Diversification of defensins and NLRs in Arabidopsis species by different evolutionary mechanisms

Abstract

Background: Genes encoding proteins underlying host-pathogen co-evolution and which are selected for new resistance specificities frequently are under positive selection, a process that maintains diversity. Here, we tested the contribution of natural selection, recombination and transcriptional divergence to the evolutionary diversification of the plant defensins superfamily in three Arabidopsis species. The intracellular NOD-like receptor (NLR) family was used for comparison because positive selection has been well documented in its members. Similar to defensins, NLRs are encoded by a large and polymorphic gene family and many of their members are involved in the immune response. Results: Gene trees of Arabidopsis defensins (DEFLs) show a high prevalence of clades containing orthologs. This indicates that their diversity dates back to a common ancestor and species-specific duplications did not significantly contribute to gene family expansion. DEFLs are characterized by a pervasive pattern of neutral evolution with infrequent positive and negative selection as well as recombination. In comparison, most NLR alignment groups are characterized by frequent occurrence of positive selection and recombination in their leucine-rich repeat (LRR) domain as well negative selection in their nucleotide-binding (NB-ARC) domain. While major NLR subgroups are expressed in pistils and leaves both in presence or absence of pathogen infection, the members of DEFL alignment groups are predominantly transcribed in pistils. Furthermore, conserved groups of NLRs and DEFLs are differentially expressed in response to Fusarium graminearum regardless of whether these genes are under positive selection or not. Conclusions: The present analyses of NLRs expands previous studies in Arabidopsis thaliana and highlights contrasting patterns of purifying and diversifying selection affecting different gene regions. DEFL genes show a different evolutionary trend, with fewer recombination events and significantly fewer instances of natural selection. Their heterogeneous expression pattern suggests that transcriptional divergence probably made the major contribution to functional diversification. In comparison to smaller families encoding pathogenesis-related (PR) proteins under positive selection, DEFLs are involved in a wide variety of processes that altogether might pose structural and functional trade-offs to their family-wide pattern of evolution.

Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats

“…NLRs can have an N-terminal TIR-domain (TNLs) or CC-domain (CNLs), followed by a nucleotide binding site and leucine-rich repeats. In A. thaliana, some NLRs appear to show signatures of positive or balancing selection (Bakker et al, 2006) and overall NLRs seem to show more positive selection than other defence-related gene families (Mondrag on-Palomino et al, 2017). A recent study on the total NLR complement of 65 A. thaliana accessions shows that not all NLRs show similar levels of diversity; those recognizing biotrophs are the most genetically diverse (de Weyer et al, 2019).…”

Population studies of the wild tomato species Solanum chilense reveal geographically structured major gene-mediated pathogen resistance

“…Recombination and gene conversion have been shown to play a major role in gene family evolution for RLP family as well as other resistance gene families (Paniske et al , 1997; Mondragon-Palomino & Gaut, 2005; Mondragon-Palomino et al , 2017). Recently, it has been reported that such gene conversions, or micro recombinations, of NLR genes can also be observed between accessions of another wild Solanum sp., leading to an alternative mechanism to maintain different functional alleles (Witek et al , 2020).…”

Plant peptides in plant defense responses

“…26 In Arabidopsis genome, it contains approximate 285 PDF and defensin-like genes. 27 Majority of Arabidopsis PDFs have eight Cys residues except for some contain only four to six. PDFs in diverse model plants and crops exhibited their involvement in the innate immune responses to fungal pathogens including Fusarium spp., Botrytis cinerea, and Verticillium dahlia, and bacteria pathogens like Pectobacterium carotovorum.…”