Person: Caicedo, Ana
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Associate Professor, Department of Biology, College of Natural Sciences
Last Name
Caicedo
First Name
Ana
Discipline
Biology
Genomics
Molecular Genetics
Genomics
Molecular Genetics
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Introduction
Adaptive evolution, the product of natural selection, underlies much of all biological diversity. My research seeks to understand the genetic basis of adaptation, as well as the population and genomic context in which adaptive evolution occurs. To this effect, research interests in the lab span a range of disciplines, including population genetics, molecular evolution, evolutionary ecology, phylogeography, and evolutionary genomics. We focus on the study of loci contributing to traits of evolutionary or ecological importance and the processes governing diversification within and between closely related plant species. Among the questions we address are: Which are the genes underlying adaptive traits? How is variation at these genes distributed at the population level? What evolutionary forces act on these genes and what are their molecular signatures? What role does the genomic context play in the evolution of ecologically important genes?
Our research makes use of model organisms (e.g. Arabidopsis thaliana), wild relatives of crop species (e.g. Solanum spp., Oryza spp.), and domesticated plant species (e.g. cultivated rice, O. sativa). The process of domestication, in particular, can provide insight into rapid evolution and adaptive responses under strong selection. By comparing domesticated species with their wild and weedy relatives we can learn about the genetic/genomic changes that accompany domestication, and those leading to adaptation in agricultural environments. Understanding of selective processes in the wild can also be gained by studying the wild relatives of domesticated plants; the genetic and genomic resources available for many crop species can inform the search for ecologically relevant genes and the characterization of genomic variation. Current projects in the lab include the molecular evolution of genes associated with weedy phenotypes in red rice (a weedy form of O. sativa) and the identification of genes contributing to diversification and stress tolerance in the wild tomato relative, S. cheesmaniae.
Our research makes use of model organisms (e.g. Arabidopsis thaliana), wild relatives of crop species (e.g. Solanum spp., Oryza spp.), and domesticated plant species (e.g. cultivated rice, O. sativa). The process of domestication, in particular, can provide insight into rapid evolution and adaptive responses under strong selection. By comparing domesticated species with their wild and weedy relatives we can learn about the genetic/genomic changes that accompany domestication, and those leading to adaptation in agricultural environments. Understanding of selective processes in the wild can also be gained by studying the wild relatives of domesticated plants; the genetic and genomic resources available for many crop species can inform the search for ecologically relevant genes and the characterization of genomic variation. Current projects in the lab include the molecular evolution of genes associated with weedy phenotypes in red rice (a weedy form of O. sativa) and the identification of genes contributing to diversification and stress tolerance in the wild tomato relative, S. cheesmaniae.
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Publication Molecular Evolution of the Rice Blast Resistance Gene Pi-ta in Invasive Weedy Rice in the USA(2011-01-01) Caicedo, Ana; Lee, S.; Jia, Y.; Gealy, D.; Olsen, K.The Pi-ta gene in rice has been effectively used to control rice blast disease caused by Magnaporthe oryzae worldwide. Despite a number of studies that reported the Pi-ta gene in domesticated rice and wild species, little is known about how the Pi-ta gene has evolved in US weedy rice, a major weed of rice. To investigate the genome organization of the Pi-ta gene in weedy rice and its relationship to gene flow between cultivated and weedy rice in the US, we analyzed nucleotide sequence variation at the Pi-ta gene and its surrounding 2 Mb region in 156 weedy, domesticated and wild rice relatives. We found that the region at and around the Pi-ta gene shows very low genetic diversity in US weedy rice. The patterns of molecular diversity in weeds are more similar to cultivated rice (indica and aus), which have never been cultivated in the US, rather than the wild rice species, Oryza rufipogon. In addition, the resistant Pi-ta allele (Pi-ta) found in the majority of US weedy rice belongs to the weedy group strawhull awnless (SH), suggesting a single source of origin for Pi-ta. Weeds with Pi-ta were resistant to two M. oryzae races, IC17 and IB49, except for three accessions, suggesting that component(s) required for the Pi-ta mediated resistance may be missing in these accessions. Signatures of flanking sequences of the Pi-ta gene and SSR markers on chromosome 12 suggest that the susceptible pi-ta allele (pi-ta), not Pi-ta, has been introgressed from cultivated to weedy rice by out-crossing.Publication Genomic patterns of nucleotide diversity in divergent populations of U.S. weedy rice(2010-06-15) Reagon, Michael; Thurber, Carrie; Gross, Brian; Olsen, Kenneth; Jia, Yulin; Caicedo, AnaBackground: Weedy rice (red rice), a conspecific weed of cultivated rice (Oryza sativa L.), is a significant problem throughout the world and an emerging threat in regions where it was previously absent. Despite belonging to the same species complex as domesticated rice and its wild relatives, the evolutionary origins of weedy rice remain unclear. We use genome-wide patterns of single nucleotide polymorphism (SNP) variation in a broad geographic sample of weedy, domesticated, and wild Oryza samples to infer the origin and demographic processes influencing U.S. weedy rice evolution. Results: We find greater population structure than has been previously reported for U.S. weedy rice, and that the multiple, genetically divergent populations have separate origins. The two main U.S. weedy rice populations share genetic backgrounds with cultivated O. sativa varietal groups not grown commercially in the U.S., suggesting weed origins from domesticated ancestors. Hybridization between weedy groups and between weedy rice and local crops has also led to the evolution of distinct U.S. weedy rice populations. Demographic simulations indicate differences among the main weedy groups in the impact of bottlenecks on their establishment in the U.S., and in the timing of divergence from their cultivated relatives. Conclusions: Unlike prior research, we did not find unambiguous evidence for U.S. weedy rice originating via hybridization between cultivated and wild Oryza species. Our results demonstrate the potential for weedy life-histories to evolve directly from within domesticated lineages. The diverse origins of U.S. weedy rice populations demonstrate the multiplicity of evolutionary forces that can influence the emergence of weeds from a single species complex.Publication Evidence of fruit syndromes in the recently diverged wild tomato clade opens new possibilities for the study of fleshy fruit evolution(2023-01-01) Barnett, Jacob R.; Sharma, Rovin; Buonauro, Gina; Gillis, Ian M.; Rashidzade, Maryam; Caicedo, Ana L.Societal Impact Statement Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits. Summary Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine-grained scale with a group of recently diverged species while controlling for environmental effects. We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden-based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (Solanum sect. Lycopersicon). We laid the groundwork for further testing of potential evolutionary drivers by assessing patterns of clustering and correlation among disperser-relevant fruit traits as well as historical climate variables. We found evidence of two distinct clusters of associated fruit traits defined by color, sugar type, and malic acid concentration. We also observed correlations between a fruit's external appearance and internal nutrient content that could function as honest signals to dispersers. Analyses of historical climate and soil variables revealed an association between red/orange/yellow fruits and high annual average temperature. Our results establish the tomato clade as a promising system for testing hypotheses on the drivers of divergence behind early-stage fleshy fruit evolution, particularly selective pressure from frugivores.Publication Genomic Evidence for Complex Domestication History of the Cultivated Tomato in Latin America(2020-01-01) Razifard, Hamid; Ramos, Alexis; Della Valle, Audrey L.; Bodary, Cooper; Goetz, Erika; Manser, Elizabeth J.; Li, Xiang; Visa, Sofia; Tieman, Denise; van der Knaap, Esther; Caicedo, Ana L.The process of plant domestication is often protracted, involving underexplored intermediate stages with important implications for the evolutionary trajectories of domestication traits. Previously, tomato domestication history has been thought to involve two major transitions: one from wild Solanum pimpinellifolium L. to a semidomesticated intermediate, S. lycopersicum L. var. cerasiforme (SLC) in South America, and a second transition from SLC to fully domesticated S. lycopersicum L. var. lycopersicum in Mesoamerica. In this study, we employ population genomic methods to reconstruct tomato domestication history, focusing on the evolutionary changes occurring in the intermediate stages. Our results suggest that the origin of SLC may predate domestication, and that many traits considered typical of cultivated tomatoes arose in South American SLC, but were lost or diminished once these partially domesticated forms spread northward. These traits were then likely reselected in a convergent fashion in the common cultivated tomato, prior to its expansion around the world. Based on these findings, we reveal complexities in the intermediate stage of tomato domestication and provide insight on trajectories of genes and phenotypes involved in tomato domestication syndrome. Our results also allow us to identify underexplored germplasm that harbors useful alleles for crop improvement.Publication Timing is everything: early degradation of abscission layer is associated with increased seed shattering in U.S. weedy rice(2011-01-01) Caicedo, Ana; Thurber, C.; Helper, P.Background Seed shattering, or shedding, is an important fitness trait for wild and weedy grasses. U.S. weedy rice (Oryza sativa) is a highly shattering weed, thought to have evolved from non-shattering cultivated ancestors. All U.S. weedy rice individuals examined to date contain a mutation in the sh4 locus associated with loss of shattering during rice domestication. Weedy individuals also share the shattering trait with wild rice, but not the ancestral shattering mutation at sh4; thus, how weedy rice reacquired the shattering phenotype is unknown. To establish the morphological basis of the parallel evolution of seed shattering in weedy rice and wild, we examined the abscission layer at the flower-pedicel junction in weedy individuals in comparison with wild and cultivated relatives. Results Consistent with previous work, shattering wild rice individuals possess clear, defined abscission layers at flowering, whereas non-shattering cultivated rice individuals do not. Shattering weedy rice from two separately evolved populations in the U.S. (SH and BHA) show patterns of abscission layer formation and degradation distinct from wild rice. Prior to flowering, the abscission layer has formed in all weedy individuals and by flowering it is already degrading. In contrast, wild O. rufipogon abscission layers have been shown not to degrade until after flowering has occurred. Conclusions Seed shattering in weedy rice involves the formation and degradation of an abscission layer in the flower-pedicel junction, as in wild Oryza, but is a developmentally different process from shattering in wild rice. Weedy rice abscission layers appear to break down earlier than wild abscission layers. The timing of weedy abscission layer degradation suggests that unidentified regulatory genes may play a critical role in the reacquisition of shattering in weedy rice, and sheds light on the morphological basis of parPublication The Role of Standing Variation in the Evolution of Weedines Traits in South Asian Weedy Rice (Oryza spp.)(2018-01-01) Huang, Zhongyung; Kelly, Shannon; Matsuo, Rika; Li, Lin-Feng; Li, Yaling; Olsen, Kenneth M.; Jia, Yulin; Caicedo, Ana L.Weedy rice (Oryza spp.) is a problematic weed of cultivated rice (O. sativa) around the world. Recent studies have established multiple independent evolutionary origins of weedy rice, raising questions about the traits and genes that are essential for the evolution of this weed. Among world regions, South Asia stands out due to the heterogeneity of its weedy rice populations, which can be traced to at least three origins: two through de-domestication from distinct cultivated rice varieties, and one from local wild rice (O. rufipogon/O. nivara). Here we examine five traits considered typical of or advantageous to weedy rice in weedy, cultivated and wild rice samples from South Asia. We establish that convergence among all three weed groups occurs for easy seed shattering, red pericarp color, and compact plant architecture, suggesting that these traits are essential for weed success in the South Asian agricultural environment. A high degree of convergence for black hull color is also seen among weeds with wild ancestors and weeds evolved from the aus cultivated rice group. We also examine polymorphism in five known domestication candidate genes, and find that Rc and Bh4 are associated with weed seed pericarp color and hull color, respectively, and weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy-linked gene Sdr4. The presence of a domestication related allele at the seed shattering locus, sh4, in weedy rice populations with cultivated ancestry supports a de-domestication origin for these weedy groups, and raises questions about the reacquisition of the shattering trait in these weedy populations. Our characterization of weedy rice phenotypes in South Asia and their associated candidate genes contribute to the emerging understanding of the mechanisms by which weedy rice evolves worldwide, suggesting that standing ancestral variation is often the source of weedy traits in independently evolved groups, and highlighting the reservoir of genetic variation that is present in cultivated varieties as well as in wild rice, and its potential for phenotypic evolution.Publication Genome-Wide Patterns of Nucleotide Polymorphism in Domesticated Rice(2007-01-01) Caicedo, Ana; Williamson, S.; Hernandez, R,; Boyko, A.; Fleded-Alon, A.; York, T.; Polato, N.; Olsen, K.; Nielsen, R.; McCouch, S.; Bustamante, C.; Purugganan, M.Domesticated Asian rice (Oryza sativa) is one of the oldest domesticated crop species in the world, having fed more people than any other plant in human history. We report the patterns of DNA sequence variation in rice and its wild ancestor, O. rufipogon, across 111 randomly chosen gene fragments, and use these to infer the evolutionary dynamics that led to the origins of rice. There is a genome-wide excess of high-frequency derived single nucleotide polymorphisms (SNPs) in O. sativa varieties, a pattern that has not been reported for other crop species. We developed several alternative models to explain contemporary patterns of polymorphisms in rice, including a (i) selectively neutral population bottleneck model, (ii) bottleneck plus migration model, (iii) multiple selective sweeps model, and (iv) bottleneck plus selective sweeps model. We find that a simple bottleneck model, which has been the dominant demographic model for domesticated species, cannot explain the derived nucleotide polymorphism site frequency spectrum in rice. Instead, a bottleneck model that incorporates selective sweeps, or a more complex demographic model that includes subdivision and gene flow, are more plausible explanations for patterns of variation in domesticated rice varieties. If selective sweeps are indeed the explanation for the observed nucleotide data of domesticated rice, it suggests that strong selection can leave its imprint on genome-wide polymorphism patterns, contrary to expectations that selection results only in a local signature of variation.