Reshaping of the maize transcriptome by domestication

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Although applied over extremely short timescales, artificial selection has dramatically altered the form, physiology, and life history of cultivated plants. We have used RNAseq to define both gene sequence and expression divergence between cultivated tomato and five related wild species. Based on sequence differences, we detect footprints of positive selection in over 50 genes. We also document thousands of shifts in gene-expression level, many of which resulted from changes in selection pressure. These rapidly evolving genes are commonly associated with environmental response and stress tolerance. The importance of environmental inputs during evolution of gene expression is further highlighted by large-scale alteration of the light response coexpression network between wild and cultivated accessions. Human manipulation of the genome has heavily impacted the tomato transcriptome through directed admixture and by indirectly favoring nonsynonymous over synonymous substitutions. Taken together, our results shed light on the pervasive effects artificial and natural selection have had on the transcriptomes of tomato and its wild relatives.domestication | biotic stress | abiotic stress D omestication has long served as an important example of severe phenotypic divergence in response to selection. Darwin recognized the parallel between the processes of domestication and adaptation in the wild and used this analogy to emphasize the power of selection in generating phenotypic diversity (1). The genetic basis of domestication-associated phenotypes has been examined in several instances, most notably in maize, rice, tomato, and dogs (reviewed in refs. 2-5). The clear conclusion from these studies is that the rapid phenotypic divergence associated with domestication is often attributable to very few genetic loci (6). Improvements to DNA sequence technologies have allowed studies of the effect of domestication at the whole-genome level. Early population genetic analyses in maize found that very few genes (∼5%) show evidence of positive selection during domestication of maize (7), and recent work using whole-genome resequencing has found a similar proportion of the genome was under positive selection (8). Evidence for strong selective sweeps at a limited number of loci has also been found in rice and dog genomes (9). Together with the previous genetic mapping work, these studies support the model that relatively few mutations experienced extremely strong selection by humans during domestication.Although not the target of direct positive selection, the rest of the genome still experiences a dramatic shift in evolutionary pressures during domestication. Most characterized domestication events are associated with an extreme genetic bottleneck and alleviation of selective constraints in the original niche (10). These factors are predicted to increase the relative rate of nonsynonymous to synonymous (dN/dS) substitution, potentially resulting in the fixation of deleterious alleles (11). Previous studies comparing the distribution ...

Section: Discussionmentioning

confidence: 56%

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confidence: 99%

Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato

Koenig

Jiménez‐Gómez²,

Kimura

et al. 2013

325

268

“…This technique is effective for detecting not only differentially expressed genes, but also sequence variants and new transcripts (17). Recent advances in the characterization and quantification of transcriptome with RNA-Seq have been made in rice (18), maize (19), and barley (20). In view of the large genome of barley and the wide genetic diversity of wild barley (4,14,21), RNA-Seq has become a very effective and powerful technology in generating comprehensive transcriptome profiles (22).…”

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confidence: 99%

Transcriptome profiling reveals mosaic genomic origins of modern cultivated barley

Dai

Chen

Wang

et al. 2014

The domestication of cultivated barley has been used as a model system for studying the origins and early spread of agrarian culture. Our previous results indicated that the Tibetan Plateau and its vicinity is one of the centers of domestication of cultivated barley. Here we reveal multiple origins of domesticated barley using transcriptome profiling of cultivated and wild-barley genotypes. Approximately 48-Gb of clean transcript sequences in 12 Hordeum spontaneum and 9 Hordeum vulgare accessions were generated. We reported 12,530 de novo assembled transcripts in all of the 21 samples. Population structure analysis showed that Tibetan hulless barley (qingke) might have existed in the early stage of domestication. Based on the large number of unique genomic regions showing the similarity between cultivated and wildbarley groups, we propose that the genomic origin of modern cultivated barley is derived from wild-barley genotypes in the Fertile Crescent (mainly in chromosomes 1H, 2H, and 3H) and Tibet (mainly in chromosomes 4H, 5H, 6H, and 7H). This study indicates that the domestication of barley may have occurred over time in geographically distinct regions.evolution | genetic diversity | genomic similarity | RNA-Seq | single nucleotide variants

“…Other research revealed cryptic genetic variation in teosinte associated with major domestication traits such as ear disarticulation (24), and recent genome-wide scans found evidence of human selection during domestication at many more loci than previously identified, suggesting that as much as 5% of the genome may have played a functional role in domestication (4,57). Furthermore, many of the transcription and coexpression networks of maize have been substantially modified during domestication (26), and a number of genes showing evidence of selection show directional changes in gene expression (4). The demonstrated importance of human selection on regulatory elements and gene expression (e.g., no fixed amino acid differences in the tb1 protein were found between maize and teosinte) together with known environmental effects on major domestication QTLs invite research into the effects of changing environmental conditions on Zea phenotypic change during the timeframe of maize domestication.…”

Section: Maize As a Possible Model Plant For The Study Of Developmentmentioning

confidence: 96%

“…These processes include (i) regulatory changes that targeted diverse developmental pathways and led to changes in gene expression (e.g., how, when, and to what degree existing genes are expressed through changes in the amount of mRNA during transcription); (ii) extensive rewiring of transcriptomic and coexpression networks; (iii) in an increasing number of wild progenitors, the presence and availability to the first cultivators of preexisting, nondeleterious genetic components for major domestication traits (known as "cryptic genetic variation") that induce trait variation only under specific environmental or genetic conditions; and (iv) deviations from simple Mendelian expectations (e.g., refs. 4,20,21,[23][24][25][26].…”

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confidence: 99%

Assessing elements of an extended evolutionary synthesis for plant domestication and agricultural origin research

Piperno

2017

The development of agricultural societies, one of the most transformative events in human and ecological history, was made possible by plant and animal domestication. Plant domestication began 12,000–10,000 y ago in a number of major world areas, including the New World tropics, Southwest Asia, and China, during a period of profound global environmental perturbations as the Pleistocene epoch ended and transitioned into the Holocene. Domestication is at its heart an evolutionary process, and for many prehistorians evolutionary theory has been foundational in investigating agricultural origins. Similarly, geneticists working largely with modern crops and their living wild progenitors have documented some of the mechanisms that underwrote phenotypic transformations from wild to domesticated species. Ever-improving analytic methods for retrieval of empirical data from archaeological sites, together with advances in genetic, genomic, epigenetic, and experimental research on living crop plants and wild progenitors, suggest that three fields of study currently little applied to plant domestication processes may be necessary to understand these transformations across a range of species important in early prehistoric agriculture. These fields are phenotypic (developmental) plasticity, niche construction theory, and epigenetics with transgenerational epigenetic inheritance. All are central in a controversy about whether an Extended Evolutionary Synthesis is needed to reconceptualize how evolutionary change occurs. An exploration of their present and potential utility in domestication study shows that all three fields have considerable promise in elucidating important issues in plant domestication and in agricultural origin and dispersal research and should be increasingly applied to these issues.