Syntenic relationships between cucumber (Cucumis sativus L.) and melon (C. melo L.) chromosomes as revealed by comparative genetic mapping

Dawei Li 0 2 Hugo E Cuevas 0 1 Luming Yang 0 Yuhong Li 0 2 Jordi Garcia-Mas 4 Juan Zalapa 0 3 Jack E Staub Feishi Luan Umesh Reddy Xiaoming He 0 Zhenhui Gong 2 Yiqun Weng 0 3 0 Horticulture Department, University of Wisconsin , Madison, WI 53706 , USA 1 USDA ARS Tropical Agriculture Research Station , Mayaguez, P.R. 00680 , Puerto Rico 2 Horticulture College, Northwest A & F University , Yangling 712100 , China 3 USDA ARS Vegetable Crops Research Unit, Horticulture Department, University of 4 IRTA, Center for Research in Agricultural Genomics CSIC-IRTA- UAB , Campus UAB, Edifici CRAG, 08193 Bellaterra (Barcelona) , Spain Background: Cucumber, Cucumis sativus L. (2n = 2 = 14) and melon, C. melo L. (2n = 2 = 24) are two important vegetable species in the genus Cucumis (family Cucurbitaceae). Both species have an Asian origin that diverged approximately nine million years ago. Cucumber is believed to have evolved from melon through chromosome fusion, but the details of this process are largely unknown. In this study, comparative genetic mapping between cucumber and melon was conducted to examine syntenic relationships of their chromosomes. Results: Using two melon mapping populations, 154 and 127 cucumber SSR markers were added onto previously reported F2- and RIL-based genetic maps, respectively. A consensus melon linkage map was developed through map integration, which contained 401 co-dominant markers in 12 linkage groups including 199 markers derived from the cucumber genome. Syntenic relationships between melon and cucumber chromosomes were inferred based on associations between markers on the consensus melon map and cucumber draft genome scaffolds. It was determined that cucumber Chromosome 7 was syntenic to melon Chromosome I. Cucumber Chromosomes 2 and 6 each contained genomic regions that were syntenic with melon chromosomes III+V+XI and III+VIII+XI, respectively. Likewise, cucumber Chromosomes 1, 3, 4, and 5 each was syntenic with genomic regions of two melon chromosomes previously designated as II+XII, IV+VI, VII+VIII, and IX+X, respectively. However, the marker orders in several syntenic blocks on these consensus linkage maps were not co-linear suggesting that more complicated structural changes beyond simple chromosome fusion events have occurred during the evolution of cucumber. Conclusions: Comparative mapping conducted herein supported the hypothesis that cucumber chromosomes may be the result of chromosome fusion from a 24-chromosome progenitor species. Except for a possible inversion, cucumber Chromosome 7 has largely remained intact in the past nine million years since its divergence from melon. Meanwhile, many structural changes may have occurred during the evolution of the remaining six cucumber chromosomes. Further characterization of the genomic nature of Cucumis species closely related to cucumber and melon might provide a better understanding of the evolutionary history leading to modern cucumber. - Background The genus Cucumis (family Cucurbitaceae) includes two economically important vegetable crop species that are cultivated worldwide: cucumber (C. sativus L., 2n = 2 = 14) and melon (C. melo L., 2n = 2 = 24). The genetic, phylogenetic, and evolutionary relationships of cucumber and melon have been the subject of much research. The genus Cucumis initially contained 32 species that was divided into two subgenera, Melo and Cucumis [1]. While the subgenus Melo is centered in Africa with 30 species including melon (all of which have 2n = 24 chromosomes), the subgenus Cucumis is of Asian origin and includes the cultivated cucumber C. sativus and its wild relative C. hystrix Char. (2n = 2 = 24). Although C. melo is considered the most morphologically diverse species in Cucumis [1,2], two inter-fertile botanical varieties (2n = 2 = 14), the cultivated C. sativus var. sativus L. and the wild C. sativus var. hardwickii (Royle) Alef., comprise the primary gene pool of cucumber. This gene pool has a rather narrow genetic base as evidenced in various genetic diversity studies [3-6]. No interspecific hybrids between melon and cucumber have been reported due to their sexual incompatibility [7]. The genus Cucumis has undergone considerable revision in recent years. For instance, molecular phylogenetic studies indicated that the genera such as Cucumella, Mukia, Dicaelospermum, Myrmecosicyos, and Oreosyce possess genetic affinities with Cucumis species resulting in their inclusion in Cucumis in more recent taxonomic treatments [8-10]. The genus Cucumis in the newest treatment contains 52 species, which are grouped into two subgenera: Humifructus (two species, C. humifructus and C. hirsutus) and Cucumis (consisting of the remaining 50 species) [9,11]. In addition, both melon and cucumber are believed to be of Asian origin, which were derived from a common ancestor approximately nine million years ago [12]. The genome size of melon (12 chromosome pairs) is estimated to be 454 Mb, and cucumber (7 chromosome pairs) has a genome size of 367 Mbp [13]. The evolutionary relationship between melon and cucumber can be investigated through chromosome analysis. In Kirkbrides taxonomic assessment of Cucumis [2], subgenus Cucumis is considered primitive and subgenus Melo was hypothesized to have been derived from it through chromosomal fragmentation [14-16]. In contrast, cytological investigations have also suggested that ancestral species of subgenus Melo gave rise to subgenus Cucumis species via chromosome fusion or non-homologous translocation [17,18]. However, Ramachandran and Seshadri [19] argued that the two subgenera are not closely related given differences in geographical distribution and chromosome number, size, organization, and behavior. More recent molecular-based phylogenetic analyses of Cucumis support the hypothesis that the base chromosome number of x = 7 was achieved by chromosome reduction from x = 12 progenitor species [8,10,12]. Despite their distinct phylogenetic relationships [20,21], the genomes of melon and cucumber seem to be highly conserved. Cross-species similarities based on molecular marker transferability among cucurbit crops are well documented. Neuhausen [20] first reported affinities among cucurbit species by identifying molecular cross-hybridizations (i.e., signals) using RFLP probes. More recently, Katzir et al. [21] and Danin-Poleg et al. [22] defined specific genomic regions using SSR primer products to reveal considerable sequence homologies between cucumber and melon. Danin-Poleg et al. [23] identified nine SSR markers shared between melon and cucumber and proposed that their cucumber Linkage Group B and melon Linkage Groups E and 2 were syntenic. Since 2000, molecular markers (primarily SSRs) developed from melon have been used routinely in cucumber genetic mapping studies or vice versa [24-37]. The high degree of synteny and conservation between the melon and cucumber genomes has also been demonstrated at the DNA sequen (...truncated)