Interspecific Sex in Grass Smuts and the Genetic Diversity of Their Pheromone-Receptor System

The grass smuts comprise a speciose group of biotrophic plant parasites, so-called Ustilaginaceae, which are specifically adapted to hosts of sweet grasses, the Poaceae family. Mating takes a central role in their life cycle, as it initiates parasitism by a morphological and physiological transition from saprobic yeast cells to pathogenic filaments. As in other fungi, sexual identity is determined by specific genomic regions encoding allelic variants of a pheromone-receptor (PR) system and heterodimerising transcription factors. Both operate in a biphasic mating process that starts with PR–triggered recognition, directed growth of conjugation hyphae, and plasmogamy of compatible mating partners. So far, studies on the PR system of grass smuts revealed diverse interspecific compatibility and mating type determination. However, many questions concerning the specificity and evolutionary origin of the PR system remain unanswered. Combining comparative genetics and biological approaches, we report on the specificity of the PR system and its genetic diversity in 10 species spanning about 100 million years of mating type evolution. We show that three highly syntenic PR alleles are prevalent among members of the Ustilaginaceae, favouring a triallelic determination as the plesiomorphic characteristic of this group. Furthermore, the analysis of PR loci revealed increased genetic diversity of single PR locus genes compared to genes of flanking regions. Performing interspecies sex tests, we detected a high potential for hybridisation that is directly linked to pheromone signalling as known from intraspecies sex. Although the PR system seems to be optimised for intraspecific compatibility, the observed functional plasticity of the PR system increases the potential for interspecific sex, which might allow the hybrid-based genesis of newly combined host specificities

Expression Profiling of the Wheat Pathogen Zymoseptoria tritici Reveals Genomic Patterns of Transcription and Host-Specific Regulatory Programs

Host specialization by pathogens requires a repertoire of virulence factors as well as fine-tuned regulation of gene expression. The fungal wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola) is a powerful model system for the discovery of genetic elements that underlie virulence and host specialization. We transcriptionally profiled the early stages of Z. tritici infection of a compatible host (wheat) and a noncompatible host (Brachypodium distachyon). The results revealed infection regulatory programs common to both hosts and genes with striking wheat-specific expression, with many of the latter showing sequence signatures of positive selection along the Z. tritici lineage. Genes specifically regulated during infection of wheat populated two large clusters of coregulated genes that may represent candidate pathogenicity islands. On evolutionarily labile, repeat-rich accessory chromosomes (ACs), we identified hundreds of highly expressed genes with signatures of evolutionary constraint and putative biological function. Phylogenetic analyses suggested that gene duplication events on these ACs were rare and largely preceded the diversification of Zymoseptoria species. Together, our data highlight the likely relevance for fungal growth and virulence of hundreds of Z. tritici genes, deepening the annotation and functional inference of the genes of this model pathogen

Emerging oomycete threats to plants and animals

Oomycetes, or water moulds, are fungal-like organisms phylogenetically related to algae. They cause devastating diseases to both plants and animals. Here, we describe seven oomycete species that are emerging or re-emerging threats to agriculture, horticulture, aquaculture, and natural ecosystems. They include the plant pathogens Phytophthora infestans, Phytophthora palmivora, Phytophthora ramorum, Plasmopara obducens, and the animal pathogens Aphanomyces invadans, Saprolegnia parasitica, and Halioticida noduliformans. For each species, we describe its pathology, importance, and impact, discuss why it is an emerging threat, and briefly review current research activities

Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain

A subset of plant NLR immune receptors carry unconventional integrated domains in addition to their canonical domain architecture. One example is rice Pik-1 that comprises an integrated heavy metal-associated (HMA) domain. Here, we reconstructed the evolutionary history of Pik-1 and its NLR partner, Pik-2, and tested hypotheses about adaptive evolution of the HMA domain. Phylogenetic analyses revealed that the HMA domain integrated into Pik-1 before Oryzinae speciation over 15 million years ago and has been under diversifying selection. Ancestral sequence reconstruction coupled with functional studies showed that two Pik-1 allelic variants independently evolved from a weakly binding ancestral state to high-affinity binding of the blast fungus effector AVR-PikD. We conclude that for most of its evolutionary history the Pik-1 HMA domain did not sense AVR-PikD, and that different Pik-1 receptors have recently evolved through distinct biochemical paths to produce similar phenotypic outcomes. These findings highlight the dynamic nature of the evolutionary mechanisms underpinning NLR adaptation to plant pathogens

Nine things to know about elicitins

Elicitins are structurally conserved extracellular proteins in Phytophthora and Pythium oomycete pathogen species. They were first described in the late 1980s as abundant proteins in Phytophthora culture filtrates that have the capacity to elicit hypersensitive (HR) cell death and disease resistance in tobacco. Later, they became well-established as having features of microbe-associated molecular patterns (MAMPs) and to elicit defences in a variety of plant species. Research on elicitins culminated in the recent cloning of the elicitin response (ELR) cell surface receptor-like protein, from the wild potato Solanum microdontum, which mediates response to a broad range of elicitins. In this review, we provide an overview on elicitins and the plant responses they elicit. We summarize the state of the art by describing what we consider to be the nine most important features of elicitin biology

Der Einfluss sexueller Reproduktion und Virulenz auf die Evolution und Speziation der biotrophen Brandpilzfamilie Ustilaginaceae

Die Brandpilzfamilie Ustilaginaceae umfasst eine Gruppe pflanzenbiotropher Pilze, welche sich spezifisch an Wirte der Poaceae angepasst haben. Sie evolvierten eine bemerkenswerte Artenvielfalt mit über 250 Arten, von denen die meisten nur eine Wirtsart parasitieren. Der Gegensatz zwischen hoher Wirtsspezifität und großer Artenvielfalt wirft die Frage auf, welche Faktoren der Artbildung in dieser Gruppe zugrunde liegen. Das Ziel dieser Studie war es, die Rolle der sexuellen Fortpflanzung und Virulenz in Artbildungsprozessen der pflanzenbiotrophen Pilzfamilie Ustilaginaceae zu evaluieren. Mit der Kombination von vergleichender Genetik und biologischen Ansätzen untersucht diese Arbeit die Spezifität des Pheromon-Rezeptor Systems sowie seine genetische Vielfalt in 10 Arten der Ustilaginales und umspannt damit 100 Millionen Jahre Evolution. Darüber hinaus wurden 33 Virulenzfaktoren von bis zu 16 Stämmen von $\it Ustilago maydis$ analysiert, um die Anpassungsfähigkeit seiner Virulenz zu bewerten.The grass smut family Ustilaginaceae represents a group of plant-biotrophic fungi that have specifically adapted to hosts of the Poaceae. They evolved a remarkable diversity of more than 250 species of which most species parasitise only one host species. The contradiction of strong host specificity and species richness left many questions unanswered about the driving forces for speciation in this group. The aim of this study was to evaluate the impact of sexual reproduction and virulence on speciation in the plant-biotrophic Ustilaginaceae. Combining comparative genetics and biological approaches this work reports on the specificity of the PR system and its genetic diversity in 10 species of the Ustilaginales spanning about 100 million years of mating type evolution. Furthermore, a set of 33 virulence factors from up to 16 strains of $\ Ustilago maydis$ was analysed to evaluate the evolvability and adaptivity of virulence in $\it U. maydis$

History of A. thaliana Atg8 isoform identifiers

<div>Atg8 isoforms of <i>Arabidospis thaliana</i> were assigned multiple names in earlier publications. The presented table summarises these names with each row linking former names to the current nomenclature and coding sequence as provided by The Arabidopsis Information Resource (https://www.arabidopsis.org).</div><div><p><br></p><p><br></p><p>Doelling, J. H., Walker, J. M., Friedman, E. M., Thompson, A. R., & Vierstra, R. D. (2002). The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. <i>Journal of Biological Chemistry</i>, <i>277</i>(36), 33105–33114. http://doi.org/10.1074/jbc.M204630200</p><p>Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., … Ohsumi, Y. (2002). Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. <i>Plant Physiology</i>, <i>129</i>(3), 1181–93. http://doi.org/10.1104/pp.011024</p><p>Sláviková, S., Shy, G., Yao, Y., Glozman, R., Levanony, H., Pietrokovski, S., … Galili, G. (2005). The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. <i>Journal of Experimental Botany</i>, <i>56</i>(421), 2839–2849. http://doi.org/10.1093/jxb/eri276</p><p>Thompson, A. R. (2005). Autophagic Nutrient Recycling in Arabidopsis Directed by the ATG8 and ATG12 Conjugation Pathways. <i>Plant Physiology</i>, <i>138</i>(4), 2097–2110. http://doi.org/10.1104/pp.105.060673</p><p>Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T., & Ohsumi, Y. (2004). Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. <i>The Plant Cell</i>, <i>16</i>(11), 2967–2983. http://doi.org/10.1105/tpc.104.025395</p></div

Patterns of variation at Ustilago maydis\textit {Ustilago maydis} virulence clusters 2A and 19A largely reflect the demographic history of its populations

The maintenance of an intimate interaction between plant-biotrophic fungi and their hosts over evolutionary times involves strong selection and adaptative evolution of virulence-related genes. The highly specialised maize pathogen $\textit {Ustilago maydis}$ is assigned with a high evolutionary capability to overcome host resistances due to its high rates of sexual recombination, large population sizes and long distance dispersal. Unlike most studied fungus-plant interactions, the $\textit {U. maydis – Zea mays}$ pathosystem lacks a typical gene-for-gene interaction. It exerts a large set of secreted fungal virulence factors that are mostly organised in gene clusters. Their contribution to virulence has been experimentally demonstrated but their genetic diversity within $\textit {U. maydis}$ remains poorly understood. Here, we report on the intraspecific diversity of 34 potential virulence factor genes of $\textit {U. maydis}$. We analysed their sequence polymorphisms in 17 isolates of $\textit {U. maydis}$ from Europe, North and Latin America. We focused on gene cluster 2A, associated with virulence attenuation, cluster 19A that is crucial for virulence, and the cluster-independent effector gene $\it pep1$. Although higher compared to four house-keeping genes, the overall levels of intraspecific genetic variation of virulence clusters 2A and 19A, and $\it pep1$ are remarkably low and commensurate to the levels of 14 studied non-virulence genes. In addition, each gene is present in all studied isolates and synteny in cluster 2A is conserved. Furthermore, 7 out of 34 virulence genes contain either no polymorphisms or only synonymous substitutions among all isolates. However, genetic variation of clusters 2A and 19A each resolve the large scale population structure of $\textit {U. maydis}$ indicating subpopulations with decreased gene flow. Hence, the genetic diversity of these virulence-related genes largely reflect the demographic history of $\textit {U. maydis}$ populations

Ratios of Pa and Ps.

<p>Listed are all genes that contain non-synonymous and synonymous mutations. Grey bars indicate putatively secreted protein-coding genes and white bars indicate putatively non-secreted protein-encoding genes. Bold um gene numbers represent genes of cluster 2A. Light um gene numbers represent genes of cluster 19A.</p