Multiple domestications of Asian rice.

The origin of domesticated Asian rice (Oryza sativa L.) has been controversial for more than half a century. The debates have focused on two leading hypotheses: a single domestication event in China or multiple domestication events in geographically separate areas. These two hypotheses differ in their predicted history of genes/alleles selected during domestication. Here we amassed a dataset of 1,578 resequenced genomes, including an expanded sample of wild rice from throughout its geographic range. We identified 993 selected genes that generated phylogenetic trees on which japonica and indica formed a monophyletic group, suggesting that the domestication alleles of these genes originated only once in either japonica or indica. Importantly, the domestication alleles of most selected genes (~80%) stemmed from wild rice in China, but the domestication alleles of a substantial minority of selected genes (~20%) originated from wild rice in South and Southeast Asia, demonstrating separate domestication events of Asian rice.

Parallel Speciation of Wild Rice Associated with Habitat Shifts.

The occurrence of parallel speciation strongly implies the action of natural selection. However, it is unclear how general a phenomena parallel speciation is since it was only shown in a small number of animal species. In particular, the adaptive process and mechanisms underlying the process of parallel speciation remain elusive. Here, we used an integrative approach incorporating population genomics, common garden, and crossing experiments to investigate parallel speciation of the wild rice species Oryza nivara from O. rufipogon. We demonstrated that O. nivara originated multiple times from different O. rufipogon populations and revealed that different O. nivara populations have evolved similar phenotypes under divergent selection, a reflection of recurrent local adaptation of ancient O. rufipogon populations to dry habitats. Almost completed premating isolation was detected between O. nivara and O. rufipogon in the absence of any postmating barriers between and within these species. These results suggest that flowering time is a "magic" trait that contributes to both local adaptation and reproductive isolation in the origin of wild rice species. Our study thus demonstrates a convincing case of parallel ecological speciation as a consequence of adaptation to new environments.

Multiple origins of BBCC allopolyploid species in the rice genus (Oryza).

In the rice genus (Oryza), about one half of the species are allopolyploids. These species are not only important resources for rice breeding but also provide a unique opportunity for studying evolution of polyploid species. In the present study, we sequenced four biparentally inherited nuclear loci and three maternally inherited chloroplast fragments from all diploid and tetraploid species with the B- and C-genome types in this genus. We detected at least three independent origins of three BC-genome tetraploid species. Specifically, the diploid O. punctata (B-genome) and O. officinalis (C-genome) were the parental progenitors of O. minuta and O. malampuzhaensis with O. punctata being the maternal donors, whereas the diploid O. punctata and O. eichingeri (C-genome) were the progenitors of tetraploid O. punctata with O. punctata being the paternal donor. Our relaxed clock analyses suggest that all the BBCC species originated within the last one million years, which is coincident with the severe climate oscillations occurred during the last ice age, implying the potential impact of climate change on their formations and dispersals. In addition, our results support previous taxonomic arguments that the tetraploid O. punctata might be better treated as a separate species (O. schweinfurthiana).

Multilocus species tree analyses resolve the ancient radiation of the subtribe Zizaniinae (Poaceae).

The phylogeny of the subtribe Zizaniinae of rice tribe (Oryzeae) has not been well resolved, particularly for the monotypic Hygroryza whose systematic position was inconsistent in previous studies. Here, we used the concatenation approach and coalescent-based species tree methods to reconstruct the phylogeny of Zizaniinae based on sequences of 14 nuclear single-copy loci and concatenated chloroplast fragments. Despite the low resolution of the tree from concatenated data and substantial topological incongruence of individual gene trees, the species trees inferred from three coalescent-based methods were fully concordant and highly supported. Importantly, the genus Hygroryza was consistently recovered with strong support by all coalescent-based methods. Further various phylogenetic analyses indicated that incomplete lineage sorting was the most likely process that generated pervasive discordance among individual gene trees, although hybridization and introgression cannot be excluded completely. Our species tree inferences based on multilocus data successfully resolved the phylogenetic relationships of the Zizaniinae lineages and confirmed that ancient rapid radiation has taken place in the diversification history of Zizaniinae. This study demonstrates that coalescent-based species tree approaches outperformed the concatenation method and could effectively decipher ancient rapid radiations as long as well resolved individual gene trees were sufficiently sampled.

Multiple species of wild tree peonies gave rise to the 'king of flowers', Paeonia suffruticosa Andrews.

The origin of cultivated tree peonies, known as the 'king of flowers' in China for more than 1000 years, has attracted considerable interest, but remained unsolved. Here, we conducted phylogenetic analyses of explicitly sampled traditional cultivars of tree peonies and all wild species from the shrubby section Moutan of the genus Paeonia based on sequences of 14 fast-evolved chloroplast regions and 25 presumably single-copy nuclear markers identified from RNA-seq data. The phylogeny of the wild species inferred from the nuclear markers was fully resolved and largely congruent with morphology and classification. The incongruence between the nuclear and chloroplast trees suggested that there had been gene flow between the wild species. The comparison of nuclear and chloroplast phylogenies including cultivars showed that the cultivated tree peonies originated from homoploid hybridization among five wild species. Since the origin, thousands of cultivated varieties have spread worldwide, whereas four parental species are currently endangered or on the verge of extinction. The documentation of extensive homoploid hybridization involved in tree peony domestication provides new insights into the mechanisms underlying the origins of garden ornamentals and the way of preserving natural genetic resources through domestication.

Multilocus estimation of divergence times and ancestral effective population sizes of Oryza species and implications for the rapid diversification of the genus.

· Despite substantial investigations into Oryza phylogeny and evolution, reliable estimates of the divergence times and ancestral effective population sizes of major lineages in Oryza are challenging. · We sampled sequences of 106 single-copy nuclear genes from all six diploid genomes of Oryza to investigate the divergence times through extensive relaxed molecular clock analyses and estimated the ancestral effective population sizes using maximum likelihood and Bayesian methods. · We estimated that Oryza originated in the middle Miocene (c. 13-15 million years ago; Ma) and obtained an explicit time frame for two rapid diversifications in this genus. The first diversification involving the extant F-/G-genomes and possibly the extinct H-/J-/K-genomes occurred in the middle Miocene immediately after (within < 1 Myr) the origin of Oryza. The second giving rise to the A-/B-/C-genomes happened c. 5-6 Ma. We found that ancestral effective population sizes were much larger than those of extant species in Oryza. · We suggest that the climate fluctuations during the period from the middle Miocene to Pliocene may have contributed to the two rapid diversifications of Oryza species. Such information helps better understand the evolutionary history of Oryza and provides further insights into the pattern and mechanism of diversification in plants in general.

Phylogeny and biogeography of the rice tribe (Oryzeae): evidence from combined analysis of 20 chloroplast fragments.

Based on sequences of 20 chloroplast fragments, we generated a fully resolved phylogeny of Oryzeae and estimated divergence times of its major lineages as well as explored the historical biogeography of the tribe. Our results (1) confirmed the monophyly of Oryzeae and two-subtribe subdivision; (2) indicated that Maltebrunia, Potamophila and Prosphytochloa were genetically distinct enough to deserve generic status but Maltebrunia and Prosphytochloa were sister groups in the subtribe Oryzinae while Potamophila was a member in the subtribe Zizaniinae; (3) suggested that the previously unresolved phylogeny of the subtribe Zizaniinae was most likely explained by insufficient data due to rapid radiation; (4) provided the first well-corroborated timescale for the origin and divergence of Oryzeae, with the crown node of Oryzeae and the deepest split of Oryza at approximately 24 and 15MYA, respectively; (5) developed a biogeographic history of the tribe and substantiated the important roles of long-distance dispersal in the origin and diversification of the tribe Oryzeae.

Analysis of 142 genes resolves the rapid diversification of the rice genus.

BACKGROUND: The completion of rice genome sequencing has made rice and its wild relatives an attractive system for biological studies. Despite great efforts, phylogenetic relationships among genome types and species in the rice genus have not been fully resolved. To take full advantage of rice genome resources for biological research and rice breeding, we will benefit from the availability of a robust phylogeny of the rice genus. RESULTS: Through screening rice genome sequences, we sampled and sequenced 142 single-copy genes to clarify the relationships among all diploid genome types of the rice genus. The analysis identified two short internal branches around which most previous phylogenetic inconsistency emerged. These represent two episodes of rapid speciation that occurred approximately 5 and 10 million years ago (Mya) and gave rise to almost the entire diversity of the genus. The known chromosomal distribution of the sampled genes allowed the documentation of whole-genome sorting of ancestral alleles during the rapid speciation, which was responsible primarily for extensive incongruence between gene phylogenies and persisting phylogenetic ambiguity in the genus. Random sample analysis showed that 120 genes with an average length of 874 bp were needed to resolve both short branches with 95% confidence. CONCLUSION: Our phylogenomic analysis successfully resolved the phylogeny of rice genome types, which lays a solid foundation for comparative and functional genomic studies of rice and its relatives. This study also highlights that organismal genomes might be mosaics of conflicting genealogies because of rapid speciation and demonstrates the power of phylogenomics in the reconstruction of rapid diversification.