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Phylogenetics of Cucumis (Cucurbitaceae): Cucumber (C. Sativus) Belongs in an Asian/Australian Clade Far From Melon (C. Melo)

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Phylogenetics of Cucumis (Cucurbitaceae): Cucumber (C. Sativus) Belongs in an Asian/Australian Clade Far From Melon (C. Melo)

Susanne S Renner et al. BMC Evol Biol.

Abstract

Background: Melon, Cucumis melo, and cucumber, C. sativus, are among the most widely cultivated crops worldwide. Cucumis, as traditionally conceived, is geographically centered in Africa, with C. sativus and C. hystrix thought to be the only Cucumis species in Asia. This taxonomy forms the basis for all ongoing Cucumis breeding and genomics efforts. We tested relationships among Cucumis and related genera based on DNA sequences from chloroplast gene, intron, and spacer regions (rbcL, matK, rpl20-rps12, trnL, and trnL-F), adding nuclear internal transcribed spacer sequences to resolve relationships within Cucumis.

Results: Analyses of combined chloroplast sequences (4,375 aligned nucleotides) for 123 of the 130 genera of Cucurbitaceae indicate that the genera Cucumella, Dicaelospermum, Mukia, Myrmecosicyos, and Oreosyce are embedded within Cucumis. Phylogenetic trees from nuclear sequences for these taxa are congruent, and the combined data yield a well-supported phylogeny. The nesting of the five genera in Cucumis greatly changes the natural geographic range of the genus, extending it throughout the Malesian region and into Australia. The closest relative of Cucumis is Muellerargia, with one species in Australia and Indonesia, the other in Madagascar. Cucumber and its sister species, C. hystrix, are nested among Australian, Malaysian, and Western Indian species placed in Mukia or Dicaelospermum and in one case not yet formally described. Cucumis melo is sister to this Australian/Asian clade, rather than being close to African species as previously thought. Molecular clocks indicate that the deepest divergences in Cucumis, including the split between C. melo and its Australian/Asian sister clade, go back to the mid-Eocene.

Conclusion: Based on congruent nuclear and chloroplast phylogenies we conclude that Cucumis comprises an old Australian/Asian component that was heretofore unsuspected. Cucumis sativus evolved within this Australian/Asian clade and is phylogenetically far more distant from C. melo than implied by the current morphological classification.

Figures

Figure 1
Figure 1
Maximum likelihood tree for Cucumis based on combined sequences from chloroplast genes, introns, and a spacer (details see Table 1). The tree is rooted on Muellerargia, the closest relative of Cucumis, based on the family phylogeny shown in Fig. 4. Parsimony bootstrap values (> 85%) based on 1000 replicates above branches and ML bootstrap values from 100 replicates below branches.
Figure 2
Figure 2
Parsimony tree for Cucumis based on sequences from the nuclear internal transcribed spacer, rooted on Muellerargia as in Fig. 1. Bootstrap values (> 65%) at branches are based on 1000 replicates. The genera marked with red lines are nested in Cucumis, and their species will need to be transferred to make Cucumis monophyletic. Species with the letters GM (Garcia-Mas) are from [22], while species labeled HS were generated for this study. The GenBank sequence labeled '?Oreosyce africana?' is from misidentified material (see text).
Figure 3
Figure 3
Parsimony tree for Cucumis based on the combined chloroplast and nuclear data and rooted on Muellerargia as in Fig. 1. Parsimony bootstrap values (> 75%) based on 1000 replicates above branches and ML bootstrap values from 100 replicates below branches. Species on pale grey background occur in Africa (C. prophetarum extends into India); the clade marked in grey-green occurs in Australia, the Malaysian region, Indochina, China, and India (Mukia maderaspatana extends into the Yemen and sub-Saharan Africa; see Table 1 for geographic ranges); the natural range of melon (C. melo) is unclear. Information on chromosome numbers is from the Index to Plant Chromosome Numbers database available online at the Missouri Botanical Garden's web site.
Figure 4
Figure 4
Detail of one of highest global likelihood trees for Cucurbitaceae obtained from combined chloroplast sequences (matK, rbcL, the trnL intron and spacer, and the rpl20-rps12 spacer; 4,966 aligned nucleotides; GTR + G), with parsimony bootstrap values based on 100 replicates shown at branches. Modified from 10, which contains the full tree with all 123 genera. Highlighted are the Cucumis clade and the genera of Cucumerinae in the most recent morphological classification (11).

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