A domestication history of dynamic adaptation and genomic deterioration in Sorghum

Smith, Oliver; Nicholson, William V.; Kistler, Logan; Mace, Emma; Clapham, A. R.; Rose, Pamela; Stevens, Chris J.; Ware, Roselyn; Samavedam, Siva; Barker, Guy C.; Jordan, David R.; Fuller, Dorian Q.; Allaby, Robin G.

doi:10.1038/s41477-019-0397-9

Cited by 95 publications

(92 citation statements)

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“…Evidence for reduced nucleotide diversity in landraces from a genetic bottleneck 5 or population size decline 14 has also been reported for sorghum.…”

Section: Main Textmentioning

confidence: 75%

“…Additionally, Hamblin et al 32 showed that sorghum domestication is a complex process that might have included ancestral population structure, multiple domestication events, and/or introgressions from wild relatives. A recent study 14 has further shown that genetic load could have been reduced in modern lines by introgression with wild sorghum relatives. We hypothesize that the differences observed in load accumulation between maize and sorghum might be driven by both their different mating systems and domestication histories.…”

Section: Main Textmentioning

confidence: 99%

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Comparative evolutionary analysis and prediction of deleterious mutation patterns between sorghum and maize

Lozano

Gazave

Santos

et al. 2019

Preprint

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Sorghum and maize share a close evolutionary history that can be explored through comparative genomics. To perform a large-scale comparison of the genomic variation between these two species, we analyzed 13 million variants identified from whole genome resequencing of 468 sorghum lines together with 25 million variants previously identified in 1,218 maize lines.Deleterious mutations in both species were prevalent in pericentromeric regions, enriched in non-syntenic genes, and present at low allele frequencies. A comparison of deleterious burden between sorghum and maize revealed that sorghum, in contrast to maize, departed from the "domestication cost" hypothesis that predicts a higher deleterious burden among domesticates compared to wild lines. Additionally, sorghum and maize population genetic summary statistics were used to predict a gene deleterious index with an accuracy higher than 0.5. This research represents a key step towards understanding the evolutionary dynamics of deleterious variants in sorghum and provides a comparative genomics framework to start prioritizing them for removal through genome editing and breeding. 2 Main text: Sorghum ( Sorghum bicolor L. Moench) and maize ( Zea mays L.) are both members of the Poaceae family and often serve as a model system for comparative plant genomics. Their common Poaceae ancestor underwent a whole-genome duplication (WGD) event ~96 million years ago 1 , and a second WGD in maize corresponds closely with its divergence 12 million years ago from sorghum 2 . The role of polyploidization in maize diversification 1 makes the sorghum-maize system particularly powerful for comparative studies.A rchaeobotanical studies support a single sorghum domestication event around 3000 BC in Eastern Sudan 3 , with genetic studies supporting a potential second independent domestication center in west Africa 4,5 . Maize, in contrast, was domesticated once from teosinte in the Balsas river valley in central Mexico around 9000 years ago 6,7 . While some orthologs between these two species experienced parallel selection during domestication 8 , most domestication related genes appear to be drawn from a non-overlapping set 9 . It is well established that maize experienced a decline in effective population size due to a domestication bottleneck 10,11 that increased the burden of deleterious alleles in the domesticate compared to teosinte 12,13 .Evidence for reduced nucleotide diversity in landraces from a genetic bottleneck 5 or population size decline 14 has also been reported for sorghum.Sorghum has a hermaphroditic inflorescence, contributing to its predominantly self-pollinating nature. Domesticated sorghum has an estimated outcrossing rate of only 7 to 20% 9,15 , while the outcrossing rate tends to be higher (up to 70% 16 ) for weedy and wild sorghum. In contrast, maize and its wild progenitor teosinte are monoecious and generally outcrossing at a rate of over 90% 17 . In this study, we performed a joint analysis of functional variation in sorghum and 3 maize lines that span th...

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“…Evidence for reduced nucleotide diversity in landraces from a genetic bottleneck 5 or population size decline 14 has also been reported for sorghum.…”

Section: Main Textmentioning

confidence: 75%

Section: Main Textmentioning

confidence: 99%

Comparative evolutionary analysis and prediction of deleterious mutation patterns between sorghum and maize

Lozano

Gazave

Santos

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Genomic studies of ancient DNA are much less numerous in plants compared to animals remains [28-29], but have already provided fundamental insights into the process of domestication [24, [30][31][32][33][34]. The dynamic of this process is still debated and likely not the same in all species, but, as recently summarized [2], the consensus is that domestication was slow and gradual, and selected traits emerged at the cost of a decline in population size and genetic variation.…”

Section: Discussionmentioning

confidence: 99%

Ancient genomes reveal early Andean farmers selected common beans while preserving diversity

Trucchi

Benazzo

Lari

et al. 2019

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All crops are the product of a domestication process that started less than 12,000 years ago from one or more wild populations [1, 2]. Farmers selected desirable phenotypic traits, such as improved energy accumulation, palatability of seeds or reduced natural shattering [3], while leading domesticated populations through several more or less gradual demographic contractions [2, 4]. As a consequence, erosion of wild genetic variation [5] is typical of modern cultivars making them highly susceptible to pathogens, pests and environmental change [6,7]. The loss of genetic diversity hampers further crop improvement programs to increase food production in a changing world, posing serious threats to food security [8,9]. Using both ancient and modern seeds, we analyzed the temporal dynamic of genetic variation and selection during the domestication process of the common bean (Phaseolus vulgaris) that occurred in the Southern Andes. Here we show that most domestic traits were selected for prior to 2,500 years ago, with no or only minor loss of whole-genome variation. In fact, i) all ancient domestic genomes dated between 600 and 2,500 years ago are highly variable - at least as variable as a modern genome from the wild; the genetic erosion that we observe in modern cultivars is therefore a recent process that occurred in the last centuries; ii) the majority of changes at coding genes that differentiate wild and domestic genomes are already present in the ancient genomes analyzed here. Considering that most desirable phenotypic traits are likely controlled by multiple polymorphic genes [10], a likely explanation of this decoupling of selection and genomic erosion is that early farmers applied a relatively weak selection pressure [2] by using many phenotypically similar but genomically diverse individuals as breeders. Selection strategies during the last few centuries were probably less sustainable and produced further improvements focusing on few plants carrying the traits of interest, at the cost of marked genetic erosion.

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“…There are five landraces of sorghum (bicolor, kafir, guinea, caudatum, and durra) that are 100 classified based on morphology (Shehzad et al, 2009) and reflect different geographical 101 regions of adaptation (Price et al, 2005;Morris et al, 2013;Mace et al, 2013;Mullet et 102 al., 2014;Smith et al, 2019). There are also 10 intermediate landraces that are a 103 combination of the five landraces (Oliveira et al, 1996;Price et al, 2005).…”

Section: Plant Materials 99mentioning

confidence: 99%

“…Interpretation of these results within this phylogenetic context suggests that, 530 during further selection and improvement, salinity tolerance was lost in lineages that 531 were no longer subjected to continued environmental pressure. Lastly, given that S. 532 bicolor and especially the landrace durra (Smith et al, 2019) is known to be relatively 533 drought tolerant (Mullet et al, 2014;Fracasso et al, 2016;McCormick et al, 2018;Guo 534 et al, 2018) and, as with drought stress, salt stress has an initial osmotic component, we 535…”

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confidence: 98%

Phenotypic and physiological responses to salt exposure inSorghumreveal diversity among domesticated landraces

Henderson

Crim

Cumming

et al. 2019

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Phenotypic and physiological responses to salt exposure in Sorghum reveal diversity among domesticated landraces ABSTRACT 1 Soil salinity negatively impacts plant function, development, and yield. Sorghum bicolor 2 is a staple crop known to be drought tolerant, to have adapted to a variety of conditions, 3 and to contain significant standing genetic diversity, making it an exemplary species to 4 study phenotypic and physiological variation in salinity tolerance. In our study, a diverse 5 group of sorghum landraces and accessions was first rank-ordered for salinity tolerance 6 and then individuals spanning a wide range of response were analyzed for foliar proline 7 and ion accumulation. We found that, while proline is often a good indicator of osmotic 8 adjustment and is historically associated with increased salt tolerance, proline 9 accumulation in sorghum reflects stress-response injury rather than acclimation. When 10 combining ion profiles with growth responses and stress tolerance indices, the variation 11 observed in tolerance was similarly not a sole result of Na + accumulation, but rather 12 reflected accession-specific mechanisms that may integrate these and other metabolic 13 responses. When we compared variation in tolerance to phylogenetic relationships, we 14 conclude that the most parsimonious explanation for the variation observed among 15 accessions is that salinity tolerance was acquired early during domestication and was 16 subsequently maintained or lost in diverged lineages during improvement in areas that 17 vary in soil salinity. 18 19 Key words: comparative analysis, environmental adaptation, potassium sodium 20 ratio, salinity stress, sorghum landraces, Sorghum bicolor, stress tolerance index 21 22 Abbreviations: 23 RDPB: relative decrease in plant biomass 24 ST: stress tolerance 25 STI: stress tolerance index 26 27 28 Tari I, Laskay G, Takacs Z, Poor P. 2013. Response of Sorghum to abiotic stresses: A review. Journal of Agronomy and Crop Science 199: 264-274. Theerakulpisut P, Bunnag S, Kong-ngern K. 2005. Genetic diversity, salinity tolerance and physiological responses to NaCl of six rice (Oryza sativa L.) cultivars. Asian Journal of Plant Sciences.

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A domestication history of dynamic adaptation and genomic deterioration in Sorghum

Cited by 95 publications

References 60 publications

Comparative evolutionary analysis and prediction of deleterious mutation patterns between sorghum and maize

Comparative evolutionary analysis and prediction of deleterious mutation patterns between sorghum and maize

Ancient genomes reveal early Andean farmers selected common beans while preserving diversity

Phenotypic and physiological responses to salt exposure inSorghumreveal diversity among domesticated landraces

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