The origins of many plant diseases appear to be recent and associated with the rise of domestication, the spread of agriculture or recent global movements of crops. Distinguishing between these possibilities is problematic because of the difficulty of determining rates of molecular evolution over short time frames. Heterochronous approaches using recent and historical samples show that plant viruses exhibit highly variable and often rapid rates of molecular evolution. The accuracy of estimated evolution rates and age of origin can be greatly improved with the inclusion of older molecular data from archaeological material. Here we present the first reconstruction of an archaeological RNA genome, which is of Barley Stripe Mosaic Virus (BSMV) isolated from barley grain ~750 years of age. Phylogenetic analysis of BSMV that includes this genome indicates the divergence of BSMV and its closest relative prior to this time, most likely around 2000 years ago. However, exclusion of the archaeological data results in an apparently much more recent origin of the virus that postdates even the archaeological sample. We conclude that this viral lineage originated in the Near East or North Africa, and spread to North America and East Asia with their hosts along historical trade routes.

The evolution of domesticated cereals was a complex interaction of shifting selection pressures and repeated introgressions. Genomes of archaeological crops have the potential to reveal these dynamics without being obscured by recent breeding or introgression. We report a temporal series of archaeogenomes of the crop sorghum (Sorghum bicolor) from a single locality in Egyptian Nubia. These data indicate no evidence for the effects of a domestication bottleneck but instead suggest a steady decline in genetic diversity over time coupled with an accumulating mutation load. Dynamic selection pressures acted sequentially on architectural and nutritional domestication traits, and adaptation to the local environment. Later introgression between sorghum races allowed exchange of adaptive traits and achieved mutual genomic rescue through an ameliorated mutation load. These results reveal a model of domestication in which genomic adaptation and deterioration was not focused on the initial stages of domestication but occurred throughout the history of cultivation.

Transposable elements (TEs) are drivers of evolution resulting in episodic surges of genetic innovation and genomic reorganization (Oliver KR, Greene WK. 2009. TEs: powerful facilitators of evolution. Bioessays 31:703-714.), but there is little evidence of the timescale in which this process has occurred (Gingerich PD. 2009. Rates of evolution. Ann Rev Ecol Evol Syst. 40:657-675.). The paleontological and archaeological records provide direct evidence for how evolution has proceeded in the past, which can be accessed through ancient DNA to examine genomes using high-throughput sequencing technologies (Palmer SA, Smith O, Allaby RG. 2011. The blossoming of plant archaeogenetics. Ann Anat. 194:146-156.). In this study, we report shotgun sequencing of four archaeological samples of cotton using the GS 454 FLX platform, which enabled reconstruction of the TE composition of these past genomes and species identification. From this, a picture of lineage specific evolutionary patterns emerged, even over the relatively short timescale of a few thousand years. Genomic stability was observed between South American Gossypium barbadense samples separated by over 2,000 miles and 3,000 years. In contrast, the TE composition of ancient Nubian cotton, identified as G. herbaceum, differed dramatically from that of modern G. herbaceum and resembled closely the A genome of the New World tetraploids. Our analysis has directly shown that considerable genomic reorganization has occurred within the history of a domesticated plant species while genomic stability has occurred in closely related species. A pattern of episodes of rapid change and periods of stability is expected of punctuated evolution. This observation is important to understanding the process of evolution under domestication.

Genomic methylation is variable under biotic and abiotic stresses in plants. In particular, viral infection is thought to significantly increase genomic methylation with particularly high activity around transposable elements. Here we present the genomic methylation profiles of grains of archaeological barley (Hordeum vulgare) from several strata from a site in southern Egypt, from the Napatan to the Islamic periods (800 BCE – 1812 CE). One sample tested positive for viral infection and exhibits an unusually high degree of genomic methylation compared to the rest. A decreasing trend in global methylation levels according to deposition date shows in-situ de-methylation of 5-methylcytosine, which can be described as a diagenetic process. This is most likely a deamination mediated de-methylation process and is expected to lead to 5 mC > T base modifications in addition to the C > U modifications due to cytosine deamination, so represents a time-dependent process of DNA diagenesis in ancient DNA.