Genetic structure of pearl millet, an African cereal

Quickies

Zhenbin Hu et al., Population genomics of pearl millet (Pennisetum glaucum (L.) R. Br.): Comparative analysis of global accessions and Senegalese landraces. BMC genomics 2015. Open access → LINK [doi:10.1186/s12864-015-2255-0]

Abstract

Background

Pearl millet is a staple food for people in arid and semi-arid regions of Africa and South Asia due to its high drought tolerance and nutritional qualities. A better understanding of the genomic diversity and population structure of pearl millet germplasm is needed to support germplasm conservation and genetic improvement of this crop. Here we characterized two pearl millet diversity panels, (i) a set of global accessions from Africa, Asia, and the America, and (ii) a collection of landraces from multiple agro-ecological zones in Senegal.

Results

We identified 83,875 single nucleotide polymorphisms (SNPs) in 500 pearl millet accessions, comprised of 252 global accessions and 248 Senegalese landraces, using genotyping by sequencing (GBS) of PstI-MspI reduced representation libraries. We used these SNPs to characterize genomic diversity and population structure among the accessions. The Senegalese landraces had the highest levels of genetic diversity (π), while accessions from southern Africa and Asia showed lower diversity levels. Principal component analyses and ancestry estimation indicated clear population structure between the Senegalese landraces and the global accessions, and among countries in the global accessions. In contrast, little population structure was observed across in the Senegalese landraces collections. We ordered SNPs on the pearl millet genetic map and observed much faster linkage disequilibrium (LD) decay in Senegalese landraces compared to global accessions. A comparison of pearl millet GBS linkage map with the foxtail millet (Setaria italica) and sorghum (Sorghum bicolor) genomes indicated extensive regions of synteny, as well as some large-scale rearrangements in the pearl millet lineage.

Conclusions

We identified 83,875 SNPs as a genomic resource for pearl millet improvement. The high genetic diversity in Senegal relative to other regions of Africa and Asia supports a West African origin of this crop, followed by wide diffusion. The rapid LD decay and lack of confounding population structure along agro-ecological zones in Senegalese pearl millet will facilitate future association mapping studies. Comparative population genomics will provide insights into panicoid crop evolution and support improvement of these climate-resilient crops.

Fig. 4

The genetic relatedness of pearl millet accessions. a F-statistic (F _ST ) between populations with different origins. The circles indicate the countries of origin, and the values represent the F _ST between accessions from the two countries. The thickness of the lines is proportional to the value of F _ST . b Genetic relatedness among 500 accessions assessed with the neighbor joining method. Global accessions are colored by countries of origin, and Senegalese landraces are colored by regions of origin

See also: Review of Tropical Neolithic flows (a most important agricultural development in the African and Asian Tropics).

Plants do use epigenetics to adapt to diverse environments

If you've ever grown plants that come from a distant land, you may be familiar with the fact that you may need an adaptive process of one or more generations to get the best of them. Oddly enough this time is often too short for genetic adaption to happen and sweep over, especially as most of the ill-adapted plants don't really die nor fail to reproduce (i.e. they are not too aggressively selected against). How does it happen then? Epigenetics may have the answer.

Robert J. Schmidt et al., Patterns of population epigenomic diversity. Nature 2013. Pay per view → LINK [doi:10.1038/nature11968]

Abstract

Natural epigenetic variation provides a source for the generation of phenotypic diversity, but to understand its contribution to such diversity, its interaction with genetic variation requires further investigation. Here we report population-wide DNA sequencing of genomes, transcriptomes and methylomes of wild Arabidopsis thaliana accessions. Single cytosine methylation polymorphisms are not linked to genotype. However, the rate of linkage disequilibrium decay amongst differentially methylated regions targeted by RNA-directed DNA methylation is similar to the rate for single nucleotide polymorphisms. Association analyses of these RNA-directed DNA methylation regions with genetic variants identified thousands of methylation quantitative trait loci, which revealed the population estimate of genetically dependent methylation variation. Analysis of invariably methylated transposons and genes across this population indicates that loci targeted by RNA-directed DNA methylation are epigenetically activated in pollen and seeds, which facilitates proper development of these structures.

From the body of the article:

Epiallele formation in the absence of genetic variation can result in phenotypic variation, which is most evident in the plant kingdom, as exemplified by the peloric and colorless non-ripening variants from Linaria vulgaris and Solanum lycopersicum, respectively^{6, 7}. Although rates of spontaneous variation in DNA methylation and mutation can be decoupled in the laboratory^{8, 9, 10, 11}, in natural settings, these two features of genomes co-evolve to create phenotypic diversity on which natural selection can act.

...

Similarly to the limited examples of pure epialleles (methylation variants that form independent of genetic variation), few examples of DNA methylation variants linked to genetic variants are known^{15, 16, 17}.

And the 'Conclusion remarks' (emphasis is mine):

Natural epigenomic variation is widespread within A. thaliana, and the population-based epigenomics presented here has uncovered features of the DNA methylome that are not linked to underlying genetic variation, such as all forms of SMPs and CG-DMRs. However, C-DMRs have positional association decay patterns similar to linkage disequilibrium decay patterns for SNPs and in some cases are associated with genetic variants, but the majority of C-DMRs were not tested by association mapping due to low allele frequencies and could result from rare sequence variants. Our combined analyses of genetic and methylation variation did not uncover a correlation between major effect mutations and genes silenced by RdDM, suggesting that this pathway may target these genes for another purpose. This purpose could be to restrict expression from vegetative tissues similarly to transposons. Another possible purpose of being targeted by RdDM could be to coordinate expression specifically in pollen and in seed to ensure proper gametophytic and embryonic development. Animals also use small RNA-directed DNA methylation and heterochromatin formation mechanisms to maintain the epigenome of the germ line through the use of Piwi-interacting RNAs³⁶. In both plants and animals these small RNAs are derived from the genome of companion cells, which are terminal in nature and can afford widespread reactivation of transposon and repeat sequences as they are not passed on to the next generation. Our study provides evidence that RdDM-targeted genes may have co-opted this transposon silencing mechanism to maintain their silenced state in vegetative tissues and transgenerationally, as well as to ensure proper expression important for pollen, seed and germ line development.

Olive domestication origins tracked to West Asia

Olive tree - Pelion, Greece
(CC by Dennis Koutou)

A new genetic study claims that the origins of olive domestication are in West Asia, more precisely at the Turkish-Syrian border (Kurdistan again?), apparently settling the doubts on whether this tree's domestic variant may have originated either in that area, the Aegean Sea basin, Southern Iberia or North Africa, or even that many independent domestications had taken place.

G. Besnard et al., The complex history of the olive tree: from Late Quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant. Proceedings of the Royal Society B, 2013. Pay per view → LINK [doi: 10.1098/rspb.2012.2833]

Abstract

The location and timing of domestication of the olive tree, a key crop in Early Mediterranean societies, remain hotly debated. Here, we unravel the history of wild olives (oleasters), and then infer the primary origins of the domesticated olive. Phylogeography and Bayesian molecular dating analyses based on plastid genome profiling of 1263 oleasters and 534 cultivated genotypes reveal three main lineages of pre-Quaternary origin. Regional hotspots of plastid diversity, species distribution modelling and macrofossils support the existence of three long-term refugia; namely the Near East (including Cyprus), the Aegean area and the Strait of Gibraltar. These ancestral wild gene pools have provided the essential foundations for cultivated olive breeding. Comparison of the geographical pattern of plastid diversity between wild and cultivated olives indicates the cradle of first domestication in the northern Levant followed by dispersals across the Mediterranean basin in parallel with the expansion of civilizations and human exchanges in this part of the world.

The study was made only on chloroplast DNA, roughly equivalent to animal mtDNA, transmitted only by the "female" line (notice that olive trees, as most plants are dioic, having both sexes and also that the preferred method of agricultural reproduction today is growing new trees from stumps, i.e. cloning). However André Berville, geneticist of the French National Institute for Agricultural Research prefers to remain cautious because, in his opinion, looking only at chloroplast DNA is not enough.

"Pollen from the olive tree is wind-transported, so it can migrate long distances" he said. 

Combining both types of DNA would allow researchers to understand both how local olive tree cultivation occurred and how more long-distance changes occurred, he said. 

Secondary source: NBC News (via Pileta). 

Some genetic support for South China origin of rice

CC by IRRI Images

I really miss Vietnam and other parts of Indochina (Cambodia, Thailand...) in this oh-so-Chinese study. Draw a line on a map and go to sleep...

Xin Wei et al., Origin of Oryza sativa in China Inferred by Nucleotide Polymorphisms of Organelle DNA. PLoS ONE 2012. Open access ··> LINK [doi]

Abstract

China is rich of germplasm resources of common wild rice (Oryza rufipogon Griff.) and Asian cultivated rice (O. sativa L.) which consists of two subspecies, indica and japonica. Previous studies have shown that China is one of the domestication centers of O. sativa. However, the geographic origin and the domestication times of O. sativa in China are still under debate. To settle these disputes, six chloroplast loci and four mitochondrial loci were selected to examine the relationships between 50 accessions of Asian cultivated rice and 119 accessions of common wild rice from China based on DNA sequence analysis in the present study. The results indicated that Southern China is the genetic diversity center of O. rufipogon and it might be the primary domestication region of O. sativa. Molecular dating suggested that the two subspecies had diverged 0.1 million years ago, much earlier than the beginning of rice domestication. Genetic differentiations and phylogeography analyses indicated that indica was domesticated from tropical O. rufipogon while japonica was domesticated from O. rufipogon which located in higher latitude. These results provided molecular evidences for the hypotheses of (i) Southern China is the origin center of O. sativa in China and (ii) the two subspecies of O. sativa were domesticated multiple times.

The main interest of the study is to compare Oryza sativa (domestic rice) with O. rufipogon (wild rice and the ancestor of the former). It soon becomes obvious that both are the same species and that all O. sativa cluster with specific subpopulations of O. rufipogon (red rice, considered a weed):

Figure 3. Population structuring of O. sativa and O.rufipogon.

Complementarily a haploid phylogeny is studied and mapped by geography:

Figure 4. A map showing the sampled populations of O. rufipogon and the distribution of haplotypes.

From fig.2 we know that H1 corresponds to the haplotype found in O. sativa var. japonica (temperate climate variant) and that H2 and H3 correspond with the haplotypes found in O. sativa var. indica (tropical variant).

However notice how rare is the indica cluster in Tropical China O. rufipogon and that the exact combo only seems to show up in Hainan. For this reason, I would suggest future researchers to study the ancestor species also in Indochina, so we can understand better the origins of rice and particularly the indica variant, especially associated to Austroasiatic speakers now living almost exclusively in Indochina and parts of India.

Genetic insights on tomato origins

Who doesn't love tomato? Well, my dad. But besides him... 

But one thing is loving tomato sauce, tomato salad, tomato in sandwich or other tomato based cuisine and another thing is to know much about its origins. 

While it is generally accepted that Europeans brought tomato from Mexico, the species has its greatest diversity in the Andean region. This new study should help us to better understand the nuances of tomato origins:

José Blanca et al., Variation Revealed by SNP Genotyping and Morphology Provides Insight into the Origin of the Tomato. PLoS ONE, 2012. Open access ··> LINK [doi:10.1371/journal.pone.0048198]

Abstract

Tomato, Solanum lycopersicum, is divided into two widely distributed varieties: the cultivated S. lycopersicum var. lycopersicum, and the weedy S. lycopersicum var. cerasiforme. Solanum pimpinellifolium is the most closely related wild species of tomato.

The roles of S. pimpinellifolium and S. l. cerasiforme during the domestication of tomato are still under debate. Some authors consider S. l. cerasiforme to be the ancestor, whereas others think that S. l. cerasiforme is an admixture of S. pimpinellifolium and the cultivated S. l. lycopersicum. It is also not clear whether the domestication occurred in the Andean region or in Mesoamerica. We characterized 272 accessions (63 S. pimpinellifolium, 106 S. l. cerasiforme, 95 S. l. lycopersicum and 8 derived from hybridization processes) were morphologically and genetically using the SolCap platform (7,414 SNPs). The two species were distinguished in a PCA analysis and displayed a rich geographic structure. Solanum lycopersicum var. cerasiforme and S. l. lycopersicum were also differentiated in the PCA and Structure analyses, which supports maintaining them as different varieties. Solanum pimpinellifolium and the Andean S. l. cerasiforme were more diverse than the non-Andean S. lycopersicum. Solanum lycopersicum var. cerasiforme was morphologically and molecularly intermediate between S. pimpinellifolium and tomato. Solanum lycopersicum var. cerasiforme, with the exception of several Ecuadorian and Mexican accessions, is composed of the products of admixture processes according to the Structure analysis. The non-admixtured S. l. cerasiforme might be similar to the ancestral cultivars from which the cultivated tomato originated, and presents remarkable morphological diversity, including fruits of up to 6 cm in diameter. The data obtained would fit a model in which a pre-domestication took place in the Andean region, with the domestication being completed in Mesoamerica. Subsequently, the Spaniards took plants from Mesoamerica to Spain and from there they were exported to the rest of the world.

Fig. 2A (with legend from fig. 1) - PCA analysis of the S. lycopersicum samples

East Asian oaks in the Ice Age

It may sound botanically erudite but it is also of great relevance in order to better understand the ecology and geography of people living in East Asia in the Upper Paleolithic. Hence worth mentioning here.

Dongmei Chen et al., Phylogeography of Quercus variabilis Based on Chloroplast DNA Sequence in East Asia: Multiple Glacial Refugia and Mainland-Migrated Island Populations. PLoS ONE 2012. Open access ··> LINK [doi:10.1371/journal.pone.0047268]

Abstract

The biogeographical relationships between far-separated populations, in particular, those in the mainland and islands, remain unclear for widespread species in eastern Asia where the current distribution of plants was greatly influenced by the Quaternary climate. Deciduous Oriental oak (Quercus variabilis) is one of the most widely distributed species in eastern Asia. In this study, leaf material of 528 Q. variabilis trees from 50 populations across the whole distribution (Mainland China, Korea Peninsular as well as Japan, Zhoushan and Taiwan Islands) was collected, and three cpDNA intergenic spacer fragments were sequenced using universal primers. A total of 26 haplotypes were detected, and it showed a weak phylogeographical structure in eastern Asia populations at species level, however, in the central-eastern region of Mainland China, the populations had more haplotypes than those in other regions, with a significant phylogeographical structure (NST = 0.751 > GST = 0.690, P < 0.05). Q. variabilis displayed high interpopulation and low intrapopulation genetic diversity across the distribution range. Both unimodal mismatch distribution and significant negative Fu’s F_S indicated a demographic expansion of Q. variabilis populations in East Asia. A fossil calibrated phylogenetic tree showed a rapid speciation during Pleistocene, with a population augment occurred in Middle Pleistocene. Both diversity patterns and ecological niche modelling indicated there could be multiple glacial refugia and possible bottleneck or founder effects occurred in the southern Japan. We dated major spatial expansion of Q. variabilis population in eastern Asia to the last glacial cycle(s), a period with sea-level fluctuations and land bridges in East China Sea as possible dispersal corridors. This study showed that geographical heterogeneity combined with climate and sea-level changes have shaped the genetic structure of this wide-ranging tree species in East Asia.

 
Maybe most interesting of all is this map: 

Figure 5. Ecological niche modelling.

Predicted distribution probability (in logistic value) is shown in each 2.5 arc-min pixel, based on the palaeodistribution modelling at present (0BP) (a) and at the last glacial maximum (LGM) (21KaBP) (b). The distribution of river systems on the exposed East China Sea during the LGM was drawn from Shota et al. (2012). Occurrence records of Q. variabilis at present are also plotted as black points in the maps.

Much more data for those interested in the genetic details can be found in the paper. 

Genetic history of European barley

Barley

Nice new information on the genetics of Hordeum vulgare that may help to understand the Neolithic in Europe:

Huw Jones et al. Evolutionary history of barley cultivation in Europe revealed by genetic analysis of extant landraces. BMC Evolutionary Biology 2011. Open access.

These landraces are what was being grown traditionally before the advent of 20th century industrial homogenization of crops. The authors discern nine populations using STRUCTURE, however, as we can see in fig. 4 below, some of these populations are paraphyletic.

Fig. 6 Geographical distributions of landraces for each of the barley populations
identified at K = 9. (Note: Pop3 is restricted to the Alps, barely visible)

Fig. 4 Neighbour-joining tree constructed from
the microsatellite genotypes of all accessions

The authors inform us in greater detail of the characteristics of the various populations within the paper's "origins of the populations" section.

Coconut scatter shows that, once established, a population structure is hard to alter

You may have heard of this by now:

B. F. Gunn et al, Independent Origins of Cultivated Coconut (Cocos nucifera L.) in the Old World Tropics. PLoS ONE 2011. Open access.

I was a bit perplex at first because what I have read around is that this paper somehow demonstrates that coconuts only spread with human domestication and colonizing flows. This is a most extreme claim which hardly fits the nature of this plant, which is not truly a domesticate but a widely exploited wild plant in fact. It is a very hardy plant that grows primarily at the high tide line and is naturally transported across the oceans by mere drift.

Fig. 2 has the essence of the paper

It is evident from this paper that coconuts have at least two distinct ancestral populations: one seemingly originated in South Asia and the other from SE Asia/Pacific, that its dispersal to the Atlantic Ocean happened necessarily with human help and that the East African population while essentially the Indian variety, has some admixture from the SE Asian/Pacific variants.

Coconut germinating at a volcanic beach

This last element is argued by the authors to signify human influence by means of the Austronesian colonists of Madagascar. While this is plausible I see no definitive argument for this logic in fact. Similarly I fail to see the hand of Austronesians in the Pacific  scatter as something cast on iron, rather as just a possibility. 

The only clear case of human intervention are the Dwarf variants because they are self-pollinating and this is not a trait you typically find in wild plants. But the Dwarf component is relatively rare and is not even present in the alleged Austronesian-mediated arrivals to East Africa and South America (Panama variant). 

So I am not really persuaded of their thesis that most of this structure was caused by humans. It is possible but very far from demonstrated in fact. 

Regardless, what eventually brought me to write this entry was after all their other discovery, which is quite solid and obvious: that in spite of the palm being so widely exploited and moved around in the Modern Era, the original genetic structure has persisted almost unaffected. 

This is quite astonishing because copra (dried coconut flesh) and palm oil, as well as the fibre and the fresh fruit, so suitable as natural preserve for the long travels of sailors of not so long ago, make the coconut a clear candidate for extensive alteration of its ancestral genetic landscape, yet it has resisted all that almost impassible in all its range from Africa to South America. 

A lesson to be assimilated by all those who happily proclaim that established populations can easily be altered. It can happen indeed but it is not easy.