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Laboratory of Keith Adams

Gossypium tomentosum

Research Description

My research interests intersect between molecular genetics and evolutionary biology. My lab's research is in the areas of molecular evolution, genome evolution, and gene expression. We study how gene structures, expression patterns, alternative splicing, regulation, and function evolve. We use molecular techniques and bioinformatics analyses of large data sets to test hypotheses and answer questions. Some of the major questions that we study include: How do duplicated genes change in expression patterns, alternative splicing patterns, and functions at different evolutionary time scales? How does gene expression and alternative splicing change upon polyploidy and interspecific hybridization, as well as over evolutionary time in a polyploid plant? How does duplicate gene expression vary by organ type and developmental stage and what impacts does that have on gene retention and function? How is duplicate gene expression affected by environmental stress conditions? How do duplicate gene sequences and structures evolve?

Expression, silencing, and alternative splicing of duplicated genes in polyploids

Most eukaryotes have a large number of duplicated genes, many of which appear to have arisen from one or more cycles of genome doubling. Polyploidy has been especially common in flowering plants, with most plants being ancient polyploids that have become diploids, followed by recent rounds of polyploidy in many plant species. Allopolyploidy is a prominent mode of speciation in angiosperms. Polyploids can display novel phenotypes leading to morphological evolution. Polyploidy is a dynamic process at the gene level that is associated with considerable and rapid genomic reorganization in some plants and changes in gene expression including gene silencing.

We are studying the consequences of polyploidy on expression, silencing, and alternative splicing of duplicate genes, using polyploid cotton and canola as study systems. We determined that silencing of duplicated genes can be organ-specific and developmentally regulated, and that expression levels between the two copies can vary widely by organ type and developmental stage (Adams et al. 2003; Liu and Adams 2007). Expression of the two duplicates can be partitioned between different organs (i.e., one copy is silenced in some organs and the other copy is silenced in other organs). Such reciprocal silencing of duplicated genes is indicative of subfunctionalization and suggests that both duplicates will be retained. We have been studying the effects of environmental stress conditions on expression of genes duplicated by polyploidy. We discovered that expression of a duplicated gene pair can vary extensively in response to various abiotic stresses and that reciprocal silencing of duplicated genes can occur in response to two different stresses, indicating subfunctionalization in response to stress (Liu and Adams 2007). Changes in expression patterns of duplicated genes appear to be a common occurrence in a polyploid in response to different abiotic stresses (Dong and Adams, in preparation). In addition we have been studying alternative splicing patterns of duplicated genes in a polyploid (canola) to examine the effects of gene duplication on alternative splicing, using multiple organs and abiotic stress conditions. Several gene pairs show different alternative splicing patterns in one duplicate, including cases where only one of the two duplicated copies is alternatively spliced. Loss or gain of alternatively spliced forms appears to be more common after polyploidy than gene silencing. Changes in alternative splicing after gene duplication may have effects on duplicate gene function.

Effects of interspecific hybridization on gene expression and alternative splicing

It has become apparent from recent studies of allopolyploids that hybridization between two species has a greater effect than chromosome doubling on gene expression. Thus we have been studying the effects of interspecific hybridization on allelic expression and alternative splicing patterns. We examined allelic expression patterns of a set of genes in interspecific F1 hybrids of Populus trichocarpa × P. deltoides. A large majority of the genes showed unequal allelic expression, some of which appears to be caused by inter-species hybridization (Zhuang and Adams 2007). In another project we examined alternative splicing patterns in a set of 40 genes in the Populus hybrids compared with their parents (Scascitelli et al. 2010). Two genes for splicing factors showed novel splice forms in the hybrids. Our results suggest that novel alternative splicing patterns are present in a small percentage of genes in hybrids, but they could make a considerable impact on the expression of some genes. Changes in alternative splicing are likely to be an important component of the genetic changes that occur upon interspecific hybridization.

Evolution of expression, alternative splicing, and function of genes duplicated by ancient polyploidy events

To examine the long-term evolutionary effects of whole genome duplication on gene expression we studied genes duplicated by an ancient polyploidy event (approximately 23 million years ago) during the evolutionary history of the Brassicaceae family (includes Arabidopsis and Brassica). We found that the duplicated genes show extensive divergence in alternative splicing patterns including organ and abiotic stress-specific differences (Zhang et al. 2010). Some of the diverged alternative splicing events result in loss or disruption of functional domains that would affect protein function if the transcripts are translated, potentially resulting in functional divergence between the duplicates. Alternative splicing divergence between duplicated genes may have contributed to gene functional evolution and led to preservation of some duplicated genes. In addition we have been analyzing expression patterns of the duplicated genes using microarray data sets including a large developmental data set and an abiotic stress data set. Those analyses indicate that one duplicate in a pair often becomes expressed in a new organ type, suggesting neofunctionalization, and that expression of many of the duplicated genes in response to abiotic stress conditions has diverged between the gene pairs.

We have characterized a dramatic case of neofunctionalization after the ancient polyploidy event in the Brassicaceae involving the change in function of a duplicated gene from being involved in brassinosteroid signal transduction to regulating zygote elongation after fertilization (Liu and Adams, submitted). The gene shows accelerated sequence evolution, it lost its original function by deletions in a functional domain, and its expression pattern is completely different from its duplicate.

Other research areas

Another line of research in the lab is a study of gene regulation in native vs. invasive populations of Canada thistle. Genes whose expression is up or down regulated in the native vs. invasive populations are being studied to infer the mode of regulation, cis or trans that is responsible. Cis regulation would indicate that direct selective pressure favored change in a linked regulatory sequence, whereas trans regulation would indicate that is a gene is affected indirectly as a consequence of being downstream from the true target of selection in a common pathway or by being regulated by the gene product that was selected for. We have done genome-wide transcriptome profiling using Illumina RNA-seq, and data analysis is ongoing. This project is part of a larger collaborative project with Loren Rieseberg, Sally Otto, and Jeannette Whitton.

Transfers of mitochondrial genes to the nucleus: The transfer of mitochondrial genes to the nucleus is a duplicative process because the transferred nuclear copy must become functional before the organellar copy is deleted. A small number of cases exist where a gene for the same organellar protein is present and expressed in both the organelle and nucleus representing a special type (trans-compartmental) of gene duplication, for example in Choi et al. (2006). We performed comparative analyses of gene structures and sequence evolution of 77 genes transferred to the nucleus in various angiosperms to reveal the frequency and origins of numerous chimeric transferred genes and to analyze sequence evolution of the transferred genes (Liu et al. 2009). Also we have studied sequence and expression evolution in organellar rps13 genes in which the product of a duplicated nuclear gene is targeted to mitochondria (Liu and Adams, 2008). We are not currently pursuing projects on this topic.

Selected publications

Liu S-L, Adams KL
Complete change in function and expression pattern of a gene duplicated by polyploidy created a paternal effect gene in the Brassicaceae.
submitted, 2010.

Scascitelli M, Cognet M, Adams KL
An interspecific plant hybrid shows novel changes in parental alternative splice forms of genes for splicing factors
GENETICS in press, accepted manuscript available on the journal's website, 2010

Zhang PG, Huang S, Pin A-L, Adams KL
Extensive divergence in alternative splicing patterns after gene and genome duplication during the evolutionary history of Arabidopsis
MOLECULAR BIOLOGY AND EVOLUTION in press, accepted manuscript available on the journal's website, 2010

Liu S-L*, Zhuang Y*, Zhang P, Adams KL
Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus
MOLECULAR BIOLOGY AND EVOLUTION 26: 875-891. 2009
*equal contributions

Liu S-L, Adams KL
Molecular adaptation and expression evolution following duplication of genes for organellar ribosomal protein S13 in rosids. BMC EVOLUTIONARY BIOLOGY 8: 25 (15 pages). 2008

Adams KL
Insights into the evolution of duplicated gene expression in polyploids from Gossypium
BOTANY 86: 827-834. 2008

Liu Z, Adams KL
Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development
CURRENT BIOLOGY 17: 1669-1674. 2007

Dispatches article about the paper: Hegarty, M., and Hiscock, S. Polyploidy: Doubling up for evolutionary success
CURRENT BIOLOGY 17: R927-929.

Adams KL
Evolution of duplicate gene expression in polyploid and hybrid plants
JOURNAL OF HEREDITY 98: 136-141. 2007

Zhuang Y, Adams KL
Extensive allelic variation in gene expression in Populus F1 hybrids
GENETICS 177: 1987-1996. 2007

Choi C, Liu Z, Adams KL
Evolutionary transfers of mitochondrial genes to the nucleus in the Populus lineage and co-expression of nuclear and mitochondrial Sdh4 genes
NEW PHYTOLOGIST 172: 429-439. 2006

Article highlighting the paper: Bonen L. 2006. Mitochondrial genes leave home.
NEW PHYTOLOGIST 172: 379-381. 2006

Adams KL, Wendel JF
Polyploidy and genome evolution in plants
CURRENT OPINION IN PLANT BIOLOGY 8: 135-141. 2005

Adams KL, Wendel JF
Allele-specific, bi-directional silencing of an alcohol dehydrogenase gene in different organs of interspecific diploid cotton hybrids
GENETICS 171: 2139-2142. 2005

Adams KL, Wendel JF
Novel patterns of gene expression in polyploid plants
TRENDS IN GENETICS 21: 539-543. 2005

Adams KL, Percifield R, Wendel JF
Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid
GENETICS 168: 2217-2226. 2004

Adams KL, Cronn R, Percifield R, Wendel JF
Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing.
PROC NATL ACAD SCI USA 100 (8): 4649-54 APR 15 2003, Epub 2003 Mar 28.

Bergthorsson U, Adams KL, Thomason B, Palmer JD
Widespread horizontal transfer of mitochondrial genes in flowering plants
NATURE 424: 197-201. 2003.

Adams KL, Qiu YL, Stoutemyer M, Palmer JD
Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution.
PROC NATL ACAD SCI USA 99 (15): 9905-12 JUL 23 2002, Epub 2002 Jul 15.

Adams KL, Daley DO, Qiu YL, Whelan J, Palmer JD
Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants.
NATURE 408 (6810): 354-7 2000 Nov 16.

Additional papers that I published during 1998 - 2005 can be found by doing a PubMed search.

Research Team

Teaching

Genome Evolution (BIOL 430)
Plant Genomics (BIOL/ABPI 440)
Topics in Systematics and Evolution: Topics in Molecular Evolution (BIOL 525c)