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Systematics and Phytogeography |
2Biology Department, Acadia University, 24 University Avenue, Wolfville, Nova Scotia, B0P 1X0, Canada; 3Department of Biological Sciences, University of Maine, Orono, Maine 04469-5751 USA
Received for publication January 15, 2002. Accepted for publication April 18, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Gillenia • hybridization • low-copy-number nuclear genes • Maloideae origin • Rosaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). By the 1920s this pattern of chromosome number in the Rosaceae was established and piqued the interest of plant evolutionary biologists. These early workers initiated a long history of explanations of the assumed polyploidy of the Maloideae and, with others who followed, developed three major hypotheses for the origin of the Maloideae.
The first hypothesis for the origin of Maloideae involved ancestors with x = 7. We refer to this hypothesis as the rosoid hypothesis because x = 7 is restricted to Rosoideae. Nebel (1929)
proposed pentaploidy followed by the loss of one chromosome and halving of the chromosome compliment: ([5x – 1]/2). Darlington and Moffett (1930
). Moffett (1931)
also thought that Maloideae have seven types of chromosomes, four of which duplicated and three of which triplicated. The basis of their alternate version of this hypothesis was the formation of multivalents in Maloideae during meiosis. Nebel's alternative does not specify autopolyploidy or allopolyploidy, but Darlington and Moffett's claim of multivalent formation indicates autopolyploidy.
Sax (1931
, 1932
, 1933)
argued against autopolyploidy because he observed a predominance of univalents, not multivalents, in Maloideae triploids during meiosis. He favored allopolyploidy, which was later well supported by isozyme studies (Chevreau, Lespinasse, and Gallet, 1985
; Weeden and Lamb, 1987
; see below) and specifically what we call the wide-hybridization hypothesis for the origin of the Maloideae. He supposed that maloids were derived from an ancient hybridization between progenitors with x = 8 and x = 9, either from the Spiraeoideae or from Spiraeoideae plus Amygdaloideae. Stebbins (1950)
reasoned, on the basis of fruit morphology, that the Maloideae were likely a cross between amygdaloid (x = 8) and spiraeoid (x = 9) progenitors. Phipps, Robertson, and Rohrer (1991)
supported Stebbins' version of the wide-hybridization hypothesis and inferred that extensive homoplasy in their phylogenetic analysis of Maloideae reproductive and vegetative characters resulted from multiple ancient hybridizations following the origin of the subfamily.
In a series of papers on the comparative morphology of carpels in Rosaceae, Sterling (1966b)
reported that the carpels of Lindleya are fused in a way that is very similar to that of Maloideae and that the carpels of Vauquelinia are "clearly pomoid" (Maloideae being referred to then as Pomoideae). Lindleya and Vauquelinia are traditionally placed in Spiraeoideae. Sterling (1966a
, b)
emphasized a "pomoid-spiraeoid affinity" from his work and that of others extending back to 1879. Gladkova (1972)
agreed with what we call the spiraeoid hypothesis for the origin of Maloideae, having rejected Amygdaloideae as an ancestor because he considered them a "specialized, collateral line of evolution." The phytochemical work of Challice (1973
, 1974
, 1981)
highlighted some similarities between Lindleya and maloids but failed to support unequivocally either the wide-hybridization or spiraeoid hypotheses. He did, however, refute Rosoideae as ancestors of Maloideae because the two groups do not share important chemotaxonomic characteristics.
An important contribution to our understanding of the origin of Maloideae came from Goldblatt's (1976)
reports of high chromosome counts in genera traditionally placed in Spiraeoideae. Goldblatt observed base chromosome numbers of x = 17 in Kageneckia and Lindleya and x = 15 in Vauquelinia. These data, while strengthening the ties between these genera and Maloideae, did not explain the evolution of x = 17. Goldblatt refined the spiraeoid hypothesis by postulating that the 17 chromosomes of Maloideae arose by doubling of an x = 9 spiraeoid ancestor followed by an aneuploid loss of one chromosome. Morgan, Soltis, and Robinson (1994)
, Campbell, Donoghue, and Baldwin (1995)
, and Evans (1999)
all demonstrated that spiraeoids with a high base chromosome number (Kageneckia, Lindleya, and Vauquelinia) are closely allied to Maloideae despite their dry, dehiscent fruits that are superficially unlike the fruits of most Maloideae. In this work we define Maloideae as including these three genera. Morgan, Soltis, and Robertson (1994)
and Evans (1999)
used chloroplast DNA data to demonstrate that Amygdaloideae are not closely related to Maloideae. Evans (1999)
also presented morphological evidence in support of these relationships and showed that a genus with x = 9, Gillenia, is sister to Maloideae.
Whereas hybridization has clearly been important in many Rosaceae lineages (Robertson, Phipps, and Rohrer, 1991
) and is of undoubted importance in plant evolution (Arnold, 1992
), there are no well-supported examples of the origin of large groups via wide hybridization. Assertions that Maloideae arose through hybridization between phylogenetically remote groups rest largely on its distinctive x = 17 status and have not been rigorously tested.
Chloroplast DNA (cpDNA) has been the source of DNA sequence data for the broadest samplings of Rosaceae to date, but cannot be used for a rigorous test of a hypothesis of hybrid ancestry because chloroplasts are maternally inherited in most plants (Corriveau and Coleman, 1988
). Nuclear genes, and especially low-copy-number genes, do preserve the evolutionary history of both maternal and paternal ancestries. We have therefore used low-copy-number nuclear gene, granule-bound starch synthase (GBSSI) or waxy, to investigate the origin of Maloideae. Southern analysis and large sequence divergence are evidence for a duplication of the GBSSI gene occurring prior to the origin of the Rosaceae, giving rise to GBSSI-1 and GBSSI-2 (Evans et al., 2000
). We have obtained four distinct copies of the gene (GBSSI-1A and -1B, GBSSI-2A and -2B: Evans et al., 2000
) in Maloideae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) is 1.8–2.0 kilobases (kb) long and includes 47 base pairs (bp) at the 3' end of the first translated exon, 105 bp from the 5' end of the ninth exon, seven complete exons, and eight complete introns (Fig. 1). In addition to the 112 clones from 18 species in 12 genera previously screened (Evans et al., 2000
), we have added complete sequence from 89 additional clones representing 33 new genera and additional copies not previously obtained for genera included in Evans et al. (2000)
. We have included at least one member from each clade identified in the Morgan, Soltis, and Robinson (1994)
analysis of Rosaceae chloroplast DNA sequences, except the Neviusia-Rhodotypos clade. This sampling gives particular attention to clades hypothesized to be involved in the origin of Maloideae (see http://ajbsupp.botany.org/v89/). Our choice of Frangula and Rhamnus (Rhamnaceae) as outgroups is based upon analyses of chloroplast DNA sequences (Morgan, Soltis, and Robertson, 1994
; Savolainen et al., 2000
), as well as our ability to obtain two GBSSI copies from plants of Frangula.
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. Before sequencing a particular clone we used a restriction enzyme assay to identify each of the four Maloideae loci (Table 1). A clone was identified as GBSSI-1A if EcoRI cut within the insert, but neither XbaI nor VspI cut. A clone was identified as GBSSI-1B if EcoRI and VspI did not cut the insert and XbaI cut the insert at approximately 900 bp. Identification of GBSSI-2A clones was similar to GBSSI-1B except that XbaI cut the insert at approximately 500 bp. A clone was identified as GBSSI-2B if neither EcoRI nor XbaI cut the insert and VspI cut the insert.
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). This was to demonstrate the position of all non-Maloideae GBSSI sequences. To facilitate subsequent analyses, we included only those genera for which we have at least two (non-maloid genera) or three (maloid genera) copies of the GBSSI gene. Parsimony analyses with PAUP* (Swofford, 2001
) were performed with 1000 random step additions of sequences, STEEPEST DESCENT, multiple parsimonious trees (MULPARS), and tree–bisection–reconstruction (TBR) branch swapping. A subsequent analysis to determine branch support on all trees used 1000 bootstrap replicates in PAUP* using simple addition sequence, STEEPEST DESCENT, MULPARS, and TBR branch swapping.
We performed maximum likelihood estimation (ML) to test the relationship between Gillenia and Maloideae in our most parsimonious trees. To make ML tractable, we reduced taxon sample size by excluding Chamaemespilus, Cormus, Eriolobus, Frangula, Lindleya, plus Pyrus and also performed separate analyses of GBSSI-1 and GBSSI-2 sequences. The resulting data sets of 25 taxa were bootstrapped with parsimony, using the same settings as in analysis of the full data set, and with ML, using 100 replicates of as-is addition sequence and nearest neighbor interchange (NNI) branch swapping. The model for sequence evolution was chosen for each data set using an hierarchical likelihood ratio test, as implemented in Modeltest (version 3.04: Posada and Crandall, 1998
). The model for sequence evolution for the GBSSI-1 data set was General Time Reversal (Rodriguez et al., 1990
) and rates not equal among sites (G), with a gamma distribution shape parameter of 0.6411. The model chosen for GBSSI-2 was transition rates not equal to transversion rates (K80; Kimura, 1980
) with a transition/transversion ratio of 2.0590, and rates not equal among sites (G), with a gamma distribution shape parameter of 0.4905.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1200 bp in one direction) clones of Gillenia. Parsimony analysis of 70 total GBSSI clones from 23 genera results in 150 most parsimonious trees (Figs. 3 and 4). The relationships within these trees are identical to those observed in the neighbor-joining tree (Fig. 2) and have slightly higher bootstrap support (Fig. 4). With respect to the relationship of Gillenia to Maloideae GBSSI clades, bootstrap values were 61% for Gillenia plus GBSSI-1B and 56% for Gillenia with GBSSI-2B.
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We confirm Evans et al.'s (2000)
discovery of three structural, molecular synapomorphies that are associated with particular clades. All GBSSI-2 sequences, including the outgroup genus Frangula (Rhamnaceae), have a GT to GC mutation at the beginning of the fourth intron, and GBSSI-1 Maloideae and Gillenia sequences are missing the sixth intron and have a first intron that is approximately 150 bp longer than that of other Rosaceae sequences (Figs. 1 and 4). These GBSSI-1 structural changes give further evidence for the close relationship between Gillenia and Maloideae. Additional support for the close relationship between Gillenia and Maloideae comes from the alignability of their GBSSI introns (http://ajbsupp.botany.org/v89/).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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If Maloideae did evolve through hybridization between distantly related amygdaloid and spiraeoid ancestors, then an amygdaloid sequence would be strongly linked to either the A or B locus in GBSSI-1 and GBSSI-2 maloid clades. However, our data and considerable cpDNA sequence data (Morgan, Soltis, and Robertson, 1994
; Evans, 1999
) do not provide close links between Maloideae and Amygdaloideae. An allopolyploid origin involving distantly related plants would have brought together already divergent orthologs of GBSSI-1 and GBSSI-2. One would therefore expect the ancestors, and extant descendants of the ancestors, of Maloideae to be strongly linked to either the A or B loci in both GBSSI-1 and GBSSI-2 clades of Maloideae. Instead we see a weak association between Maloideae and Gillenia. The weak associations of Gillenia GBSSI-1 and Maloideae GBSSI-1B (bootstrap support of 61%: Fig. 2) and Gillenia GBSSI-2 and Maloideae GBSSI-2B (bootstrap support of 56%; Fig. 2) are consistent with an origin of Maloideae from closely related parents. The unresolved evolutionary relationships between Gillenia and GBSSI Maloideae clades might be thought of as "hard" trichotomies.
We are confident that our findings are not the result of under-sampling of taxa within Rosaceae. We have obtained GBSSI sequences from all extant genera of Amygdaloideae and from at least one taxon from each of the Schulze-Menz (1964)
Spiraeoideae tribes, except Holodisceae. Within tribe Gillenieae, Schulze-Menz (1964)
included Spiraeanthus, a genus of Asia. Sterling (1966a)
observed that the ovules, carpels, and degree of intercarpellary fusion of Gillenia, Spiraeanthus, as well as Kageneckia, Lindleya, and Vauquelinia closely resemble pome-bearing members of Maloideae. Although we were able to obtain DNA from a rather old herbarium specimen of Spiraeanthus, we could not PCR-amplify GBSSI for this genus. We did, however, sequence ndhF, which demonstrated that this genus is far more closely related to Sorbaria than to Maloideae (R. C. Evans, unpublished data).
Nonmolecular evidence for the origin of Maloideae
Nonmolecular support for a Gillenia-origin hypothesis includes association with a fungal pathogen, floral morphology, and fossil flowers. Only genera of Maloideae (including Vauquelinia) and Gillenia have been reported to be associated with the rust fungus Phragmidium (Savile, 1979
). Ovule morphology within the majority of Maloideae, Vauquelinia, and Gillenia is identical and differs from other Rosaceae (Sterling, 1966b
; Evans, 1999
; Evans and Dickinson, 1999
). This morphology includes a pair of basally inserted, anatropous ovules, each of which is associated with a papillate funicular obturator. Fossil flowers of Paleorosa similkameenensis from the middle Eocene show characteristics similar to those found in Gillenia, Vauquelinia, and some Maloideae (Basinger, 1976
; Cevallos-Ferriz, Erwin, and Stockey, 1993
). These characteristics include fruit morphology similar to Spiraeoideae and floral and pollen morphology that is similar to some Maloideae. These similarities led Cevallos-Ferriz, Erwin, and Stockey (1993)
to suggest that Spiraeoideae were involved in the evolution of Maloideae.
The molecular and nonmolecular evidence that clarify the origin of Maloideae also point toward a North American origin for the subfamily, contrary to traditional hypotheses of an Asian origin (Kalkman, 1988
; Phipps, Robertson, and Rohrer, 1991
). Evidence for a North American origin comes from the distribution of extant taxa at the base of Maloideae clades and the collection site of Paleorosa fossils. Gillenia is endemic to southeastern USA, Vauquelinia and Lindleya are native to Mexico and southwestern USA, and Kageneckia, which is found in South America, is the only one of these taxa that occurs outside North America. Paleorosa is known only from the Princeton chert of southern British Columbia.
Polyploid evolution and hybridization
Both autopolyploidy (Darlington and Moffett, 1930
) and allopolyploidy (Sax, 1933
; Stebbins, 1950
; Challice, 1981
) have been postulated or implied in the origin of Maloideae. Evidence from isozyme analyses support an allopolyploid origin. Chevreau, Lespinasse, and Gallet (1985)
demonstrated bigenic disomic inheritance for five pollen enzymes and fixed heterozygosity for several enzymes in commercial apple (2n = 34). For two other enzymes they also documented monogenic control, which they noted could represent loss of gene expression at one homeologous locus for each enzyme. Weeden and Lamb (1987)
confirmed polyploidy in apple from the occurrence of numerous duplicate loci among nine enzyme systems, found no evidence of tetrasomic inheritance, and concluded that apple arose through allopolyploidy or has undergone "significant diploidization if produced by autopolyploidy" (p. 870). Thus hybridization is strongly implicated in the origin and evolution of Maloideae.
Advocates of the wide-hybridization hypothesis of the origin of Maloideae point out that the parental forms would likely have been more alike than their modern descendants (Challice, 1974
). Even so, a major problem with wide hybridizations is that hybridization is "almost always between species that are closely related" (McDade, 1995
, p. 323). The wide-hybridization hypothesis is clearly incompatible with our conclusion that the putative founding hybridization involved closely related ancestral species of Gillenia or of ancestors very closely related to this genus. The hybridization and accompanying polyploidization, which may have occurred multiple times, would have created additional copies of GBSSI-1 and GBSSI-2 that diverged over time to the present 5–7% levels between GBSSI-1A and GBSSI-1B and 7–9% levels between GBSSI-2A and GBSSI-2B (Evans et al., 2000
).
Assuming the ancestor of Gillenia was also x = 9, the originating polyploidization event would have produced an x = 18 offspring in which aneuploid loss of one pair of homologous chromosomes gave rise to x = 17 Maloideae at or about the same time. As with other allopolyploids, this offspring would have been fertile and unable to cross with the parents because of differences in chromosome constitution. Hence it was set to establish what turned out to be a highly successful plant lineage.
Ancient hybridizations, like the one giving rise to Maloideae, are likely to have spawned other major groups. We can infer that hybridization has likely been important throughout the history of angiosperms from estimates that up to 70% of angiosperms have polyploidy in their ancestry (Masterson, 1994
) and from the observation that allopolyploidy is more common than autopolyploidy (Soltis and Soltis, 1993
). Several families—such as Cercidiphyllaceae, Hippocastanaceae, Lauraceae, Magnoliaceae, Myristicaceae, Salicaceae, and Trochodendraceae—are thought to be ancient polyploids because of high base chromosome numbers (Stebbins, 1971
) and higher numbers of isozymes than that characteristic of diploid angiosperms (Soltis and Soltis, 1993
). Unlike these groups whose diploid progenitors are apparently extinct, Maloideae are unusual in that their diploid progenitors, or at least a close relative of them, appear to be extant.
A significant feature of the evolution of Maloideae is the low level of divergence among genera. Alignability of maloid GBSSI introns is straightforward, many maloid genera may be grafted successfully, there are numerous natural intergeneric hybrids (Robertson, Phipps, and Rohrer, 1991
), and sequence divergence is low in four cpDNA genes: matK (C. S. Campbell, unpublished data), ndhF (Evans, 1999
), rbcL (Morgan, Soltis, and Robertson, 1994
), and trnL (C. S. Campbell, unpublished data). This lack of divergence is surprising in a group that extends back to at least the Middle Eocene (Wolfe and Wehr, 1988
). This limited evolutionary divergence could be a result of relatively slow rates of evolution in woody plants or of continued gene flow between the genera or a combination of these two factors.
Despite the close affinity of Gillenia and Maloideae suggested above by molecular and nonmolecular features, the putative derivation of Maloideae from ancestors of Gillenia was likely accompanied by major morphological shifts. Gillenia is herbaceous, and all members of Maloideae are woody. The leaves of Gillenia are compound, but only a minority of Maloideae (Cormus, Osteomeles, and Sorbus) has compound leaves. Because the first branches within Maloideae clade are the non-pome-bearing Kageneckia, Lindleya, and Vauquelinia, the pome was a later adaptation that may have contributed to the success of many maloid species as colonizing plants.
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FOOTNOTES |
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4 Author for reprint requests (rodger.evans{at}acadiau.ca
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Basinger J. F. 1976 Paleorosa similkameenensis, gen. et sp. nov., permineralized flowers (Rosaceae) from the Eocene of British Columbia. Canadian Journal of Botany 54: 2293-2305
Campbell C. S. M. J. Donoghue B. G. Baldwin 1995 Phylogenetic relationships in Maloideae (Rosaceae): evidence from sequences of the internal transcribed spacers of nuclear ribosomal DNA and its congruence with morphology. American Journal of Botany 82: 903-918[CrossRef][ISI]
Cevallos-Ferriz S. R. S. D. M. Erwin R. A. Stockey 1993 Further observations of Paleorosa similkameenensis (Rosaceae) from the middle Eocene Princeton chert of British Columbia, Canada. Review of Paleobotany and Palynology 78: 277-291
Challice J. S. 1973 Phenolic compounds of the subfamily Maloideae: a chemotaxonomic survey. Phytochemistry 12: 1095-1101[CrossRef][ISI]
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Challice J. S. 1981 Chemotaxonomic studies in the Rosaceae and the evolutionary origins of the subfamily Maloideae. Preslia 53: 289-304
Chevreau E. Y. Lespinasse M. Gallet 1985 Inheritance of pollen enzymes and polyploid origin of apple (Malus x domestica Borkh). Theoretical and Applied Genetics 71: 268-277[ISI]
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