| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Systematics |
2Institut für Biologie, Systematische Botanik und Pflanzengeographie, Freie Universität Berlin, Altensteinstrasse 6, D-14195 Berlin, Germany; 3Institut für Systematische Botanik, Ludwig-Maximilians-Universität, Menzinger Strasse 67, D-80638 München, Germany
Received for publication December 7, 2000. Accepted for publication July 24, 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Boraginaceae • Boraginales • Heliotropium • Heliotropiaceae • ITS1 • Ixorhea • molecular systematics • morphology • Schleidenia • taxonomy • Tournefortia
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
. Now, the Boraginaceae appear to be a paraphyletic taxon (Chase et al., 1993
; Böhle and Hilger, 1997
; Ferguson, 1999
) because the Hydrophyllaceae R. Br. ex Edwards appear to be the sister group to a Ehretiaceae Mart. ex Lindl./Heliotropiaceae clade. Apart from the molecular results, some morphological characters, e.g., anatropous ovules (Khaleel, 1985
), support this view. This has lead us to accept Heliotropiaceae as a separate family. Morphological and anatomical investigations of the Boraginaceae s.l. have shown similar trends. The common occurrence of long suspensors (Rosanoff, 1866)
in combination with endosperm haustoria (Svensson, 1925
; Pal, 1963
) led Svensson (1925)
and Di Fulvio (1978)
to remove Heliotropioideae (Schrad.) Arn., Cordioideae (R.Br.) Lindl., and Ehretioideae (Mart. ex Lindl.) Arn. from the Boraginaceae s.l. and to include them in the Heliotropiaceae.
The Heliotropiaceae are small trees, lianas, shrubs, subshrubs, or perennial or annual herbs with pentamerous, tetracyclic flowers and actinomorphic corollas. They are characterized by a terminal style and a highly modified conical stigmatic head with a basal stigma and an infertile apex (conical style-stigma complex; Gürke, 1893
; Khaleel, 1978
). The fruits are one- or two-seeded mericarpids or drupes. The nature of the infrafamilial relationships of Heliotropiaceae are controversial. Linné (1753, 1767)
described three genera: Heliotropium L., Tournefortia L., and the monotypic Messerschmidia L. based on differences in habit and fruit shape. Subsequent authors segregated additional small, often monotypic genera, which were not widely accepted (e.g., DeCandolle, 1845
; Gürke, 1893
; Johnston, 1935
). The increasing confusion within the Heliotropiaceae led Förther (1998)
to complete a badly needed monographic study of Heliotropium and the genera closely associated with it.
Förther (1998)
recognized a total of 
450 species in Heliotropiaceae (as Heliotropioideae [Schrad.] Arn.). Besides Heliotropium and Tournefortia, he accepted Argusia Böhm., Schleidenia Endl., and the monotypic genera Ceballosia Kunkel, Ixorhea Fenzl, as well as Nogalia Verdc. In addition, he proposed the new genus Hilgeria Förther, from the West Indies, into which he transferred three former Heliotropium species due to their prostrate herbaceous habit, subsessile single flowers, and pedicels strongly elongating after pollination. The small segregate genera differ mainly in aberrant fruit morphology and habit, and it is these differences that have caused the controversial discussion of their systematic position.
Narrowly endemic Ixorhea only occurs in the province of Salta in Argentina. It is a resinous shrub with four unusually large (up to 10 mm long), winged mericarpids. The systematic relationships of Ixorhea within the Heliotropiaceae are unknown. It is the only taxon in Heliotropiaceae that has never been associated with either Heliotropium or Tournefortia (Fenzl, 1886
; Spegazzini, 1901
; Hauman, 1922
; Di Fulvio, 1978
). Ceballosia is a shrub of the Macaronesian Islands with two-seeded mericarpids that have striking surface protuberances. Its systematic position was also unresolved prior to this study. Previous authors either included Ceballosia in Tournefortia (Roemer and Schultes, 1819)
, Heliotropium (Kuntze, 1891)
, or remained uncertain about its position (Johnston, 1935
). Hilger (1989)
and Förther (1998)
considered Ceballosia as a possibly relict link between Tournefortia and Heliotropium. Pantropical Schleidenia is distinguished by herbaceous habit, pedicellate, apparently solitary flowers, and drupaceous fruits. While Gürke (1893)
and Johnston (1928)
reduced it to synonymy under Heliotropium, Förther (1998)
reestablished its generic rank. The species of Central Asian Argusia are characterized by perennial herbaceous habit and two-seeded, trichomatose mericarpids with a corky exocarp. Johnston (1935)
redefined the generic name Messerschmidia L. for this taxon and transferred three species of Tournefortia to it, based on their exocarp characters. This name was still used by Riedl (1967)
in his Flora Iranica, but Dandy (1972)
, Heine (1976)
, and Czerepanov (1981)
step by step transferred each Messerschmidia species to Argusia as the appropriate name. Another benefit of this transfer was the elimination the generic name Messerschmidia (also spelled Messersmidia and Messerschmidtia), which led to much confusion (see Johnston [1935
] for a detailed discussion). Verdcourt (1987)
renamed Heliotropium drepanophyllum Baker and created a new genus to accommodate Nogalia drepanophylla (Baker) Verdc. because of the shape of the fruit and the structure of the endocarp. Monotypic Nogalia from Somalia and southwestern Arabia is a weakly succulent herb or subshrub with trichomatose drupaceous fruits.
The species of Heliotropium are nearly cosmopolitan or pantropical. They are herbs, subshrubs, or, very rarely, shrubs and are characterized by dry fruits, which divide into four or two mericarpids. Pantropical Tournefortia, on the other hand, consists of small trees or lianas with drupaceous fruits, which never divide into mericarpids.
The infrageneric classification of Heliotropium into sections has been a controversial subject. DeCandolle (1845)
subdivided Heliotropium into four sections and excluded the genus Heliophytum DC. Gürke (1893)
recognized seven sections and excluded the genus Cochranea Miers. Förther (1998)
split the genus into 19 sections (nine Old World, seven New World, and three cosmopolitan sections), once again including both Heliophytum and Cochranea in Heliotropium.
The taxonomy of Tournefortia is also problematical. DeCandolle (1845)
recognized five sections. Three of these sections are currently referred to other genera: species of Mallota A.DC. and Argusia (Amman) DC. (sic) now constitute the genus Argusia Böhm. Gürke (1893)
placed section Messerschmidia sensu DC. under Heliotropium. The two remaining sections, Pittonia HBK. and Tetrandra DC., were renamed by Johnston (1930)
as the two sections Tournefortia (Eutournefortia I.M.Johnst., nomen illegitimum) and Cyphocyema I.M.Johnst. Currently the division of Johnston (1930)
is accepted (Al-Shebaz, 1991
; Förther, 1998
) but a critical evaluation of this division is still missing.
The main aim of this study was to evaluate the infrafamilial relationships of Heliotropiaceae with special reference to Heliotropium and Tournefortia by sequence analysis of the nuclear ribosomal internal transcribed spacer region (ITS1) and morphological data.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
DNA extraction, amplification, and sequencing
The ITS1 primers were those used by Baldwin (1992)
. The DNA segment was amplified in one step, using the primers P1 (5'-TTC AAC GAG GAA TTC CTA GT-3') and P2 (5'-TAC GTT CTT CAT CGA TGC GA-3').
Genomic DNA was extracted using a modified CTAB (cetyltrimethylammonium bromide) extraction protocol from Doyle and Doyle (1990
; tissue ground in sea sand, 70% [v/v] isopropanol substituted for the RNase step). Approximately 40 mg of leaf tissue were used for each extraction. The DNA was amplified with Taq polymerase chain reaction (PCR) kits (Quiagen, Hilden, North Rhine-Westphalia, Germany). The PCR products were cleaned with QIAquick PCR purification columns (Quiagen, Hilden, North Rhine-Westphalia, Germany), quantified with a 100-base pair (bp) DNA ladder (MBI-Fermentas, Sankt Leon-Rot, Baden-Württemberg, Germany), and cycle-sequenced with a GeneAmp PCRSystem 2400 (Perkin Elmer, Weiterstadt, Hesse, Germany). A SequiThermExcel II sequencing kit (Epicentre Technologies, Madison, Wisconsin, USA) was used with a stop/loading solution for terminating. Sequences were run on a GATC model 1500 (GATC, Konstanz, Baden-Württemberg, Germany). Polyacrylamide gels were prepared using SequaGel-6 (National Diagnostics, Atlanta, Georgia, USA). The biotinylized PCR products were transferred onto a Biodyne A nylon membrane (Pall Filtron, Dreieich, Hesse, Germany) and visualized by a reaction using basic phosphatase.
Phylogenetic analyses
Sequences were edited with the Alignment-Editor Align32 (Hepperle, 1997
) and manually aligned (see http://www.ajbsupp.botany.org/ for the data matrix). Phylogenetic analyses were performed by PAUP* 4.0b1. Parsimony analysis (Swofford, 1998
) was performed using a heuristic search. The starting trees were obtained by random stepwise addition to the taxa with 100 replicates, tree-bisection-reconnection (TBR) branch swapping, saving all parsimonious trees, and MAXTREES set to "autoincrease." All characters were weighted equally, and character state transitions were treated as unordered. Gaps were treated as missing data, because of the large deletions. We added an additional set of characters to the data matrix to signify the presence or absence of seven characteristic informative deletions (see http://www.ajbsupp.botany.org/). These additional characters were also unweighted. Bootstrap resampling (Felsenstein, 1985
) was performed with 1000 replicates and a heuristic search. The starting trees were obtained by random addition, with 100 random addition replicates, the TBR branch swapping option and the MULTREE option in effect. MAXTREES was set to 100 for each bootstrap replicate. Gaps were treated as missing data.
Neighbor-joining analyses (Saitou and Nei, 1987
) were performed using a heuristic search run in PAUP. Sequence divergence values were calculated by Kimura's two-parameter method (Kimura, 1980
) with the settings ADDSEQ = random, NREPS = 100, and TBR branch swapping. Bootstrap analysis with neighbor-joining search (Kimura's two-parameter method) was performed with 1000 replicates.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Gürke, 1893
; Johnston, 1928, 1930, 1935
; Förther, 1998
). Tournefortia species (Figs. 1 and 2) occur in two distinct clades. Tournefortia section Cyphocyema appears monophyletic and distinct, while the relationships and phylogeny of Tournefortia section Tournefortia remain unresolved. The ITS1 data suggest that Tournefortia, as traditionally defined by (convergent) traits such as drupaceous fruits and ligneous habit, is polyphyletic. Tournefortia section Cyphocyema is the monophyletic sistergroup of all other taxa under investigation. The species of Tournefortia section Tournefortia are all nested (but not together) in the well-supported New World Heliotropium s.s. clade (excluding section Orthostachys).
The phylogeny of Heliotropium (Fig. 1) inferred from molecular data does not contradict other molecular analyses of this taxon (Böhle and Hilger, 1997
). Heliotropium is paraphyletic, identified as such on the basis of plesiomorphic traits like free mericarpids. Four well-supported clades can be distinguished by molecular analyses. Pantropical Heliotropium section Orthostachys, including Schleidenia, is the sister group of all other Heliotropium s.s. species. This grouping is supported by flower and fruit morphological traits (see below). The second highly supported clade includes the Heliotropium s.s. species of section Heliothamnus, a well-characterized group of Heliotropium s.s. from the South American Andes. The third strongly supported clade comprises the Heliotropium s.s. species of the Old World. The fourth clade includes the unresolved New World clade of Heliotropium s.s. plus Ceballosia and Tournefortia section Tournefortia. Heliotropium s.s. species of the New World are much more closely related to Tournefortia section Tournefortia than to Heliotropium section Orthostachys. Our molecular results cannot resolve the exact position of the morphologically aberrant taxon Ixorhea (Figs. 1 and 2). The strict consensus tree indicates Ixorhea as one of the basal clades between Tournefortia section Cyphocyema and the clade of Heliotropium, Schleidenia, Ceballosia, and Tournefortia section Tournefortia. On the other hand, the neighbor-joining tree demonstrates an affinity of this taxon to the clade of the Heliotropium s.s. species of the New and Old World, Tournefortia section Tournefortia, and Ceballosia and a large genetic distance to Tournefortia section Cyphocyema and Heliotropium section Orthostachys including Schleidenia.
Tournefortia section Cyphocyema
Our results indicate that Tournefortia section Cyphocyema is a monophyletic group and has no close relationships to Tournefortia section Tournefortia. DeCandolle (1845)
, Gürke (1893)
, and Johnston (1930)
united all the woody Heliotropiaceae (mostly climbers or small trees) with drupaceous fruits and four or two endocarpids in Tournefortia. Johnston (1930)
renamed two very distinct sections Cyphocyema and Tournefortia in Tournefortia. He emphasized his doubts with regards to the real relationship between these sections (Johnston, 1930
). "Drupaceous fruits" and "woody habit" are convergent characters and are not appropriate for defining a monophyletic taxon (Fig. 3). The tropical American section Cyphocyema is characterized by the following traits (Fig. 3): (1) apex of the anthers is always hairy; (2) anthers connate; (3) fruits drupaceous, distinctly lobed, and never dividing into mericarpids; (4) four one-seeded endocarpids, each strongly curved with curved embryos (endocarpid type I in Fig. 4d) (Miers, 1868
; Johnston, 1930
); (5) corolla lobes elongate, very narrow with involute margins (Fig. 4a; Miers, 1868
; Johnston, 1930
); (6) habit climbing or subscandent (Miers, 1868
; Johnston, 1930
); and (7) tetrahedral crystals in the wood of some species (Heubl, Gaviria, and Wanner, 1990
). The genus Tournefortia in its current circumscription is polyphyletic. A comparison between the morphological traits of Tournefortia section Cyphocyema with section Tournefortia (Fig. 3) shows that there are, except for drupaceous fruit and woody habit, no shared characters between these Tournefortia sections. The curved embryo is a plesiomorphic trait also found in Ehretiaceae (Gottschling and Hilger, 2001)
. The hairy apex of the connate anthers occurs within Heliotropium section Orthostachys and Heliotropium s.s. section Heliothamnus, and it also seems to be a plesiomorphic trait within the Heliotropiaceae. All these morphological features strongly support a basal position of Tournefortia section Cyphocyema within Heliotropiaceae.
|
|
); and (3) they are resinous shrubs.
For Ixorhea, the molecular results currently available indicate two possibilities for its phylogenetic relationships in Heliotropiaceae. On the one hand, Ixorhea might be a sister group of the large clade of Heliotropium (including Heliotropium section Orthostachys and Schleidenia) and Tournefortia section Tournefortia (strict consensus tree, 57% BS). On the other hand, Ixorhea might be closely related to the clade of the Heliotropium species of the New and Old World, Tournefortia section Tournefortia, and Ceballosia (neighbor-joining tree). Morphological traits (Fig. 3) do not contradict these placements, and both possibilities are conceivable and in agreement with the results of Di Fulvio (1978)
. The morphology of this taxon is so abberant that future investigations will have to clarify its precise relationships within the Heliotropiaceae.
Heliotropium section Orthostachys and Schleidenia
The monophyletic group Heliotropium section Orthostachys including Schleidenia is well supported based on molecular results. Johnston (1928)
treated Schleidenia as subsection Axillaria of section Orthostachys, the largest and probably the most difficult group of Heliotropium, and the molecular data confirm this placement. Heliotropium section Orthostachys including Schleidenia is defined by the following four traits: (1) apex of the anthers is always hairy; (2) anthers mostly connate (compare Fig. 4b with 4c); (3) four one-seeded endocarpids with characteristic surface sculpturing (described below), with curved embryos (endocarpid type II in Fig. 4e, f); and (4) Kranz chlorenchyma organization in leaves of some species (Frohlich, 1978
). The four mericarpids of Orthostachys share a characteristic surface sculpturing, described by different authors as "Male" (which means "markings" in German, Förther, 1998
) or "pits" (Fig. 4e; Johnston, 1928
; Frohlich, 1978
). Schleidenia shares a similar structure, which is not immediately visible because of the more or less fleshy mesocarp (Fig. 4f). Both taxa are characterized by the occurrence of Kranz chlorenchyma organization in leaves of some species. These autapomorphic morphological-anatomical traits and the molecular results strongly support an isolated position. Plesiomorphic morphological traits like the connate anthers with hairy apices and the curved embryo do not occur in the large clade of New and Old World Heliotropium s.s. species, Tournefortia section Tournefortia, and Ceballosia (for an exception see under Heliotropium s.s. section Heliothamnus below).
The molecular results confirm that Schleidenia and Heliotropium section Orthostachys are closely related, which has already been postulated by Johnston (1928)
and Förther (1998)
, on the basis of morphological traits. Section Orthostachys seems to be paraphyletic, with Schleidenia forming a weakly supported (58% BS) clade within Orthostachys. Further investigations are necessary to demonstrate their precise relationships. Nevertheless, both taxa are characterized by separate fruit characters and are provisionally treated as sister groups in Fig. 3. Drupaceous fruits, pedicellate single flowers, and exclusively herbaceous habit identify Schleidenia. Heliotropium section Orthostachys, on the other hand, is characterized by four one-seeded mericarpids, many-flowered inflorescences and shrubby or herbaceous habit.
Heliotropium s.s. section Heliothamnus
The New World clade of Heliotropium s.s., Tournefortia section Tournefortia, and Ceballosia excludes a well-supported clade (99% BS) with Andean species of Heliotropium s.s. section Heliothamnus (H. mandonii, H. arborescens). This latter group is morphologically characterized by the following four traits (Fig. 3): (1) apex of the anthers is always hairy; (2) anthers mostly connate (compare Fig. 4b with 4c); (3) four one-seeded endocarpids, embryo straight (Johnston, 1930
; Miers, 1868
); and (4) they are shrubs.
The species of section Heliothamnus have connate anthers with hairy apex and four endocarpids like those of Heliotropium section Orthostachys and Tournefortia section Cyphocyema. Possibly this plesiomorphic trait indicates a basal position within the large clade of Heliotropium s.s., Tournefortia section Tournefortia, and Ceballosia. Further investigations are necessary to substantiate this hypothesis.
Heliotropium s.s. species of the New World, Ceballosia, and Tournefortia section Tournefortia
This large clade, including New and Old World Heliotropium s.s. species, Ceballosia, and Tournefortia section Tournefortia is less well supported (72% BS) than the other clades and falls into three subclades. The subclade of the New World Heliotropium s.s. species including Tournefortia section Tournefortia and Ceballosia is still unresolved (51% BS) but indicates a close relationship between these taxa. It is, however, characterized by the following three morphological traits that suggest it may be a likely monophylum (Fig. 3): (1) embryos straight (Johnston, 1930
; Miers, 1868
); (2) endocarpids are two-seeded in many species (Johnston, 1930
; Förther, 1998
); and (3) empty chambers (cavities) border on the locules of some species (Johnston, 1930
; Förther, 1998
).
Autapomorphic morphological traits like straight embryos, occurrence of two-seeded endocarpids, and empty chambers support the molecular results. To clarify the exact relationships between these taxa further molecular analyses with more highly resolving markers are necessary. At this stage of investigation, it is not possible to assume any sister group relationships.
On the other hand, morphological traits separate Tournefortia section Tournefortia from section Cyphocyema and confirm the assumption of Johnston (1930)
that the Tournefortia sections are not closely related. The interesting fact that the woody species of Tournefortia section Tournefortia seem to be derived from herbaceous or shrubby Heliotropium s.s. species of the New World has not been predicted. Investigations on wood anatomy (Record and Hess, 1941
) of some Tournefortia species of section Tournefortia show decidedly heterogeneous rays, with most of the cells upright or square. Predominance of upright ray cells indicates secondary woodiness, which in turn indicates herbaceous ancestry, e.g., within the Asteraceae (Carlquist, 1992
).
Heliotropium s.s. species of the Old World
The molecular results demonstrate strong support for a monophyly of the Old World Heliotropium s.s. species, but they have no clear morphological characters separating them from their sister clade (Heliotropium s.s. of the New World, Ceballosia, and Tournefortia section Tournefortia) (Figs. 2 and 3). On the other hand, the alignment of ITS1 shows a single characteristic long deletion between positions 61 and 111, which separates and defines the Heliotropium s.s. species of the Old World.
The large deletion can be regarded as an autapomorphic character of that group based on a single deletion event. Monophyly indicates that this clade of Heliotropium s.s. species seems to go back to a single colonization event from the New World. Other Heliotropium s.s. species, e.g., cosmopolitan H. curassavicum, colonized the Old World later and was perhaps introduced by Man, but the ancestors of this species will be found in the New World.
Taxonomical consequences
Heliotropium and Tournefortia are not monophyletic on the basis of molecular and morphological data. Classification should reflect phylogeny, and nomenclatural changes are therefore necessary. Tournefortia section Cyphocyema constitutes a separate lineage based on both molecular results and complex morphological traits. The only generic name available for this group is Myriopus Small (Small, 1933
).
A clade including Heliotropium section Orthostachys and Schleidenia is also well supported and should be removed from Heliotropium s.s. The species of this clade can be accommodated in a more broadly defined genus Schleidenia Endl. The taxonomic recombination for the investigated taxa will be made next.
Currently, we advocate a conservative approach for Heliotropium s.s., Ceballosia, and Tournefortia section Tournefortia. The exact relationships are still unclear and a reduction of all taxa under one genus name would be premature. The exact position of Ixorhea within the Heliotropiaceae is still unresolved. In summary we conclude that the superficial morphological resemblance of the genera Schleidenia and Heliotropium s.s. on the one hand and Myriopus and Tournefortia on the other has consistently confused previous authors and has obscured the phylogenetic relationships within the Heliotropiaceae. We expect that similar patterns will emerge once other major taxa of Boraginales are studied in detail.
|
FOOTNOTES |
|---|
4 Authors for reprint requests (diane{at}zedat.fu-berlin.de
, foerther{at}botanik.biologie.uni-muenchen.de
, and hahilger{at}zedat.fu-berlin.de
).
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Baldwin B. G. 1992 Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Molecular Phylogeny and Evolution 1: 3-16
Böhle U.-R. H. H. Hilger 1997 Chloroplast DNA systematics of "Boraginaceae" and related families: a goodbye to the old familiar concept of 5 subfamilies. Scripta Botanica Belgica 15: 30
Carlquist S. 1992 Wood anatomy of sympetalous dicotyledon families: a summary, with comments on systematical relationships and evolution of the woody habit. Annals of the Missouri Botanical Garden 79: 303-332[CrossRef][ISI]
Chase M. W. et al 1993 Phylogenetics of seed plants: an analysis of nucleotid sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528-580[CrossRef][ISI]
Czerepanov S. K. 1981 Boraginaceae Juss. Plantae vasculares URSS, 111–119. Nauka, Leningrad, USSR
Dandy J. E. 1972 Note on Argusia Boehmer (Boraginaceae). Journal of the Linnean Society, Botany 65: 256
DeCandolle A. P. 1845 CXXXIX. Borragineae. In Prodomus systematis naturalis regni vegetabilis, vol. 9, 466–559. Fortin and Masson, Paris, France
Di Fulvio T. E. 1978 Sobre la vasculatura floral, embriología y chromosomas de Ixorhea tschudiana (Heliotropiaceae). Kurtziana 11: 75-105
Doyle J. J. J. L. Doyle 1990 Isolation of plant DNA from fresh tissue. Focus 12: 13-15
Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791[CrossRef][ISI]
Fenzl E. 1886 Vier neue Pflanzenarten Süd-Amerikas. Verhandlungen der kaiserlich-königlichen zoologisch-botanischen Gesellschaft in Wien 36: 287-294
Ferguson D. M. 1999 Phylogenetic analysis and relationship in Hydrophyllaceae based on ndhF sequence data. Systematic Botany 23: 253-268
Förther H. 1998 Die infragenerische Gliederung der Gattung Heliotropium L. und ihre Stellung innerhalb der subfam. Heliotropioideae (Schrad.) Arn. (Boraginaceae). Sendtnera 5: 35-241
Frohlich M. W. 1978 Systematics of Heliotropium section Orthostachys in Mexico. Ph.D. dissertation, Harvard University, Cambridge, Massachusetts, USA
Gottschling M. H. H. Hilger 2001 Phylogenetic analysis and character evolution of Ehretia and Bourreria (Ehretiaceae, Boraginales) and their allies based on ITS1 sequences. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 123: 249-268
Gürke M. 1893 Boraginaceae. In A. Engler and K. Prantl [eds.], Die natürlichen Pflanzenfamilien, vol. 4, 59–96. W. Engelmann, Leipzig, Germany
Hauman L. 1922 Nótula sobre Oxyosmyles viscosissima Speg. Physis 5: 306-307
Heine H. 1976 Boraginaceae. In A. Aubréville and J.-F. Leroy [eds.], Flora de la Nouvelle Caledonie et dépendances, vol. 7, 95–118. Muséum National d'Histoire Naturelle, Paris, France
Hepperle D. 1997 Alignment editor align 3.5a. Heidelberg, Germany
Heubl G. R. J. C. Gaviria G. Wanner 1990 A contribution to the taxonomy and evolution of Cordia (Boraginaceae) and allied genera: chromosome numbers, pollen morphology and crystal pattern in wood. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 112: 129-165
Hilger H. H. 1989 Flower and fruit development in the Macaronesian endemic Ceballosia fruticosa (syn. Messerschmidia fruticosa, Boraginaceae, Heliotropioideae). Plant Systematics and Evolution 166: 119-129[CrossRef][ISI]
Johnston I. M. 1928 Studies in the Boraginaceae. VII. 1. The South American species of Heliotropium. Contributions from the Gray Herbarium of Harvard University 81: 3-83
Johnston I. M. 1930 Studies in the Boraginaceae. VIII. I. 3. Treatment of Tournefortia. Contributions from the Gray Herbarium of Harvard University 92: 66-89
Johnston I. M. 1935 Studies in the Boraginaceae. XI. 1. The species of Tournefortia and Messerschmidia in the Old World. Journal of the Arnold Arboretum 16: 145-168
Khaleel T. F. 1978 Embryology of Heliotropium scabrum and H. strigosum (Boraginaceae). Plant Systematics and Evolution 129: 45-62[CrossRef][ISI]
Khaleel T. F. 1985 A review of endosperm and the taxonomic position of Boraginaceae. Journal of Plant Science Research 1: 117-133
Kimura M. 1980 A simple method for estimating evolutionary rate of the base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120[CrossRef][ISI][Medline]
Kuntze K. E. O. 1891 Revisio genera plantarum, part 2. Felix, Leipzig, Germany
Linné C. v. 1753 Species plantarum. Stockholm. Facsimile reprint (1957) by Quaritch, London, UK
Linné C. v. 1767 Mantissa plantarum, altera. Stockholm. Facsimile reprint (1961) by Wheldon and Wesley, and Hafner Publishing, New York, New York, USA
Miers J. 1868 XI. Observations on some of the Heliotropieae. Annals and Magazine of Natural History 2: 121-133
Pal P. 1963 Comparative studies in four species of Heliotropium L. Proceedings of the National Institute of Science of India 29: 1-40
Record J. S. R. W. Hess 1941 American woods of the family Boraginaceae. Tropical Woods 76: 19-33
Riedl H. 1967 Boraginaceae. In H. K. Rechinger [ed.], Flora Iranica, Lfg. 48, 1–281. Akademische Druck- und Verlagsgesellschaft, Graz, Austria
Roemer J. J. J. A. Schultes 1819 Systema vegetabilium, vol. 4. Cotta, Stuttgart, Germany
Rosanoff S. 1866 Morphologisch-embryologische Studien. Jahrbücher für wissenschaftliche Botanik 5: 72-81
Saitou N. M. Nei 1987 The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425[Abstract]
Small J. K. 1933 Manual of the southeastern flora. University of North Carolina Press, New York, New York, USA
Spegazzini C. L. 1901 Plantae novae nonullae americae australis. Comunicaciones de Museo Nacional Buenos Aires 1: 312-323
Svensson H. G. 1925 Zur Embryologie der Hydrophyllaceen, Borraginaceen und Heliotropiaceen mit besonderer Rücksicht auf die Endospermbildung, 1–176. Uppsala Universitets Arsskrift, Uppsala, Sweden
Swofford D. L. 1998 PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, Massachusetts, USA
Verdcourt B. 1987 A new genus Nogalia (Boraginaceae-Heliotropioideae) from Somaliland and southern Arabia. Kew Bulletin 43: 431-435[CrossRef]
This article has been cited by other articles:
|
|
 |
|
  F. SELVI, A. COPPI, and M. BIGAZZI Karyotype Variation, Evolution and Phylogeny in Borago (Boraginaceae), with Emphasis on Subgenus Buglossites in the Corso-Sardinian System Ann. Bot., October 1, 2006; 98(4): 857 - 868. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. H. HILGER, F. SELVI, A. PAPINI, and M. BIGAZZI Molecular Systematics of Boraginaceae Tribe Boragineae Based on ITS1 and trnL Sequences, with Special Reference to Anchusa s.l. Ann. Bot., August 1, 2004; 94(2): 201 - 212. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Gottschling and J. Plotner Secondary structure models of the nuclear internal transcribed spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoflagellates Nucleic Acids Res., January 13, 2004; 32(1): 307 - 315. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
