Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response

Baggs, Erin; Monroe, J. Grey; Thanki, Anil; O’Grady, R; Schudoma, Christian; Haerty, Wilfried; Krasileva, Ksenia V.

doi:10.1105/tpc.19.00903

Cited by 71 publications

(89 citation statements)

References 128 publications

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“…That is, 11 of the 12 aquatic plants surveyed had no more than 200 NLR genes, and nine of these had fewer than 100 NLR genes. This is consistent with the findings of a previous study, which showed convergent reductions of NLR genes among four aquatic plants in two orders (Baggs et al, 2020).…”

Section: Nlr Contraction Tends To Occur In Aquatic Parasitic and Casupporting

confidence: 93%

“…Baggs et al (2020) reported the convergent loss of EDS1, PAD4, and ADR1 in four aquatic species, and hypothesized that the plant immune system co-evolved with thedrought response system. Of the 16 species lacking the RNL and EDS1 gene families identified in the present study, eight are indeed aquatic species: Spirodela polyrhiza, Lemna minor, Zostera marina, Zostera muelleri, U. gibba, G. aurea, Cladopus chinensis, and Ceratophyllum demersum.…”

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confidence: 99%

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An angiospermNLRatlas reveals thatNLRgene reduction is associated with ecological specialization and signal transduction component deletion

Liu

Zeng

et al. 2021

Preprint

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Nucleotide-binding site-leucine-rich repeat receptor (NLR) genes comprise the largest family of plant disease resistance genes. NLR genes are phylogenetically divided into the TNL, CNL, and RNL subclasses. NLR copy numbers and subclass composition vary tremendously across angiosperm genomes. However, the evolutionary associations between genomic NLR content and plant lifestyle, or between NLR content and signal transduction components, are poorly characterized due to limited genome availability. Here, we established an angiosperm NLR atlas (ANNA, http://compbio.nju.edu.cn/app/ANNA/), which includes NLR genes from over 300 angiosperm genomes. Using ANNA, we revealed that NLR copy numbers differ up to 66-fold among closely related species due to rapid gene loss and gain. Interestingly, NLR contraction was associated with adaptations to aquatic, parasitic, and carnivorous lifestyles. The convergent NLR reduction in aquatic plants resembles the long-term evolutionary silence of NLR genes in green algae before the colonization of land. A co-evolutionary pattern between NLR subclasses and plant immune-pathway components was also identified, suggesting that immune pathway deficiencies may drive TNL loss. Finally, we recovered a conserved TNL lineage that may function independently of the RNL pathway. Our findings provide new insights into the evolution of NLR genes in the context of plant lifestyles and genome content variation.

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Section: Nlr Contraction Tends To Occur In Aquatic Parasitic and Casupporting

confidence: 93%

mentioning

confidence: 99%

An angiospermNLRatlas reveals thatNLRgene reduction is associated with ecological specialization and signal transduction component deletion

Liu

Zeng

et al. 2021

Preprint

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“…Enrichment of non-synonymous variants compared to genome wide average and Waterson's diversity estimate (theta) of non-synonymous variation were calculated independently. The frequency of loss-of-function was calculated similar to previous descriptions 61,62 , where loss-of-function was defined as alleles (premature stop codons and frameshifts) resulting in disruption of at least 10% of the coding region of the canonical gene model. Genes experiencing purifying selection should exhibit lower levels of natural polymorphism than what would be predicted by mutation rate alone.…”

Section: Signatures Of Selection and Constraint From Natural Populationsmentioning

confidence: 99%

Mutation bias shapes gene evolution in Arabidopsis thaliana

Monroe

Srikant

Carbonell‐Bejerano

et al. 2020

Preprint

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Classical evolutionary theory maintains that mutation rate variation between genes should be random with respect to fitness 1-4 and evolutionary optimization of genic mutation rates remains controversial 3,5 . However, it has now become known that cytogenetic (DNA sequence + epigenomic) features influence local mutation probabilities 6 , which is predicted by more recent theory to be a prerequisite for beneficial mutation rates between different classes of genes to readily evolve 7 . To test this possibility, we used de novo mutations in Arabidopsis thaliana to create a high resolution predictive model of mutation rates as a function of cytogenetic features across the genome . As expected, mutation rates are significantly predicted by features such as GC content, histone modifications, and chromatin accessibility. Deeper analyses of predicted mutation rates reveal effects of introns and untranslated exon regions in distancing coding sequences from mutational hotspots at the start and end of transcribed regions in A. thaliana . Finally, predicted coding region mutation rates are significantly lower in genes where mutations are more likely to be deleterious, supported by numerous estimates of evolutionary and functional constraint. These findings contradict neutral expectations that mutation probabilities are independent of fitness consequences. Instead they are consistent with the evolution of lower mutation rates in functionally constrained loci due to cytogenetic features, with important implications for evolutionary biology 8 .Monroe et al. Genome-wide mutation bias in A. thalianaA core maxim of evolutionary biology, codified through experiments completed in the early 1940s 1 , is that the "consequences of a mutation have no influence whatsoever on the probability that this mutation will or will not occur." 2 This assertion has profound implications for understanding organismal evolution and predicting human disease. That genic mutation rates might have been optimized during evolution has been extensively challenged with a strong argument: selection for mutation rates on a gene-by-gene basis cannot overcome the barrier of genetic drift 3 . And while reports of non-random relationships between mutation rates and fitness consequences have been previously made, these have been questioned because they have largely relied on substitution rates in natural populations rather than direct measures of de novo mutations 3,9-12 .More recently though, discoveries in genome biology have inspired a reevaluation of classical theories of mutation rate evolution. It is now recognized that mutation rates across genomes are influenced by DNA sequence composition, epigenomic features, and bias in the targets of DNA repair mechanisms 5,6,[13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32] . It is also known that broad classes of genes (e.g., housekeeping genes) exist in distinct cytogenetic (DNA sequence + epigenomic) states. This provides an opportunity for mutation rates to evolve in beneficial directi...

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“…In accordance with the so-called “guard” model, NLRs then trigger an ETI response (Cao et al, 2014). The Arabidopsis genome encodes 160 NLR proteins (Baggs et al, 2020), of which we identified 119 genes among our data set of DEGs (84 were assigned to clusters). Among these NLR genes, about 40% clustered across four immunity clusters, cluster C21 (18 genes), C16 (14 genes), C15 (11 genes), and C7 (4 genes), and were uniquely enriched in clusters 21 ( p -value = 2.58e−07) and 16 ( p -value = 6.82e−06), both of which include genes specifically repressed in the endophyte (Supplemental Data Set 15).…”

Section: Resultsmentioning

confidence: 99%

Metatranscriptomic comparison of endophytic and pathogenic Fusarium–Arabidopsis interactions reveals plant transcriptional plasticity

Guo

Wang

et al. 2021

Preprint

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Plants are continuously exposed to beneficial and pathogenic microbes, but how plants recognize and respond to friends versus foes remains poorly understood. Here, we compared the molecular response of Arabidopsis thaliana independently challenged with a Fusarium oxysporum endophyte Fo47 versus a pathogen Fo5176. These two Fusarium oxysporum strains share a core genome of about 46 Mb, in addition to unique 1,229 and 5,415 accessory genes. Metatranscriptomic data reveal a shared pattern of expression for most plant genes (~80%) in responding to both fungal inoculums at all time points from 12 to 96 h post inoculation (HPI). However, the distinct responding genes depict transcriptional plasticity, as the pathogenic interaction activates plant stress responses and suppresses plant growth/development related functions, while the endophytic interaction attenuates host immunity but activates plant nitrogen assimilation. The differences in reprogramming of the plant transcriptome are most obvious in 12 HPI, the earliest time point sampled and are linked to accessory genes in both fungal genomes. Collectively, our results indicate that the A. thaliana and F. oxysporum interaction displays both transcriptome conservation and plasticity in the early stages of infection, providing insights into the fine-tuning of gene regulation underlying plant differential responses to fungal endophytes and pathogens.

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Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response

Cited by 71 publications

References 128 publications

An angiospermNLRatlas reveals thatNLRgene reduction is associated with ecological specialization and signal transduction component deletion

An angiospermNLRatlas reveals thatNLRgene reduction is associated with ecological specialization and signal transduction component deletion

Mutation bias shapes gene evolution in Arabidopsis thaliana

Metatranscriptomic comparison of endophytic and pathogenic Fusarium–Arabidopsis interactions reveals plant transcriptional plasticity

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