J. Chris Pires | University of Missouri Columbia (original) (raw)
Papers by J. Chris Pires
G3 Genes|Genomes|Genetics, 2020
Homoeologous recombination, aneuploidy, and other genetic changes are common in resynthesized all... more Homoeologous recombination, aneuploidy, and other genetic changes are common in resynthesized allopolyploid Brassica napus. In contrast, the chromosomes of cultivars have long been considered to be meiotically stable. To gain a better understanding of the underlying mechanisms leading to stabilization in the allopolyploid, the behavior of chromosomes during meiosis can be compared by unambiguous chromosome identification between resynthesized and natural B. napus. Compared with natural B. napus, resynthesized lines show high rates of nonhomologous centromere association, homoeologous recombination leading to translocation, homoeologous chromosome replacement, and association and breakage of 45S rDNA loci. In both natural and resynthesized B. napus, we observed low rates of univalents, A–C bivalents, and early sister chromatid separations. Reciprocal homoeologous chromosome exchanges and double reductions were photographed for the first time in meiotic telophase I. Meiotic errors wer...
G3 Genes|Genomes|Genetics, 2021
Genome sizes of plants have long piqued the interest of researchers due to the vast differences a... more Genome sizes of plants have long piqued the interest of researchers due to the vast differences among organisms. However, the mechanisms that drive size differences have yet to be fully understood. Two important contributing factors to genome size are expansions of repetitive elements, such as transposable elements (TEs), and whole-genome duplications (WGD). Although studies have found correlations between genome size and both TE abundance and polyploidy, these studies typically test for these patterns within a genus or species. The plant order Brassicales provides an excellent system to further test if genome size evolution patterns are consistent across larger time scales, as there are numerous WGDs. This order is also home to one of the smallest plant genomes, Arabidopsis thaliana—chosen as the model plant system for this reason—as well as to species with very large genomes. With new methods that allow for TE characterization from low-coverage genome shotgun data and 71 taxa acro...
The Plant cell, Jan 16, 2017
Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally ... more Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of emergence of subgenome dominance, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized inter-species triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and progenitor species (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are reduced in regions near genes and within TEs in the first-generat...
Annual Review of Genetics, 2016
The complex manner in which organisms respond to changes in their gene dosage has long fascinated... more The complex manner in which organisms respond to changes in their gene dosage has long fascinated geneticists. Oddly, although the existence of dominance implies that dosage reductions often have mild phenotypes, extra copies of whole chromosomes (aneuploidy) are generally strongly deleterious. Even more paradoxically, an extra copy of the genome is better tolerated than is aneuploidy. We review the resolution of this paradox, highlighting the roles of biochemistry, protein aggregation, and disruption of cellular microstructure in that explanation. Returning to life's curious combination of robustness and sensitivity to dosage changes, we argue that understanding how biological robustness evolved makes these observations less inexplicable. We propose that noise in gene expression and evolutionary strategies for its suppression play a role in generating dosage phenotypes. Finally, we outline an unappreciated mechanism for the preservation of duplicate genes, namely preservation t...
Nucleic Acids Research, 2015
Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pa... more Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pathway, C4 photosynthesis, allows some plants to be more drought tolerant and fertilizer-use efficient. Strikingly, C4 photosynthesis has evolved independently in dozens of different plant lineages, a testament to its diversity and advantages in many common terrestrial environments. Currently, massive international efforts are focused on breeding and bioengineering C4 photosynthesis into C3 rice and other food and sustainable energy crops. What these efforts often overlook is that there is no “one” C4 photosynthesis. In fact, with its 60-plus distinct evolutionary origins, 20-plus anatomies, and 3 basic enzymatic sub-types, C4 is more of a diverse syndrome than it is one generalized photosynthesis type. Because the various C4 sub-types have evolved in diverse environments, different sub-types may be more efficient for different agricultural applications. Our study uses the grass tribe Pan...
Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pa... more Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pathway, C4 photosynthesis, allows some plants to be more drought tolerant and fertilizer-use efficient. Strikingly, C4 photosynthesis has evolved independently in dozens of different plant lineages, a testament to its diversity and advantages in many common terrestrial environments. Currently, massive international efforts are focused on breeding and bioengineering C4 photosynthesis into C3 rice and other food and sustainable energy crops. What these efforts often overlook is that there is no “one” C4 photosynthesis. In fact, with its 60-plus distinct evolutionary origins, 20-plus anatomies, and 3 basic enzymatic sub-types, C4 is more of a diverse syndrome than it is one generalized photosynthesis type. Because the various C4 sub-types have evolved in diverse environments, different sub-types may be more efficient for different agricultural applications. Our study uses the grass tribe Pan...
Current opinion in plant biology, 2014
Requirements to maintain dosage balance shape many genome-scale patterns in organisms, including ... more Requirements to maintain dosage balance shape many genome-scale patterns in organisms, including the resolution of whole genome duplications (WGD), as well as the varied effects of aneuploidy, segmental duplications, tandem duplications, gene copy number variations (CNV), and epigenetic marks. Like neofunctionalization and subfunctionalization, the impact of absolute and relative dosage varies over time. These variations are of particular importance in understanding the role of dosage in the evolution of polyploid organisms. Numerous investigations have found the consequences of polyploidy remain distinct from small-scale duplications (SSD). This observation is significant as all flowering plants have experienced at least two ancient polyploid events, and many angiosperm lineages have undergone additional rounds of polyploidy. Intriguingly, recent studies indicate a link between how epigenetic marks in recent allopolyploids may induce immediate changes in gene expression and the lon...
The Plant Cell, 2009
Homoeologous regions of Brassica genomes were analyzed at the sequence level. These represent seg... more Homoeologous regions of Brassica genomes were analyzed at the sequence level. These represent segments of the Brassica A genome as found in Brassica rapa and Brassica napus and the corresponding segments of the Brassica C genome as found in Brassica oleracea and B. napus. Analysis of synonymous base substitution rates within modeled genes revealed a relatively broad range of times (0.12 to 1.37 million years ago) since the divergence of orthologous genome segments as represented in B. napus and the diploid species. Similar, and consistent, ranges were also identified for single nucleotide polymorphism and insertion-deletion variation. Genes conserved across the Brassica genomes and the homoeologous segments of the genome of Arabidopsis thaliana showed almost perfect collinearity. Numerous examples of apparent transduplication of gene fragments, as previously reported in B. oleracea, were observed in B. rapa and B. napus, indicating that this phenomenon is widespread in Brassica spec...
Plant Physiology, 2005
Allopolyploid formation requires the adaptation of two nuclear genomes within a single cytoplasm,... more Allopolyploid formation requires the adaptation of two nuclear genomes within a single cytoplasm, which may involve programmed genetic and epigenetic changes during the initial generations following genome fusion. To study the dynamics of genome change, we synthesized 49 isogenic Brassica napus allopolyploids and surveyed them with 76 restriction fragment length polymorphism (RFLP) probes and 30 simple sequence repeat (SSR) primer pairs. Here, we report on the types and distribution of genetic and epigenetic changes within the S1 genotypes. We found that insertion/deletion (indel) events were rare, but not random. Of the 57,710 (54,383 RFLP and 3,327 SSR) parental fragments expected among the amphidiploids, we observed 56,676 or 99.9%. Three loci derived from Brassica rapa had indels, and one indel occurred repeatedly across 29% (14/49) of the lines. Loss of one parental fragment was due to the 400-bp reduction of a guanine-adenine dinucleotide repeat-rich sequence. In contrast to t...
Molecular Phylogenetics and Evolution, 1999
Genetics, 2010
Investigating recombination of homoeologous chromosomes in allopolyploid species is central to un... more Investigating recombination of homoeologous chromosomes in allopolyploid species is central to understanding plant breeding and evolution. However, examining chromosome pairing in the allotetraploid Brassica napus has been hampered by the lack of chromosome-specific molecular probes. In this study, we establish the identification of all homoeologous chromosomes of allopolyploid B. napus by using robust molecular cytogenetic karyotypes developed for the progenitor species Brassica rapa (A genome) and Brassica oleracea (C genome). The identification of every chromosome among these three Brassica species utilized genetically mapped bacterial artificial chromosomes (BACs) from B. rapa as probes for fluorescent in situ hybridization (FISH). With this BAC-FISH data, a second karyotype was developed using two BACs that contained repetitive DNA sequences and the ubiquitous ribosomal and pericentromere repeats. Using this diagnostic probe mix and a BAC that contained a C-genome repeat in two...
BMC Genomics, 2009
Background The Brassica species, related to Arabidopsis thaliana, include an important group of c... more Background The Brassica species, related to Arabidopsis thaliana, include an important group of crops and represent an excellent system for studying the evolutionary consequences of polyploidy. Previous studies have led to a proposed structure for an ancestral karyotype and models for the evolution of the B. rapa genome by triplication and segmental rearrangement, but these have not been validated at the sequence level. Results We developed computational tools to analyse the public collection of B. rapa BAC end sequence, in order to identify candidates for representing collinearity discontinuities between the genomes of B. rapa and A. thaliana. For each putative discontinuity, one of the BACs was sequenced and analysed for collinearity with the genome of A. thaliana. Additional BAC clones were identified and sequenced as part of ongoing efforts to sequence four chromosomes of B. rapa. Strikingly few of the 19 inter-chromosomal rearrangements corresponded to the set of collinearity d...
Biological Journal of the Linnean Society, 2004
Biological Journal of the Linnean Society, 2004
American Journal of Botany, 2002
G3 Genes|Genomes|Genetics, 2020
Homoeologous recombination, aneuploidy, and other genetic changes are common in resynthesized all... more Homoeologous recombination, aneuploidy, and other genetic changes are common in resynthesized allopolyploid Brassica napus. In contrast, the chromosomes of cultivars have long been considered to be meiotically stable. To gain a better understanding of the underlying mechanisms leading to stabilization in the allopolyploid, the behavior of chromosomes during meiosis can be compared by unambiguous chromosome identification between resynthesized and natural B. napus. Compared with natural B. napus, resynthesized lines show high rates of nonhomologous centromere association, homoeologous recombination leading to translocation, homoeologous chromosome replacement, and association and breakage of 45S rDNA loci. In both natural and resynthesized B. napus, we observed low rates of univalents, A–C bivalents, and early sister chromatid separations. Reciprocal homoeologous chromosome exchanges and double reductions were photographed for the first time in meiotic telophase I. Meiotic errors wer...
G3 Genes|Genomes|Genetics, 2021
Genome sizes of plants have long piqued the interest of researchers due to the vast differences a... more Genome sizes of plants have long piqued the interest of researchers due to the vast differences among organisms. However, the mechanisms that drive size differences have yet to be fully understood. Two important contributing factors to genome size are expansions of repetitive elements, such as transposable elements (TEs), and whole-genome duplications (WGD). Although studies have found correlations between genome size and both TE abundance and polyploidy, these studies typically test for these patterns within a genus or species. The plant order Brassicales provides an excellent system to further test if genome size evolution patterns are consistent across larger time scales, as there are numerous WGDs. This order is also home to one of the smallest plant genomes, Arabidopsis thaliana—chosen as the model plant system for this reason—as well as to species with very large genomes. With new methods that allow for TE characterization from low-coverage genome shotgun data and 71 taxa acro...
The Plant cell, Jan 16, 2017
Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally ... more Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of emergence of subgenome dominance, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized inter-species triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and progenitor species (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are reduced in regions near genes and within TEs in the first-generat...
Annual Review of Genetics, 2016
The complex manner in which organisms respond to changes in their gene dosage has long fascinated... more The complex manner in which organisms respond to changes in their gene dosage has long fascinated geneticists. Oddly, although the existence of dominance implies that dosage reductions often have mild phenotypes, extra copies of whole chromosomes (aneuploidy) are generally strongly deleterious. Even more paradoxically, an extra copy of the genome is better tolerated than is aneuploidy. We review the resolution of this paradox, highlighting the roles of biochemistry, protein aggregation, and disruption of cellular microstructure in that explanation. Returning to life's curious combination of robustness and sensitivity to dosage changes, we argue that understanding how biological robustness evolved makes these observations less inexplicable. We propose that noise in gene expression and evolutionary strategies for its suppression play a role in generating dosage phenotypes. Finally, we outline an unappreciated mechanism for the preservation of duplicate genes, namely preservation t...
Nucleic Acids Research, 2015
Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pa... more Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pathway, C4 photosynthesis, allows some plants to be more drought tolerant and fertilizer-use efficient. Strikingly, C4 photosynthesis has evolved independently in dozens of different plant lineages, a testament to its diversity and advantages in many common terrestrial environments. Currently, massive international efforts are focused on breeding and bioengineering C4 photosynthesis into C3 rice and other food and sustainable energy crops. What these efforts often overlook is that there is no “one” C4 photosynthesis. In fact, with its 60-plus distinct evolutionary origins, 20-plus anatomies, and 3 basic enzymatic sub-types, C4 is more of a diverse syndrome than it is one generalized photosynthesis type. Because the various C4 sub-types have evolved in diverse environments, different sub-types may be more efficient for different agricultural applications. Our study uses the grass tribe Pan...
Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pa... more Most plants convert sunlight into chemical energy using C3 photosynthesis. However, a modified pathway, C4 photosynthesis, allows some plants to be more drought tolerant and fertilizer-use efficient. Strikingly, C4 photosynthesis has evolved independently in dozens of different plant lineages, a testament to its diversity and advantages in many common terrestrial environments. Currently, massive international efforts are focused on breeding and bioengineering C4 photosynthesis into C3 rice and other food and sustainable energy crops. What these efforts often overlook is that there is no “one” C4 photosynthesis. In fact, with its 60-plus distinct evolutionary origins, 20-plus anatomies, and 3 basic enzymatic sub-types, C4 is more of a diverse syndrome than it is one generalized photosynthesis type. Because the various C4 sub-types have evolved in diverse environments, different sub-types may be more efficient for different agricultural applications. Our study uses the grass tribe Pan...
Current opinion in plant biology, 2014
Requirements to maintain dosage balance shape many genome-scale patterns in organisms, including ... more Requirements to maintain dosage balance shape many genome-scale patterns in organisms, including the resolution of whole genome duplications (WGD), as well as the varied effects of aneuploidy, segmental duplications, tandem duplications, gene copy number variations (CNV), and epigenetic marks. Like neofunctionalization and subfunctionalization, the impact of absolute and relative dosage varies over time. These variations are of particular importance in understanding the role of dosage in the evolution of polyploid organisms. Numerous investigations have found the consequences of polyploidy remain distinct from small-scale duplications (SSD). This observation is significant as all flowering plants have experienced at least two ancient polyploid events, and many angiosperm lineages have undergone additional rounds of polyploidy. Intriguingly, recent studies indicate a link between how epigenetic marks in recent allopolyploids may induce immediate changes in gene expression and the lon...
The Plant Cell, 2009
Homoeologous regions of Brassica genomes were analyzed at the sequence level. These represent seg... more Homoeologous regions of Brassica genomes were analyzed at the sequence level. These represent segments of the Brassica A genome as found in Brassica rapa and Brassica napus and the corresponding segments of the Brassica C genome as found in Brassica oleracea and B. napus. Analysis of synonymous base substitution rates within modeled genes revealed a relatively broad range of times (0.12 to 1.37 million years ago) since the divergence of orthologous genome segments as represented in B. napus and the diploid species. Similar, and consistent, ranges were also identified for single nucleotide polymorphism and insertion-deletion variation. Genes conserved across the Brassica genomes and the homoeologous segments of the genome of Arabidopsis thaliana showed almost perfect collinearity. Numerous examples of apparent transduplication of gene fragments, as previously reported in B. oleracea, were observed in B. rapa and B. napus, indicating that this phenomenon is widespread in Brassica spec...
Plant Physiology, 2005
Allopolyploid formation requires the adaptation of two nuclear genomes within a single cytoplasm,... more Allopolyploid formation requires the adaptation of two nuclear genomes within a single cytoplasm, which may involve programmed genetic and epigenetic changes during the initial generations following genome fusion. To study the dynamics of genome change, we synthesized 49 isogenic Brassica napus allopolyploids and surveyed them with 76 restriction fragment length polymorphism (RFLP) probes and 30 simple sequence repeat (SSR) primer pairs. Here, we report on the types and distribution of genetic and epigenetic changes within the S1 genotypes. We found that insertion/deletion (indel) events were rare, but not random. Of the 57,710 (54,383 RFLP and 3,327 SSR) parental fragments expected among the amphidiploids, we observed 56,676 or 99.9%. Three loci derived from Brassica rapa had indels, and one indel occurred repeatedly across 29% (14/49) of the lines. Loss of one parental fragment was due to the 400-bp reduction of a guanine-adenine dinucleotide repeat-rich sequence. In contrast to t...
Molecular Phylogenetics and Evolution, 1999
Genetics, 2010
Investigating recombination of homoeologous chromosomes in allopolyploid species is central to un... more Investigating recombination of homoeologous chromosomes in allopolyploid species is central to understanding plant breeding and evolution. However, examining chromosome pairing in the allotetraploid Brassica napus has been hampered by the lack of chromosome-specific molecular probes. In this study, we establish the identification of all homoeologous chromosomes of allopolyploid B. napus by using robust molecular cytogenetic karyotypes developed for the progenitor species Brassica rapa (A genome) and Brassica oleracea (C genome). The identification of every chromosome among these three Brassica species utilized genetically mapped bacterial artificial chromosomes (BACs) from B. rapa as probes for fluorescent in situ hybridization (FISH). With this BAC-FISH data, a second karyotype was developed using two BACs that contained repetitive DNA sequences and the ubiquitous ribosomal and pericentromere repeats. Using this diagnostic probe mix and a BAC that contained a C-genome repeat in two...
BMC Genomics, 2009
Background The Brassica species, related to Arabidopsis thaliana, include an important group of c... more Background The Brassica species, related to Arabidopsis thaliana, include an important group of crops and represent an excellent system for studying the evolutionary consequences of polyploidy. Previous studies have led to a proposed structure for an ancestral karyotype and models for the evolution of the B. rapa genome by triplication and segmental rearrangement, but these have not been validated at the sequence level. Results We developed computational tools to analyse the public collection of B. rapa BAC end sequence, in order to identify candidates for representing collinearity discontinuities between the genomes of B. rapa and A. thaliana. For each putative discontinuity, one of the BACs was sequenced and analysed for collinearity with the genome of A. thaliana. Additional BAC clones were identified and sequenced as part of ongoing efforts to sequence four chromosomes of B. rapa. Strikingly few of the 19 inter-chromosomal rearrangements corresponded to the set of collinearity d...
Biological Journal of the Linnean Society, 2004
Biological Journal of the Linnean Society, 2004
American Journal of Botany, 2002