The Brassicaceae Family Displays Divergent, Shoot-Skewed NLR Resistance Gene Expression

Abstract

Nucleotide-binding site leucine-rich repeat resistance genes (NLRs) allow plants to detect microbial effectors. We hypothesized that NLR expression patterns could reflect organ-specific differences in effector challenge and tested this by carrying out a metaanalysis of expression data for 1,235 NLRs from nine plant species. We found stable NLR root/shoot expression ratios within species, suggesting organ-specific hardwiring of NLR expression patterns in anticipation of distinct challenges. Most monocot and dicot plant species preferentially expressed NLRs in roots. In contrast, Brassicaceae species, including oilseed rape (Brassica napus) and the model plant Arabidopsis (Arabidopsis thaliana), were unique in showing NLR expression skewed toward the shoot across multiple phylogenetically distinct groups of NLRs. The Brassicaceae are also outliers in the sense that they have lost the common symbiosis signaling pathway, which enables intracellular infection by root symbionts. While it is unclear if these two events are related, the NLR expression shift identified here suggests that the Brassicaceae may have evolved unique patternrecognition receptors and antimicrobial root metabolites to substitute for NLR protection. Such innovations in root protection could potentially be exploited in crop rotation schemes or for enhancing root defense systems of non-Brassicaceae crops.

Insights into the evolution of symbiosis gene copy number and distribution from a chromosome-scaleLotus japonicusGifu genome sequence

“…To produce a gene expression atlas, publicly available and new RNA-seq data from Lotus Gifu was obtained for 35 conditions across different tissues, symbiotic, and pathogenic interactions ( Supplementary Table S1 ). The conditions available include root hair, nodule primordia, and nodules obtained after inoculation with Mesorhizobium loti R7A and root interactions with microbes across a symbiont-pathogen spectrum; 18 root and shoot tissues 3 days after roots were inoculated with M. loti 45 ; root symbiotic susceptible zone treated with cytokinin (1 µM BA) or M. loti R7A (this study); roots inoculated with the arbuscular mycorrhizal fungus (AMF), Glomus intraradices 46 ; root, leaf, immature flowers, mature flowers, pods, and seeds (SRA ID: PRJDB2436). Gene-level quantification of the data was normalized across conditions ( Supplementary File S4 ) and is made available through Lotus Base ( https://lotus.au.dk/expat/ ) to provide a readily accessible expression viewer.…”

Distinct Lotus japonicus Transcriptomic Responses to a Spectrum of Bacteria Ranging From Symbiotic to Pathogenic

“…Transcriptome responses during nodule colonization were examined through the harvesting of 7 dpi nodule primordia that are in the early stages of colonization by R7A and mature nitrogen-fixing nodules that are fully colonized by R7A. RNA-seq of whole roots (minus root tips) and shoots collected at 3 dpi to provide a basis for tissue-specific responses was previously performed ( Munch et al, 2018 ). For each condition examined, biological triplicate samples were harvested and total RNA was isolated.…”

“…Sequencing data is deposited at the Short Read Archive with the BioProject ID SRP127678 . Sequencing data for roots and shoots 3 dpi with R7A was obtained previously ( Munch et al, 2018 ) and is deposited at the Short Read Archive with the BioProject ID PRJNA384655 .…”

Disease Resistance Genetics and Genomics in Octoploid Strawberry

“…The highest levels of NLR expression were seen in the roots and leaves, indicating this mode of resistance may be more common in these tissues. Root-dominant expression of NLRs is common in many but not all plant species (Munch et al 2018). Strawberry NLR expression overlaps poorly between tissues, supporting the concept that NLRs are optimized for each tissue (Munch et al 2018).…”