaloids, coumarins, and flavonoids compiled by Price (1963)
and Ritchie (1964)
. A more recent phytochemical study (Da Silva et al., 1988
) also showed that Flindersia and Chloroxylon typically contain rutaceous coumarins and anthranilic-derived alkaloids, which are absent from Meliaceae. Our molecular data, too, confirm that these two genera are not members of Meliaceae and belong in Rutaceae but indicate that they are not members of a single distinct subfamily. Additional information is needed to confirm the subfamilial relationships. The seemingly unlikely pairing of the arborescent Chloroxylon with the more or less herbaceous Ruta requires closer examination.
Spathelioideae and Dictyolomatoideae
The recognition of these two subfamilies, by any circumscription, is untenable, according to our analysis. There is a consistent strongly supported pairing of Dictyoloma and Spathelia within a moderately supported clade comprising also Cneorum, Ptaeroxylon, and Harrisonia. As discussed above, the phytochemical evidence of a relationship among Spathelia, Harrisonia, Cneorum, and Ptaeroxylon is quite strong, but the phytochemically depauperate nature of Dictyoloma (Da Silva et al., 1988
) makes it impossible to assess its relationships on the basis of chemical data. In the rbcL analysis of Fernando, Gadek, and Quinn (1995)
, Harrisonia was excluded from Simaroubaceae, paired with Cneorum, and placed in a clade with Rutaceae. Although little comparative morphological or anatomical study of this group of taxa has been completed, both molecular and phytochemical data strongly support their association.
Rutoideae and Toddalioideae
Engler's delimitation of Toddalioideae from Rutoideae by the presence in the former of an indehiscent fruit is not supported by most morphological, chemical, and molecular data. Revisionary studies by Hartley (1974
, 1981
, 1982)
indicated that genera of Toddalioideae with syncarpous, drupaceous fruits (e.g., Acronychia, Toddalia, and Phellodendron) are more closely related to genera of Rutoideae with apocarpous or subapocarpous follicular fruits (e.g., Melicope, Zanthoxylum, and Tetradium). Boesewinkel's (1980)
study of ovule and seed-coat development in Rutales found little distinction between the two subfamilies. A survey of chromosome numbers in Rutaceae (Stace, Armstrong, and James, 1993
) showed similarities in base number and cytoevolutionary patterns in tribes Zanthoxyleae and Toddalieae. Biochemical studies (Fish and Waterman, 1973
; Da Silva et al., 1988
) provided strong evidence of phylogenetic links between Rutoideae and Toddalioideae. Our analysis of molecular data provides further evidence that these two subfamilies are untenable and supports Thorne's (1992)
placement of Toddalioideae in Rutoideae.
Conclusions
Our analyses show the following: (1) Simaroubaceae and Meliaceae are the closest relatives of Rutaceae. (2) Citroideae, with the exception of Luvunga, are monophyletic. (3) Flindersioideae belong in Rutaceae, but are not monophyletic; the two genera appear to be related to different genera in the Rutoideae. (4) Dictyolomatoideae and Spathelioideae, each monogeneric, are by default monophyletic, but both are part of a clade that includes Harrisonia, Cneorum, and Ptaeroxylon. We recommend the inclusion of all five genera in a recircumscribed Spathelioideae (oldest named subfamily of Rutaceae). (5) Toddalioideae should be merged with Rutoideae. (6) Rutaceae, as presently circumscribed, are paraphyletic; monophyly is achieved by the inclusion of Harrisonia, Cneorum, and Ptaeroxylon in a recircumscribed Spathelioideae.
The subfamilies of Rutaceae also need to be redefined. Before most of the taxonomic alignments can be proposed, studies using more genera, data from faster evolving DNA sequences, and anatomical, morphological, and biochemical characters are needed to resolve the subfamilial affinities of the problematic genera and the circumscriptions and generic relationships within the tribes. The information contributed here for familial and subfamilial relationships provides a framework for future studies.
Note added in proof: Just prior to receiving page proofs, we discovered upon a critical evaluation of the voucher specimen that the material identified in this paper as Luvunga eleutherandra is instead a species of Zanthoxylum, thus rendering Citroideae monophyletic instead of polyphyletic, as was reported in the Results.
|
|
|
|
|
FOOTNOTES |
|---|
5 Author for correspondence, current address: Auburn University, 101 Life Science Building, Auburn, AL 36849.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Albert, V. A., S. E. Williams, and M. W. Chase. 1992 Carnivorous plants: phylogeny and structural evolution. Science 257: 1491–5.
Bakker, F. T., D. D. Vassiliades, C. M. Morton, and V. Savolainen. 1998 Phylogenetic relationships of Biebersteinia Stephan (Geraniaceae) inferred from rbcL and atpB sequence comparisons. Botanical Journal of the Linnean Society 127: 149–58.
Bentham, G., and J. D. Hooker. 1862 Genera plantarum, vol. 1, part 1. Reeve, Williams&Norgate, London.
Boesewinkel, F. D. 1980 Development of ovule and seed-coat in the Rutales-Geraniales assembly. Academisch Proefschrift, Hugo de Vries Laboratory, University of Amsterdam, Amsterdam, The Netherlands.
Chase, M. W., et al. 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528–580.[CrossRef][ISI]
Corner, E. J. H. 1976 The seeds of dicotyledons. Cambridge University Press, Cambridge.
Cronquist, A. 1988 The evolution and classification of flowering plants, 2d. ed. New York Botanical Gardens, Bronx, NY.
———. 1993 An integrated system of classification of flowering plants. Columbia University Press, New York, N.Y.
Da Silva, M. F. Das Graças Fernandes, O.R. Gottlieb, and F. Ehrendorfer. 1988 Chemosystematics of the Rutaceae: suggestions for a more natural taxonomy and evolutionary interpretation of the family. Plant Systematics and Evolution 161: 97–134.[CrossRef][ISI]
Dahlgren, R. 1989 The last Dahlgrenogram system of classification of the dicotyledons. In K. Tan [ed.], The Davis and Hedge Festschrift: plant taxonomy, phytogeography and related subjects, 249–260. Edinburgh University Press, Edinburgh.
de Candolle, A. 1824 Prodromus systematis naturalis regni vegetabilis, vol. 1. Treuttel & Wiirtz rtz, Paris.
de Candolle, C. 1878 In A. and C. De Candolle. Monographiae Phanerogamarum 1: 419–758.
Doyle, J. J., and J. L. Doyle. 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
Engler, A. 1874 Simaroubaceae. In C. Martius, Flora Brasiliensis. 12(2): 196–247.
———. 1877 Studien uber die Verwandtschaftsverhaltnisse der Rutaceae, Simaroubaceae und Burseraceae. Abhandlungen der Naturforschenden Gesellschaft zu Halle 13(2): 115–158.
———. 1896 Rutaceae. Nat. Pflanzenfam. III. 4: 95–201.
———. 1931 Rutaceae. In A. Engler and K. Prantl [eds.], Die natürlichen Pflanzenfamilien, 2nd ed., vol. 19a, 187–359. Engelmann, Leipzig.
Erdtman, G. 1986 Pollen morphology and plant taxonomy: angiosperms. E. J. Brill, Leiden, The Netherlands.
Fay, M. F., K. M. Cameron, G. T. Prance, and M. W. Chase. 1997 Familial relationships of Rhabdodendron (Rhabdodendraceae): plastid rbcL sequences indicate a caryophyllid placement. Kew Bulletin 52: 923–932[CrossRef]
Fernando, E. S., and C. J. Quinn. 1995 Picramniaceae, a new family, and a recircumscription of Simaroubaceae. Taxon 44: 177–181.[CrossRef][ISI]
———, P. A. Gadek, and C. J. Quinn. 1995 Simaroubaceae, an artificial construct: evidence from rbcL sequence variation. American Journal of Botany 82: 92–103.[CrossRef][ISI]
Fish, F., and P. G. Waterman. 1973 Chemosystematics in the Rutaceae II. The chemosystematics of the Zanthoxylum/Fagara complex. Taxon 22: 177–203.
Fitch, W. M. 1971 Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20: 406–416.[CrossRef][ISI]
Gadek, P. A., E. S. Fernando, C. J. Quinn, S. B. Hoot, T. Terrazas, M. C. Sheahan, and M. W. Chase. 1996 Sapindales: Molecular delimitation and infraordinal groups. American Journal of Botany 83: 802–811.[CrossRef][ISI]
———, C. J. Quinn, J. E. Rodman, K. G. Karol, E. Conti, R. A. Price, and E. S. Fernando. 1992 Affinities of the Australian endemic Akaniaceae: new evidence from rbcL sequences. Australian Systematic Botany 5: 717–724.[CrossRef]
Grieve, C. M., and R. W. Scora. 1980 Flavonoid distribution in the Aurantioideae (Rutaceae). Systematic Botany 5: 39–53.
Gunter, L. E., G. Kochert, and D. E. Giannasi. 1994 Phylogenetic relationships of the Juglandaceae. Plant Systematics and Evolution 192: 11–29.[CrossRef][ISI]
Harrar, E. S. 1937 Notes on the genus Flindersia R. Br. and the systematic anatomy of the important flindersian timbers indigenous to Queensland. Journal of the Elisha Mitchell Scientific Society 53: 282–291.
Hartley, T. G. 1969 A revision of the genus Flindersia (Rutaceae). Journal of the Arnold Arboretum 50: 481–526.[ISI]
———. 1974 A revision of the genus Acronychia (Rutaceae). Journal of the Arnold Arboretum 55: 469–523, 525–567.[ISI]
———. 1981 A revision of the genus Tetradium (Rutaceae). Garden's Bulletin, Singapore 34: 91–131.
———. 1982 A revision of the genus Sarcomelicope (Rutaceae). Australian Journal of Botany 30: 359–372.[CrossRef]
Hoot, S. B., A. Culham, and P. R. Crane. 1995 The utility of atpB gene sequences in resolving phylogenetic relationships: comparison with rbcL and 18S ribosomal DNA sequences in the Lardizabalaceae. Annals of the Missouri Botanical Garden 82: 194–207.[CrossRef][ISI]
Hutchinson, J. 1973 The families of flowering plants, 3rd ed. Clarendon Press, Oxford.
Jussieu, A. 1825 Mémoire sur le groupe des Rutacées, seconde partie. Mémoires du muséum d'histoire naturelle (Paris) 12: 449–542.
Olmstead, R. G., H. J. Michaels, K. M. Scott, and J. D. Palmer. 1992 Monophyly of the Asteridae and identification of their major lineages inferred from DNA sequences of rbcL. Annals of the Missouri Botanical Garden 79: 249–265.
Pennington, T. D., and B. T. Styles. 1975 A generic monograph of the Meliaceae. Blumea 22: 419–540.
Planchon, J. E. 1846 Revue de la famille des Simaroubées. London Journal of Botany 5: 560–584.
Prance, G. T. 1968 The systematic position of Rhabdodendron Gilg & Pilg. Bulletin de Jardin Botanique National de Belgique 38: 127–146.
———. 1972 Rhabdodendraceae. Flora Neotropica, monograph no. 11. Hafner, New York, NY.
Price, J. R. 1963 The distribution of alkaloids in the Rutaceae. In T. Swain [ed.], Chemical plant taxonomy, 429–452. Academic Press, London.
Ramp, E. 1988 "Struktur, Funktion und Systematische Bedeutung des Gynoeciums bei den Rutaceae und Simaroubaceae." Inaugural Dissertation zur Eriangung der philosophischen Doktorwurde vorgelegt der Philosophischen Fakultäet II der Universitaet Zürich. ADAG Administration & Druck AG, Zurich.
Ritchie, E. 1964 Chemistry of Flindersia species. Review of Pure and Applied Chemistry 14: 47–56.
Saiki, R. K., D. H. Gelfand, S. Stoffel, S. J. Scharf, R. Higuichi, G. T. Horn, K. B. Mullis, and H. A. Erlich. 1987 Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491.
Stace, H. M., J. A. Armstrong, and S. H. James. 1993 Cytoevolutionary patterns in Rutaceae. Plant Systematics and Evolution 187: 1–28.[CrossRef][ISI]
Swingle, W. T., and P. C. Reece. 1967 The botany of Citrus and its wild relatives. In The Citrus Industry, vol. 1, History, world distribution, botany, and varieties, 190–430. University of California, Berkeley, CA.
Swofford, D. L. 1993 PAUP: phylogenetic analysis using parsimony, version 3.1.1. Computer program distributed by the Illinois Natural History Survey, Champaign, IL.
Takhtajan, A. 1983 The systematic arrangement of dicotyledonous families. In C. R. Metcalfe and L. Chalk [eds.], Anatomy of the dicotyledons, 2d ed., vol. 2. Clarendon Press, Oxford.
———. 1987 Systema magnoliophytorum. Officina Editoria "NAUKA," Leningrad.
———. 1997 Diversity and classification of flowering plants. Columbia University Press, New York, NY.
Tanaka, T. 1932 Philippine Rutaceae-Aurantioideae (Revisio Aurantiacearum, VII.). Transactions of the Natural History Society of Formosa 22: 418–433.
Taylor, D. A. H. 1983 Biogenesis, distribution, and systematic significance of limonoids in the Meliaceae, Cneoraceae, and allied taxa. In P. G. Waterman and M. F. Grundon [eds.], Chemistry and chemical taxonomy of the Rutales, 353–375. Academic Press, London.
Thorne, R. F. 1992 An updated phylogenetic classification of the flowering plants. Aliso 13: 365–389.
Waterman, P. G. 1975 Alkaloids of the Rutaceae: their distribution and systematic significance. Biochemical Systematics and Ecology 3: 149–180.[CrossRef]
———, and M. G. Grundon [eds.]. 1983 Chemistry and chemical taxonomy of the Rutales. Academic Press, London.
Wolter-Filho, W., A. I. Da Rocha, M. Yoshida, and O. R. Gottlieb. 1985 Ellagic-acid derivatives from Rhabdodendron macrophyllum. Phytochemistry 24: 1991–1994.
This article has been cited by other articles:
|
|
 |
|
  C. F. Gouvea, M. C. Dornelas, and A. P. M. Rodriguez Floral Development in the Tribe Cedreleae (Meliaceae, Sub-family Swietenioideae): Cedrela and Toona Ann. Bot., January 1, 2008; 101(1): 39 - 48. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Yingzhi, C. Yunjiang, T. Nengguo, and D. Xiuxin Phylogenetic Analysis of Mandarin Landraces, Wild Mandarins, and Related Species in China Using Nuclear LEAFY Second Intron and Plastid trnL-trnF Sequence J. Amer. Soc. Hort. Sci., November 1, 2007; 132(6): 796 - 806. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. H. J. Barfuss, R. Samuel, W. Till, and T. F. Stuessy Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions Am. J. Botany, February 1, 2005; 92(2): 337 - 351. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Morton, M. Grant, and S. Blackmore Phylogenetic relationships of the Aurantioideae inferred from chloroplast DNA sequence data Am. J. Botany, October 1, 2003; 90(10): 1463 - 1469. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. N. Muellner, R. Samuel, S. A. Johnson, M. Cheek, T. D. Pennington, and M. W. Chase Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences Am. J. Botany, March 1, 2003; 90(3): 471 - 480. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. M. Cameron, M. W. Chase, W. R. Anderson, and H. G. Hills Molecular systematics of Malpighiaceae: evidence from plastid rbcL and matK sequences Am. J. Botany, October 1, 2001; 88(10): 1847 - 1862. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
