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Alien Domains Shaped the Modular Structure of Plant NLR Proteins - PubMed

  • ️Tue Jan 01 2019

Alien Domains Shaped the Modular Structure of Plant NLR Proteins

Giuseppe Andolfo et al. Genome Biol Evol. 2019.

Abstract

Plant innate immunity mostly relies on nucleotide-binding (NB) and leucine-rich repeat (LRR) intracellular receptors to detect pathogen-derived molecules and to induce defense responses. A multitaxa reconstruction of NB-domain associations allowed us to identify the first NB-LRR arrangement in the Chlorophyta division of the Viridiplantae. Our analysis points out that the basic NOD-like receptor (NLR) unit emerged in Chlorophytes by horizontal transfer and its diversification started from Toll/interleukin receptor-NB-LRR members. The operon-based genomic structure of Chromochloris zofingiensis NLR copies suggests a functional origin of NLR clusters. Moreover, the transmembrane signatures of NLR proteins in the unicellular alga C. zofingiensis support the hypothesis that the NLR-based immunity system of plants derives from a cell-surface surveillance system. Taken together, our findings suggest that NLRs originated in unicellular algae and may have a common origin with cell-surface LRR receptors.

Keywords: R gene; NLR gene family; Viridiplantae; horizontal gene transfer; phylogenetic analysis; supra domain.

© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.

—Natural diversification of the NB-encoding gene families retrieved from bacteria, archaea, glaucophytes, algae, and bryophytes. The evolutionary history of 217 NB-encoding genes, harboring at least 50% of the NB Pfam domain, was used together with 70 well-characterized plant R genes to perform a maximum likelihood analysis. Labels showing the bootstrap values higher than 50 (out of 100) are indicated above the branches. The taxa to which the protein sequences belong are indicated by colored spots.

<sc>Fig</sc>. 2.
Fig. 2.

—Maximum likelihood phylogenetic tree and genomic reshuffles of green algae NB-encoding genes. (A) The tree includes 13 genes and one outgroup gene with an NB domain, the human APAF1. Clades were numbered with Roman numerals from I to III. Bootstrap values higher than 50 (out of 100 replicates) are indicated above the branches. (B) Identification of putative genomic reshuffles in a KfNLR locus (KFL00295_0030) is shown. The LCBs (red boxes) are conserved segments, that appear to be internally free from gene rearrangements. Collinear blocks are connected by black-dotted lines, whereas block boundaries indicate breakpoints.

<sc>Fig</sc>. 3.
Fig. 3.

—Prediction and horizontally transferred genes and genomic characterization of the two functioning units of C. zofingiensis genomic DNA (operons). (A) The negative cumulative GC-profile (violet line) for the Cz1030-34550 region of C. zofingiensis Un55705 chromosome (corresponding to the NLR-like gene cluster reported in panel C), marked with the segmentation points (green square) revealed. (B) Gel shows the genetic transcription of CzNLRs and the molecular validation of two erroneously split CzNLR genes (g00129/g00130/g00131 and g00133/g00134/g00135). The primer pairs (green triangles) designed in the Cz1030-34640 region are shown at the top. Control RT-PCRs amplifying a section of the Cz05g19160 locus (ACT) or a portion of the actinA mRNA sequence are also shown (Lee et al. 2015). (C) A cluster of NLR genes (red arrows) containing the two operons located on the Cz1030-34550 region of chromosome Un55705.

<sc>Fig</sc>. 4.
Fig. 4.

—In silico validation of PHOBIUS α-TM regions in the C. zofingiensis UNPLg00127 locus. From top to bottom, we report the putative TM-region predictions of DAS-TM, TMpred, and TMHMM software (Venko et al. 2017). A dashed black box underlines two PHOBIUS α-TM regions (ivory boxes), which were confirmed by all the predictors used (green, blue, and red peaks of DAS-TM, TMpred, and TMHMM predictions, respectively).

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