Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli  

Abstract

Plants have substantially higher gene duplication rates compared with most other eukaryotes. These plant gene duplicates are mostly derived from whole genome and/or tandem duplications. Earlier studies have shown that a large number of duplicate genes are retained over a long evolutionary time, and there is a clear functional bias in retention. However, the influence of duplication mechanism, particularly tandem duplication, on duplicate retention has not been thoroughly investigated. We have defined orthologous groups (OGs) between Arabidopsis (Arabidopsis thaliana) and three other land plants to examine the functional bias of retained duplicate genes during vascular plant evolution. Based on analysis of Gene Ontology categories, it is clear that genes in OGs that expanded via tandem duplication tend to be involved in responses to environmental stimuli, while those that expanded via nontandem mechanisms tend to have intracellular regulatory roles. Using Arabidopsis stress expression data, we further demonstrated that tandem duplicates in expanded OGs are significantly enriched in genes that are up-regulated by biotic stress conditions. In addition, tandem duplication of genes in an OG tends to be highly asymmetric. That is, expansion of OGs with tandem genes in one organismal lineage tends to be coupled with losses in the other. This is consistent with the notion that these tandem genes have experienced lineage-specific selection. In contrast, OGs with genes duplicated via nontandem mechanisms tend to experience convergent expansion, in which similar numbers of genes are gained in parallel. Our study demonstrates that the expansion of gene families and the retention of duplicates in plants exhibit substantial functional biases that are strongly influenced by the mechanism of duplication. In particular, genes involved in stress responses have an elevated probability of retention in a single-lineage fashion following tandem duplication, suggesting that these tandem duplicates are likely important for adaptive evolution to rapidly changing environments.

Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch

“…Adaptations possibly related to the arborescent habit were visible in convergent tandem expansions shared by B. pendula and Populus trichocarpa, including genes associated with fungal pathogen defense, cell wall biogenesis, and cellulose synthase activity (Supplementary Tables 11 and 12). Through evolutionary information stored within single genomes, these results suggest that whereas polyploid duplicates tend to diversify core processes in developmental and physiological regulation, tandem duplicates enhance the diversity of a plant's environmental response capacity, which is in concurrence with previous studies 15,17,18 .…”

The genome of Eucalyptus grandis

“…5) and conserved gene order on independent BAC clones spanning two large tandem gene arrays (Supplementary Data 3 and Supplementary Information 1) support the accuracy of the assembly across highly similar tandem copies. Tandem duplication often involves stress-response genes that are retained in a lineage-specific fashion, suggesting that tandem duplication is important for adaptive evolution in dynamically changing environments 16 . For example, more than 80% of the S-domain receptorlike kinase (SDRLK) subfamily occurs in tandem arrays (Supplementary Data 4).…”

Life at the extreme: lessons from the genome

“…As the result of unequal crossing-over during recombination, tandem duplications vary in their 'genetic neighborhoods', with copies receiving different regulatory motifs that can lead to drastic changes in expression [40]. A comparative study on plant genomes ranging from Arabidopsis to Physcomitrella showed genes associated with defense, transport functions, or abiotic stress responses enriched in tandem duplicates, whereas duplicates due to other mechanisms included genes enriched in other intracellular regulatory roles [41]. …”