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ResearchBlogging.orgThe Pith: the spread of domestic rice may be a function not of the spread of rice per se, as much as a specific narrow set of genes which confer domestication to disparate rice lineages.

This has been a big month for rice. At least for me. Despite my background as a rice-eater I’ve generally moved away from it of late. It’s an American thing, as we’ve replaced a fear of fat with a fear of refined carbohydrates. My parents have even shifted from white rice to brown rice because of concerns with type 2 diabetes (this caused some consternation in 2004, as when we visited Bangladesh as honored guests my father was given to lecturing our hosts about the evils of the white rice on offer. Remember that in these societies brown rice is often considered the fair of the poor). But the reality is that much of the Old World of Asia still relies on rice, and will do so for the foreseeable future. So I still take an inordinate interest in the oriental staff-of-life. I already reviewed two papers on rice genetics recently, but now it’s time for a third.

Some things are similar, some things are different. Again the stars of the show are the two cultivars of O. ativa, indica and japonica, and wild rice, O. rufipogon, from which the domestic varieties are presumably derived. The question at issue are the possible differences in the genealogy of the total genome background of rice cultivars vs. particular regions of the genome relevant for domestication. In other words, did the genes responsible for domesticate traits spread and sweep across different rice lineages? Or are different rice lineages simply derived from a common ancestor which carried the original domestication traits from a singular selection event? The first paper I reviewed suggested that there was one single domestication event, and that later differentiation between indica and japonica may simply have been a function of isolation and possible hybridization with local wild strains in the case of indica. The second paper focused on genes responsible for domestication seemed to imply that indica and japonica may have been shaped by different selection events (more precisely, they couldn’t detect signatures of selection in indica at the same loci that they did for japonica). A new paper in PLoS Genetics seems to take a broader view, highlighting both the phylogeny of the total genome as a whole and the bouts of natural selection which might have reshaped specific genes in a particular manner. Two Evolutionary Histories in the Genome of Rice: the Roles of Domestication Genes:

The origin of two cultivated rice Oryza sativa indica and O. sativa japonica has been an interesting topic in evolutionary biology. Through whole-genome sequencing, we show that the rice genome embodies two different evolutionary trajectories. Overall genome-wide pattern supports a history of independent origin of two cultivars from their wild population. However, genomic segments bearing important agronomic traits originated only once in one population and spread across all cultivars through introgression and human selection. Population genetic analysis allows us to pinpoint 13 additional candidate domestication genes.

From what I can gather the paper which argued for a common origin of indica and japonica in the same domestication event covered a much smaller fraction of the genome than this paper. All things equal then I’d lean toward the assessment of the relationship between the two in this paper, though they aren’t particular unequivocal either as to the relationship between indica and japonica. As in the second paper on domestication genes and selection they found a lot more diversity on indica than japonica. In fact indica was only marginally less diverse than rufipogon. The big headline results are in figure 5. The top two panels, A and C, are just showing you θ across the respective chromosomes for each lineage. θ is just a measure of nucelotide diversity. The higher the θ, the more diverse the genomic region. R, J, and I are the three rice lineages, rufipogon, japonica, and indica. The second two panels show the genetic distance between two pairwise lineages using Fst measures. Fst just reports the amount of genetic diversity which is partitioned in group level differences (e.g., Fst across continental human races is ~0.15). As Fst approaches 0, that means all the genetic diversity can be reduced to variance within the groups. As Fst approaches 1, that means that all the diversity can be accounted for by noting the differences between groups.

It’s pretty clear from these panels that japonica is the outlier when it comes to genetic diversity. It doesn’t have nearly as much as the other two lineages. This is in line with what the paper I blogged last week reported. In fact, there’s not much of a difference between indicia and rufipogon using this statistic. But when you move to between population differences an interesting pattern emerges. Across much of these two chromosomes (rice as 12 chromosomes by the way) the three lineages exhibit about equal genetic distance from each other, but there are segments of sharply decreased genetic distance between the two domestic cultivars! These are extended regions of reduced genetic diversity overall. And very interestingly some genes implicated in domestication are found just here. Of course it may be that the alleles which can drive domestication were part of the standing genetic variation of the wild lineages. This means that there’s a normal range of variation in a population, and independent selection events swept up in frequency the same alleles derived from the ancestral wild types. But this is not what it looks like when you examine the genomic regions around these alleles. They share the same exact variants, which implies a common selective sweep event in which an ancestral allele and its neighbors were the target of a powerful adaptive force.

The authors suggest that this peculiar constellations of disjunctions in the evolutionary histories of different regions of the genome can not be explained by simple demographic processes such as selfing, bottlenecks, etc. Rather, it is the outcome of a complex process whereby hybridization events allowed from the introgression of ancestral domestication genes from one lineage to another, and the sweeping to fixation of these domestication genes across two lineages with very different ancestries. In other words, common traits don’t always emerge from common ancestors, but rather, often from common experiences.

We know this for humans. The figure to the right is from Genetic Evidence for the Convergent Evolution of Light Skin in Europeans and East Asians. A of this figure shows the total genetic distances between West Africans (WA), Europeans (EU), South Asians (SA), Island Melanesians (EA), and Native Americans (NA). Each successive panel shows genetic distances on specific loci implicated in variation in pigmentation. Notice how incongruent they are with the tree in A in many cases. Look at E, where Europeans are a clear outgroup on the locus, and all other populations cluster. This is a variant on SLC45A2 which is highly diagnostic of Europeans, and is correlated with light complexion (the minority of Europeans who carry the variant found in the rest of the world are much more likely to have dark eyes, black hair, and olive skin, than not). We don’t need to go into the possible evolutionary reasons why dark skin and light skin are distributed as they are here. Rather, we can see in the case of this trait that the histories of the specific genes may not reflect the history as told in the total genome content, because of the importance of local adaptations and selection pressures. The case of rice may be an inversion, insofar as instead of a location adaptation differentiating relatively closer groups (e.g., look at South Asians vs. Europeans in C, D, and E), it may be a case where very different groups exhibit similarities because of convergent evolution. That convergent pressure being the impulse toward domestication.

Speaking of which, that impulse may be related to the arrival of the Munda populations from Southeast Asia into India. If the model above is correct than indica was a local cultivar, perhaps at some stage of domestication, which was improved by hybridization with japonica. Eventually admixture swamped out most of the japonica genetic background, but recurrent selection favored japonica alleles at a large set of loci implicated in domestication. In this paper they lacked the power to ascertain whether the haplotypes jumped from indica to japonica or vice versa. But I’d be willing to bet $250 dollars that it is going to turn out to have come from japonica because of other aspects of archeobotany, combined with japonica‘s extreme homogeneity, which may be a hallmark of a process of a very powerful set of selection events which gave rise to domestic rice.

Citation: Ziwen He, Weiwei Zhai, Haijun Wen, Tian Tang1, Yu Wang, Xuemei Lu, Anthony J. Greenberg, Richard R. Hudson, Chung-I Wu, & Suhua Shi (2011). Two Evolutionary Histories in the Genome of Rice: the Roles of Domestication Genes PLoS Genetics : 10.1371/journal.pgen.1002100

(Republished from Discover/GNXP by permission of author or representative)
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The Pith: What makes rice nice in one varietal may not make it nice in another. Genetically that is….

Rice is edible and has high yields thanks to evolution. Specifically, the artificial selection processes which lead to domestication. The “genetically modified organisms” of yore! The details of this process have long been of interest to agricultural scientists because of possible implications for the production of the major crop which feeds the world. And just as much of Charles Darwin’s original insights derived from his detailed knowledge of breeding of domesticates in Victorian England, so evolutionary biologists can learn something about the general process through the repeated instantiations which occurred during domestication during the Neolithic era.

A new paper in PLoS ONE puts the spotlight on the domestication of rice, and specifically the connection between particular traits which are the hallmark of domestication and regions of the genome on chromosome 3. These are obviously two different domains, the study and analysis of the variety of traits across rice strains, and the patterns in the genome of an organism. But they are nicely spanned by classical genetic techniques such as linkage mapping which can adduce regions of the genome of possible interesting in controlling variations in the phenotype. In this paper the authors used the guidelines of the older techniques to fix upon regions which might warrant further investigation, and then applied the new genomic techniques. Today we can now gain a more detailed sequence level picture of the genetic substrate which was only perceived at a remove in the past through abstractions such as the ‘genetic map.’ Levels and Patterns of Nucleotide Variation in Domestication QTL Regions on Rice Chromosome 3 Suggest Lineage-Specific Selection:

Oryza sativa or Asian cultivated rice is one of the major cereal grass species domesticated for human food use during the Neolithic. Domestication of this species from the wild grass Oryza rufipogon was accompanied by changes in several traits, including seed shattering, percent seed set, tillering, grain weight, and flowering time. Quantitative trait locus (QTL) mapping has identified three genomic regions in chromosome 3 that appear to be associated with these traits. We would like to study whether these regions show signatures of selection and whether the same genetic basis underlies the domestication of different rice varieties. Fragments of 88 genes spanning these three genomic regions were sequenced from multiple accessions of two major varietal groups in O. sativaindica and tropical japonica—as well as the ancestral wild rice species O. rufipogon. In tropical japonica, the levels of nucleotide variation in these three QTL regions are significantly lower compared to genome-wide levels, and coalescent simulations based on a complex demographic model of rice domestication indicate that these patterns are consistent with selection. In contrast, there is no significant reduction in nucleotide diversity in the homologous regions in indica rice. These results suggest that there are differences in the genetic and selective basis for domestication between these two Asian rice varietal groups.

Here’s what seems relevant for the two domestic varieties from Wikipedia:

Oryza sativa contains two major subspecies: the sticky, short grained japonica or sinica variety, and the non-sticky, long-grained indica variety. Japonica are usually cultivated in dry fields, in temperate East Asia, upland areas of Southeast Asia and high elevations in South Asia, while indica are mainly lowland rices, grown mostly submerged, throughout tropical Asia….

There’s long been debate about the exact phylogenetic relationship between these two strains of domestic rice. More on that later. In regards to domestication there are three categories we need to focus on in terms of adaptation: 1) traits which are common to all domestic cereals and tend to crop up almost immediately, 2) traits which are extensions and improvements upon the initial domestic prototype, 3) traits which are regional diversifications, often adaptations to climate. Consider an analogy to horses. The original domestic horse was rather small, and was only fit for drawing chariots. Eventually the breeds became larger, and suitable for cavalry. Finally, there was a diversification by task (e.g., workhorses vs. race horses) and to some extent climate.

As noted above previous classical genetic techniques had narrowed down the genetic regions responsible for various domesticate traits when comparing japonica to the wild rufipogon. Since domestication usually entails a process of selection the authors naturally presumed that they might be able to detect signatures of selection within the genome. What are the genomic tells of selection?

There are many, just as there are different types of selection. In this case what we know suggests that due to #1 there’s going to be an initial bout of adaptation and rapid shift from wild diversity to fixed traits suitable for a crop which is going to be controlled by humans. Just as the riotous diversity of the wild varieties become constrained to monocultures, so the diversity of the wild type often gets swept away by a few genetic variants which are responsible for the favored traits. So what they might see in the domestic varieties is a sharp reduction of variation around the quantitative trait loci (QTLs) reported earlier, because those QTLs have presumably been the target of selection. In other words, a selective sweep.

That’s what they found. At least in one lineage.

Left to right you have indica, japonica, and rufipogon. Front to back in each chart you see the three QTLs, and the distribution of nucleotide diversities by genetic fragments within these QTLs. The extremely skewed distribution of the domestic varieties in relation to the wild type rufipogon is rather obvious. Additionally, you see a stronger skew in japonica in relation to indica. The skew in the domestic strains is toward a greater proportion of the fragments having very low nucleotide diversity.

What could cause this? You need a further piece of information here. The domestic varieties have long regions of the genome characterized by linkage disequilibrium (actually, japonica is so homogeneous that you barely have enough variation to calculate LD!). So particular genetic variants are associated with each other, resulting in long runs of similar sequences, haplotypes. It’s as if a chunk of some ancient chromosome just “blew up” and took over that segment of the genome in japonica.

Natural selection could do this. Imagine that an ancestral rufipogon has a genetic variant which confers a domestic trait. It would be selected. Even if crossed with other strains with other domestic characteristics its particular QTL would be transmitted down to the descendants in general. But not only would the specific genetic variant which conferred the favored trait be passed on, but many of the flanking genomic regions carrying other variants would also be transmitted! This explains the extremely low genetic diversity in japonica, if there’s a sweep up in frequency of a particular ancestral haplotype then what were polymorphisms in the wild type become monomorphic in the domesticate.

Another explanation though could be that demographic history produced these results. Random genetic drift due to small populations, whether via bottleneck or systematic inbreeding/selfing, can also drive up the frequency of alleles favored by lady-luck and render extinct all others. To check for this the authors constructed a model where japonica and indica went through bottlenecks enforced by the domestication (note that strong selection can drive down population size as well). Even with this model the diversity in japonica in these QTLs remained far too low (though indica’s skew did not reach statistical significance).

Since both of the domestic strains exhibit traits of domestication the lack of a selective event in indica at these QTLs does not allow us to infer that there are no genes which were selected for these traits in the past in indica. On the contrary, there certainly were and are such genes. But where are they? The authors moot the possibility that selection exists at the loci under consideration, but was simply missed because the selection was by a different dynamic which might not be picked up by their test. For various reasons they are skeptical of this on its own merits, but I think the bigger issue is that the original linkage mapping was performed with japonica vs. wild type strains, so naturally if the two domestic subspecies differed in their genetic architectures then the QTLs of interest of indica would not be discovered simultaneously.

Something which I’m rather perplexed by is how this comports or aligns with the finding by many of the same researchers that the two domestic varietals derive from the same ancestral population which was domesticated from East Asian wild rice. It could be that the history of domestication is more serial than we know, and that the common QTLs to both japonica and indica have been rendered irrelevant by new adaptations subsequent to their separation. Or, one or the other may have experienced introgression at that locus and so diverged after domestication. Interestingly in figure 7 of the paper they show that phylogenetic trees which illustrates the relationship of alleles associated with each strain. It indicates that indica is not monophyletic on these regions, while japonica is. This means that the japonica variants share a common ancestor, from which all are descended. In contrast, indica variants do not. Such a pattern is consistent with the story of strong positive selection upon a single variant at some time in the past for japonica. From what I can tell they may actually have sent the PLoS ONE paper to the reviewers before the PNAS paper which I reviewed earlier. Because these two papers were published so close to each other they don’t cite each other, though in some ways the first paper in PNAS would have fleshed out the natural history of domestic rice somewhat. As it is, they kind of leave of us hanging in relation to indica.

Why does all of this matter? Yes, agricultural genetics is important for agriculture. But let’s get back to people. There is a hypothesis that man is a ‘self-domesticated’ organism. Whatever quibbles I have with artificial terms like domestication I do think that there may be broad analogies to be drawn between our own species and the organisms associated with us.

Citation: Xianfa Xie1, Jeanmaire Molina, Ryan Hernandez, Andy Reynolds, Adam R. Boyko, Carlos D. Bustamante, & Michael D. Purugganan (2011). Levels and Patterns of Nucleotide Variation in Domestication QTL Regions on Rice Chromosome 3 Suggest Lineage-Specific Selection PLoS ONE : 10.1371/journal.pone.0020670

Image Credit: IRRI Images

(Republished from Discover/GNXP by permission of author or representative)
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Razib Khan
About Razib Khan

"I have degrees in biology and biochemistry, a passion for genetics, history, and philosophy, and shrimp is my favorite food. If you want to know more, see the links at"