Study shows how plants sort and eliminate genes over millennia
WEST LAFAYETTE, Ind. - Hybrid plants with multiple genome copies show evidence of preferential treatment of the genes from one ancient parent over the genes of the other parent, even to the point where some of the unfavored genes eventually are deleted.
Brian Dilkes, an assistant professor of genetics at Purdue University, worked with a team of scientists at the University of California Davis and University of Southern California to study the genome of Arabidopsis suecica, a hybrid species with four chromosome sets formed tens of thousands of years ago from a cross between Arabidopsis arenosa and Arabidopsis thaliana, a plant commonly used in laboratories for genetic research. Dilkes said the findings, published in the journal Genome Biology and featured as an editor's choice article in the journal Science, give a glimpse into the evolutionary forces and ultimate fates of genes contributed by the two parents to a hybrid
"There often is no visible signature of these genes when we look at the plants with a microscope, but we can still observe those genes in the genome sequence," Dilkes said. "Moreover, the ability to make crosses between Arabidopsis thaliana and Arabidopsis arenosa gives us the opportunity to compare laboratory-derived plants that were generated yesterday with naturally occurring species from the wild and compare the two kinds of species hybrids. This is essentially allowing us an opportunity to 'replay the evolutionary tape,' in the words of Stephen J. Gould."
The researchers compared the genomes and gene expression among Arabidopsis suecica plants that have evolved over tens of thousands of years to similar species of hybrids made in the lab from fresh crosses.
When the contribution of genes from each parent was compared, they were not equal. One parent's genes were preferentially expressed at higher levels. In the cases where that happened, it was three times more likely that the preferentially expressed genes came from Arabidopsis arenosa.
The team also found that gene pairs that are co-expressed in similar tissues are preferentially expressed from the same parent. Even in the rare cases when an Arabidopsis thaliana gene was more abundantly expressed in the hybrid, co-expressed genes would also be preferentially expressed from the Arabidopsis thaliana copy.
"Our findings suggest an additional network dependence, where genes fine-tuned to work together within either parental species prior to hybridization are more likely to be expressed together in the hybrid. This, in turn, ensures that these genes acquired from one parental species are kept together and are not lost in the genome over time," said Peter Chang, a graduate student at USC and lead author on the paper. "Plants have had a remarkable ability to adapt to different conditions throughout Earth's history, and we are just beginning to understand some of ways this is done."
Previous work has shown that plant genomes with historical duplications from tens of millions of years ago have lost one of the two copies in large blocks along the chromosome, consistent with the preferential loss of one parent's contribution.
Dilkes said the retained genes may have a role in the plants' fitness but genes that weren't expressed would be deleted from the genome.
"The genome is moving toward a two-copy organization, a diploid, by preferentially deleting one parent. When others have looked at genomes that have ancient duplications they see large blocks of duplications in which one block has a large number of genes and the other has a sparse gene content," Dilkes said. "Perhaps a cause of this pattern in the organization of genomes is preferential expression, and, all other things being equal, the gene that is more abundantly expressed will carry a greater proportion of the fitness load for any essential function."
The National Science Foundation funded the research.
Writer: Brian Wallheimer, 765-496-2050, bwallhei@purdue.edu
Sources: Brian Dilkes, 765-494-2584, bdilkes@purdue.edu
Peter Chang, 213-821-4000, Peter.Chang@usc.edu
Ag Communications: (765) 494-2722;
Keith Robinson, robins89@purdue.edu
Agriculture News Page
ABSTRACT
Homoeolog-specific Retention and Use in Allotetraploid Arabidopsis Suecica Depends on Parent of Origin and Network Partners
Peter L. Chang, Brian P. Dilkes, Michelle McMahon,
Luca Comai, Sergey V. Nuzhdin
Background: Allotetraploids carry pairs of diverged homoeologs for most genes. With the genome doubled in size, the number of putative interactions is enormous. This poses challenges on how to coordinate the two disparate genomes and creates opportunities by enhancing the phenotypic variation. New combinations of alleles co-adapt and respond to new environmental pressures. Three stages of the allopolyploidization process - parental species divergence, hybridization, and genome duplication - have been well analyzed. The last stage of evolutionary adjustments remains mysterious.
Results: Homoeolog-specific retention and use were analyzed in Arabidopsis suecica (As), a species derived from A. thaliana (At) and A. arenosa (Aa) in a single event 12,000 to 300,000 years ago. We used 405,466 diagnostic features on tiling microarrays to recognize At and Aa contributions to the As genome and transcriptome: 324 genes lacked Aa contributions and 614 genes lacked At contributions within As. In leaf tissues, 3,458 genes preferentially expressed At homoeologs while 4,150 favored Aa homoeologs. These patterns were validated with resequencing. Genes with preferential use of Aa homoeologs were enriched for expression functions, consistent with the dominance of Aa transcription. Heterologous networks - mixed from At and Aa transcripts - were underrepresented.
Conclusions: Thousands of deleted and silenced homoeologs in the genome of As were identified. Since heterologous networks may be compromised by interspecies incompatibilities, these networks evolve co-biases, expressing either only Aa or only. At homoeologs. This progressive change towards predominantly pure parental networks might contribute to phenotypic variability and plasticity, and enable the species to exploit a larger range of environments.