Research Interests:
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, regulation, alternative splicing, and functions evolve. We use molecular techniques and bioinformatics analyses of large sequence and expression data sets (Illumina and 454) to test hypotheses and answer questions. Some of the major questions that we study include: How do duplicated genes change in expression patterns and alternative splicing patterns? How do duplicated genes change in functions and in subcellular localizations? How does gene expression and alternative splicing change upon interspecific hybridization and allopolyploidy, 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?  To answer those questions we have been studying polyploid Brassica napus (canola) and cotton, Arabidopsis thaliana for questions about the longer-term fates of duplicated genes, and hybrids of cottonwood (Populus) and Canada thistle for questions about hybridization.

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 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 (lack of expression of one duplicate that was expressed in the diploid parents).

We are studying the consequences of polyploidy on expression and alternative splicing of duplicate genes, using polyploid canola and cotton 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 regulatory 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; Dong and Adams 2011).

In addition we have been studying alternative splicing patterns of duplicated genes in polyploid Brassica napus, using both resynthesized and natural lines, to examine the effects of polyploidy on alternative splicing. Many gene pairs show different alternative splicing patterns in the polyploid, including cases where only one of the two duplicated copies is alternatively spliced, with a few gene pairs showing variation that was organ specific or induced by abiotic stress treatments (Zhou et al. 2011). In the resynthesized allotetraploids, 26–30% of the duplicated genes showed changes in AS compared with the parents, including many cases of AS event loss after polyploidy. Parallel losses of many AS events after allopolyploidy were detected in the two independently resynthesized lines.  More changes occurred in parallel between the two lines than changes specific to each line.  Loss or gain of alternatively spliced forms appears to be more common after polyploidy than gene silencing. Our findings indicate that AS patterns can change rapidly after polyploidy, that many genes are affected, and that AS changes are an important component of the transcriptome shock experienced by new allopolyploids.  We are currently expanding our analysis of alternative splicing patterns in polyploids to a genome-wide scale using RNA-seq.

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 x 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. We are currently exploring this phenomenon on a genome-wide scale.

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

To examine the long-term evolutionary effects of whole genome duplication on gene expression we are studying genes duplicated by an ancient polyploidy event during the evolutionary history of the Brassicaceae family (includes Arabidopsis and Brassica). We have characterized a dramatic case of neofunctionalization after the ancient polyploidy event in the Brassicaceae. The Short Suspensor (SSP) gene changed in function after duplication from being involved in brassinosteroid signal transduction to regulating zygote elongation after fertilization by an intriguing paternal effect mechanism (Liu and Adams, 2010). 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 with expression only in pollen. In addition the SSP gene has been tandemly duplicated, translocated, and the new gene gained a new expression pattern and function.  We have identified other cases of neofunctionalization of duplicated genes and we are further characterizing them.

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 large developmental and cell type data sets. Those analyses indicate that one duplicate in a pair often becomes expressed in a new organ type, suggesting neofunctionalization, and that regulatory neofunctionalization is more common than regulatory subfunctionalization (Liu and Adams 2011).  Those analyses showed that pollen is the most common organ type for expression gain.

Other research areas

Research Team:
Aude Darracq – postdoc
Alex Hammel – graduate student
Shao-Lun (Allen) Liu – postdoc
Yichun Qiu - graduate student
David Tack – graduate student 
Yii Van Tay – graduate student

Zhou R, Moshgabadi N, and Adams KL. 2011. Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids. PNAS, 108: 16122-16127.

Liu S-L, Baute G, and Adams KL.  2011. Organ and cell type-specific complementary expression patterns and regulatory neofunctionalization between duplicated genes in Arabidopsis thaliana. Genome Biology and Evolution,  3: 1419-1436.

Dong S, and Adams KL. 2011. Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytologist, 190: 1045–1057.

Liu S-L, and Adams KL. 2010. Dramatic change in function and expression pattern of a gene duplicated by polyploidy created a paternal effect gene in the Brassicaceae. Molecular Biology and Evolution, 27: 2817–2828.

Scascitelli M, Cognet M, and Adams KL. 2010. An interspecific plant hybrid shows novel changes in parental alternative splice forms of genes for splicing factors. Genetics, 184: 975-983. Featured in Issue Highlights at the time of publication.

Zhang PG, Huang S, Pin A-L, and Adams KL. 2010. Extensive divergence in alternative splicing patterns after gene and genome duplication during the evolutionary history of Arabidopsis. Molecular Biology and Evolution, 27: 1686-1697.

Liu S-L, Zhuang Y, Zhang P, and Adams KL. 2009. Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus. Molecular Biology and Evolution, 26: 875-891.

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

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

Liu Z and Adams KL 2007. Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Current Biology 17: 1669-1674. Dispatches feature article about the paper: Hegarty, M., and Hiscock, S. Polyploidy: Doubling up for evolutionary success. Current Biology, 17: R927-929.

Adams KL 2007. Evolution of duplicate gene expression in polyploid and hybrid plants. Journal of Heredity, 98: 136-141.

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

Choi C, Liu Z, and Adams KL 2006. 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. Feature article about the paper: Bonen L. 2006. Mitochondrial genes leave home. New Phytologist 172: 379-381.

Adams KL and Wendel JF. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135-141.

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

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

Adams KL, Cronn R, Percifield R, and Wendel JF. 2003. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 100: 4649-4654.

Adams KL, Qiu Y-L, Stoutemyer M, and Palmer, JD. 2002. 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: 9905-9912.

Adams KL, Daley DO, Qiu YL, Whelan J, and Palmer JD. 2000. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 408: 354-357.

Additional papers that I published since 1998 can be found by doing a PubMed search at http://www.ncbi.nlm.nih.gov/sites/entrez