The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication

ResearchBlogging.org
Oryza glaberrima is an African species of rice that is not of the same origin as the Asian rice (Oryza sativa) and was independently domesticated from the progenitor Oryza barthii about 3,000 years ago.In this study recently published by Nature genetics, Wang et al. use a genomic approach to investigate the evolutionary history of O. glaberrima and to identify whether the artificial selection of this species shares common traits with the domestication process that occurred in O. sativa.

Main findings and personal comments

Sequencing genomic DNA of O. glaberrima revealed that the genome of this species consists of 316 Mb arranged in 12 chromosomes. 33,000 genes were identified with ab initio gene finding, protein homology and tentative consensus transcripts, approaches that nowadays could be efficiently replaced by RNA-seq. To determine the extent of conservation of functional genes, they selected a set of O. sativa genes to search for orthologous in O. glaberrima and found that the 95.5% of these genes were intact and syntenic. However, the 178 genes in the set belong to three very important pathways associated with flowering time and light and stress response; for this reason, I think that the extent of conservation could be overestimated when considering genes with such important functions that can be more conserved across species when compared to other regions in the genome. It would be interesting to know which is the percentage of genes conserved between the two species when considering the entire genome and keeping in account that O. sativa contains about 7,000 genes more than O. glaberrima.

As shown in Fig.1, paralogous relationships between O. glaberrima chromosomes are very common, indicating a high rate of gene duplication in this species. However, given the extent of duplicated regions one could also hypothesize a whole genome duplication followed by a progressive deletion of part of duplicated regions. To assess this idea a more detailed analysis of paralogous relationships would be required.
By comparing the heat map of genes and repeats (including transposable elements) of O. glaberrima it emerges that high gene density occurs in non-repetitive regions and vice versa (e.g. centromeric regions). TEs are very common both in O. glaberrima and O. sativa as they constitute 104 Mb and 156 Mb of the genomes, respectively; this difference is consistent with the overall size difference between the two genomes, suggesting that genome size difference could be accounted for solely by transposable elements. Furthermore, by distinguishing between insertions that occurred before and those that occurred after divergence from their common ancestor (either O. sativa or O. glaberrima specific), they found out that TEs activity has been greater in O. glaberrima and that distinct families of TEs were active in each genome. Even though I find very interesting the finding that after the divergence from their common ancestor distinct TEs family had different activities in the two species, and that this difference is responsible for at least part of the differences between the two genomes, I believe that it could be interesting to study TEs families and their activity in the wild progenitor O. barthii, to assess, for example, if TEs activity is related to domestication process and if the higher transposition rate of certain families is determined stochastically or is favored by species-specific features.

To analyze the evolutionary history of O. glaberrima, they resequenced 94 accession of the wild progenitor O. barthii from different African countries. ADMIXTURE analysis of SNPs identified in these accessions and SNPs of 20 resequenced O. glaberrima accessions, together with PCA, NJ and maximum likelihood trees, revealed that modern populations of O. barthii could be partitioned in four subgroups. One of these subgroups (OB-V) clusters with all O. glaberrima accessions and is mostly present in Western Africa; these findings suggest that O. glaberrima was domesticated directly from O. barthii subgroup OB-V in a single region along the Niger river that includes Senegal, Gambia and Guinea.

Studies of domestication in many plant species have demonstrated a reduction in genetic diversity in domesticated crops. Nucleotide diversity, minor allele frequency spectrum and linkage disequilibrium analysis conducted on SNPs identified in O. glaberrima and O. barthii accessions, confirmed that the reduction of genetic variation occurred in African rice as a consequence of domestication. However, to perform this analysis, they considered a set of SNPs from different O. barthii subgroups that, by definition, have a high degree of genetic variation. For this reason, I think that it would have been more appropriate to consider in this analysis only the SNPs identified in the subgroup OB-V that is supposed to be the progenitor of O. glaberrima.

Finally, they identified several O. glaberrima genomic regions with evidence of recent artificial selection; interestingly, many of the genes in these regions have orthologs in O. sativa that are known to be agronomically important. In particular, they identified a set of O. sativa domestication genes that was also selected during domestication of African rice. However, the mutation profiles of each orthologous pair of genes are completely different. For example, a gene that controls panicle shattering in O. sativa (OsSh1) contains an insertion in its third intron that leads to reduced transcription and shattering resistant phenotype. The orthologous region in O. glaberrima instead contains a deletion of the OsSh1 ortholog, which also leads to a shattering resistant phenotype.
These findings suggest that the selection of favorable domestication traits operated by ancient African and Asian farmers occurred independently through a convergent selection of a common set of genes during two geographically distinct domestication processes.

Wang, M., Yu, Y., Haberer, G., Marri, P., Fan, C., Goicoechea, J., Zuccolo, A., Song, X., Kudrna, D., Ammiraju, J., Cossu, R., Maldonado, C., Chen, J., Lee, S., Sisneros, N., de Baynast, K., Golser, W., Wissotski, M., Kim, W., Sanchez, P., Ndjiondjop, M., Sanni, K., Long, M., Carney, J., Panaud, O., Wicker, T., Machado, C., Chen, M., Mayer, K., Rounsley, S., & Wing, R. (2014). The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication Nature Genetics, 46 (9), 982-988 DOI: 10.1038/ng.3044