Te evolution of virulence and pathogenicity in plant pathogen populations

The term virulence has a conflicting history among plant pathologists. Here we define virulence as the degree of damage caused to a host by parasite infection, assumed to be negatively correlated with host fitness, and pathogenicity the qualitative capacity of a parasite to infect and cause disease on a host. Selection may act on both virulence and pathogenicity, and their change in parasite populations can drive parasite evolution and host– parasite co-evolution. Extensive theoretical analyses of the factors that shape the evolution of pathogenicity and virulence have been reported in last three decades. Experimental work has not followed the path of theoretical analyses. Plant pathologists have shown greater interest in pathogenicity than in virulence, and our understanding of the molecular basis of pathogenicity has increased enormously. However, little is known regarding the molecular basis of virulence. It has been proposed that the mechanisms of recognition of parasites by hosts will have consequences for the evolution of pathogenicity, but much experimental work is still needed to test these hypotheses. Much theoretical work has been based on evidence from cellular plant pathogens. We review here the current experimental and observational evidence on which to test theoretical hypotheses or conjectures. We compare evidence from viruses and cellular pathogens, mostly fungi and oomycetes, which differ widely in genomic complexity and in parasitism. Data on the evolution of pathogenicity and virulence from viruses and fungi show important differences, and their comparison is necessary to establish the generality of hypotheses on pathogenicity and virulence evolution

A quantitative analysis of complementation of deleterious mutants in plant virus populations

Complementation can be defined as the process by which the function affected by a mutation is provided in trans by fully competent genotypes. Complementation can, thus, counter the effects of selection of deleterious mutants. Complementation of mutants defective for replication, movement and transmission has been often described in experiments with viruses and, occasionally, has been reported to occur in their natural populations. However, the role of complementation in virus evolution has been overlooked. Here is provided a quantitative estimate of the efficiency of complementation, defined as the probability that a non-functional mutant accomplishes a function relative to a functional one. For this, the frequency of mutants of Tobacco mosaic virus (TMV) defective for cell to cell movement was estimated in wild type tobacco plants and in transgenic plants expressing the TMV movement protein (MP) from a transgene. Mutants lethal for cell-to-cell movement were complemented by wild-type TMV in the first case, and by the transgene-expressed MP in the second case. Assuming that complementation is fully efficient in the transgenic plants, a value for the efficiency of complementation of 0.34 was obtained. Thus, complementation can efficiently counter selection on lethal mutants, and may have an important role on virus evolution. Complementation may be relevant for management of viral diseases if the complemented deleterious mutation is linked to other functions affecting the pathogenicity or epidemiology of the virus. - La complementación puede definirse como el proceso por el cual una función afectada por una mutación es provista en trans por genotipos competentes para dicha función. La complementación de mutantes defectivos para replicación, movimiento o transmisión se ha descrito con frecuencia en poblaciones experimentales de virus y, ocasionalmente, en poblaciones de campo. Sin embargo, el papel de la complementación en la evolución de los virus no se ha considerado. En este trabajo presentamos una estima de la eficacia de la complementación, definida como la probabilidad de que un mutante no funcional realice la función respecto a un genotipo funcional. Para ello se estimó la frecuencia de mutantes del virus del mosaico del tabaco (TMV) defectivos para el movimiento de célula a célula en plantas silvestres de tabaco y en plantas transgénicas que expresan constitutivamente la proteína del movimiento (MP) de TMV. En el primer caso, los mutantes letales para movimiento serán complementados por genotipos silvestres de TMV, y en el segundo, por la MP transgénica. Suponiendo que la complementación en las plantas transgénicas es totalmente eficaz, se obtuvo un valor de la eficacia de complementación de 0,34. Esto muestra que la complementación puede contrarrestar eficazmente el efecto de la selección sobre mutantes deletéreos y tener un papel importante en la evolución de virus, con importantes implicaciones prácticas si la mutación deletérea complementada está ligada a otras funciones que afecten a la patogenicidad o epidemiología del virus

How Do Pathogens Evolve Novel Virulence Activities?

This article is part of the Top 10 Unanswered Questions in MPMI invited review series.We consider the state of knowledge on pathogen evolution of novel virulence activities, broadly defined as anything that increases pathogen fitness with the consequence of causing disease in either the qualitative or quantitative senses, including adaptation of pathogens to host immunity and physiology, host species, genotypes, or tissues, or the environment. The evolution of novel virulence activities as an adaptive trait is based on the selection exerted by hosts on variants that have been generated de novo or arrived from elsewhere. In addition, the biotic and abiotic environment a pathogen experiences beyond the host may influence pathogen virulence activities. We consider host-pathogen evolution, host range expansion, and external factors that can mediate pathogen evolution. We then discuss the mechanisms by which pathogens generate and recombine the genetic variation that leads to novel virulence activities, including DNA point mutation, transposable element activity, gene duplication and neofunctionalization, and genetic exchange. In summary, if there is an (epi)genetic mechanism that can create variation in the genome, it will be used by pathogens to evolve virulence factors. Our knowledge of virulence evolution has been biased by pathogen evolution in response to major gene resistance, leaving other virulence activities underexplored. Understanding the key driving forces that give rise to novel virulence activities and the integration of evolutionary concepts and methods with mechanistic research on plant-microbe interactions can help inform crop protection.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license

Fungal endophytes of Brassicaceae: molecular interactions and crop benefits

Brassicaceae family includes an important group of plants of great scientific interest, e.g., the model plant Arabidopsis thaliana, and of economic interest, such as crops of the genus Brassica (Brassica oleracea, Brassica napus, Brassica rapa, etc.). This group of plants is characterized by the synthesis and accumulation in their tissues of secondary metabolites called glucosinolates (GSLs), sulfur-containing compounds mainly involved in plant defense against pathogens and pests. Brassicaceae plants are among the 30% of plant species that cannot establish optimal associations with mycorrhizal hosts (together with other plant families such as Proteaceae, Chenopodiaceae, and Caryophyllaceae), and GSLs could be involved in this evolutionary process of non-interaction. However, this group of plants can establish beneficial interactions with endophytic fungi, which requires a reduction of defensive responses by the host plant and/or an evasion, tolerance, or suppression of plant defenses by the fungus. Although much remains to be known about the mechanisms involved in the Brassicaceae-endophyte fungal interaction, several cases have been described, in which the fungi need to interfere with the GSL synthesis and hydrolysis in the host plant, or even directly degrade GSLs before they are hydrolyzed to antifungal isothiocyanates. Once the Brassicaceae-endophyte fungus symbiosis is formed, the host plant can obtain important benefits from an agricultural point of view, such as plant growth promotion and increase in yield and quality, increased tolerance to abiotic stresses, and direct and indirect control of plant pests and diseases. This review compiles the studies on the interaction between endophytic fungi and Brassicaceae plants, discussing the mechanisms involved in the success of the symbiosis, together with the benefits obtained by these plants. Due to their unique characteristics, the family Brassicaceae can be seen as a fruitful source of novel beneficial endophytes with applications to crops, as well as to generate new models of study that allow us to better understand the interactions of these amazing fungi with plants.SD-G was funded by the "Margarita Salas" Grants Program for Young Doctors (RD 289/2021) of the Ministry of Universities of Spain, which is included in the European Recovery Plan "Next Generation EU."MD-U was funded by the proyect IN607A 2021/03, Xunta de Galicia, Spain

Plant Pathogenic Microorganisms: State-of-the-Art Research in Spain

We would like to thank all the authors who contributed their papers to this Special Issue and the reviewers for their helpful recommendations. We are also grateful to Marta Colomer, Josephine Xue, and members of the Microorganisms’ Editorial Office for their continuous support in managing and organizing this Special Issue. In addition, we would like to acknowledge the academic editors James F. White, Mohamed Hijri, and Michael J. Bidochka who made decisions for certain papers.Publishe

España y Portugal durante la Segunda Guerra Mundial

Cuando las relaciones internacionales entran en franco deterioro en el escenario europeo, el entendimiento político entre España y Portugal presentaba a la Península Ibérica como un bloque relativamente unido ante la conflagración mundial. La política exterior de estos dos Estados durante la segunda guerra mundial se enmarca dentro de unas coordenadas, que son tenidas en cuenta por los diplomáticos de ambas naciones, de los beligerantes y neutrales: la coincidencia del talante político e ideológico de los regímenes de Salazar y Franco se sumaba a la importancia estratégica de la Península, que obligaba a un entendimiento entre ambos Estados, siempre amenazados por el peligro de un ataque proveniente del exterior

Alternative polyadenylation and salicylic acid modulate root responses to low nitrogen availability

Nitrogen (N) is probably the most important macronutrient and its scarcity limits plant growth, development and fitness. N starvation response has been largely studied by transcriptomic analyses, but little is known about the role of alternative polyadenylation (APA) in such response. In this work, we show that N starvation modifies poly(A) usage in a large number of transcripts, some of them mediated by FIP1, a component of the polyadenylation machinery. Interestingly, the number of mRNAs isoforms with poly(A) tags located in protein-coding regions or 5 '-UTRs significantly increases in response to N starvation. The set of genes affected by APA in response to N deficiency is enriched in N-metabolism, oxidation-reduction processes, response to stresses, and hormone responses, among others. A hormone profile analysis shows that the levels of salicylic acid (SA), a phytohormone that reduces nitrate accumulation and root growth, increase significantly upon N starvation. Meta-analyses of APA-affected and fip1-2-deregulated genes indicate a connection between the nitrogen starvation response and salicylic acid (SA) signaling. Genetic analyses show that SA may be important for preventing the overgrowth of the root system in low N environments. This work provides new insights on how plants interconnect different pathways, such as defense-related hormonal signaling and the regulation of genomic information by APA, to fine-tune the response to low N availability

Alternative Polyadenylation and Salicylic Acid Modulate Root Responses to Low Nitrogen Availability

16 Pág.Nitrogen (N) is probably the most important macronutrient and its scarcity limits plant growth, development and fitness. N starvation response has been largely studied by transcriptomic analyses, but little is known about the role of alternative polyadenylation (APA) in such response. In this work, we show that N starvation modifies poly(A) usage in a large number of transcripts, some of them mediated by FIP1, a component of the polyadenylation machinery. Interestingly, the number of mRNAs isoforms with poly(A) tags located in protein-coding regions or 5'-UTRs significantly increases in response to N starvation. The set of genes affected by APA in response to N deficiency is enriched in N-metabolism, oxidation-reduction processes, response to stresses, and hormone responses, among others. A hormone profile analysis shows that the levels of salicylic acid (SA), a phytohormone that reduces nitrate accumulation and root growth, increase significantly upon N starvation. Meta-analyses of APA-affected and fip1-2-deregulated genes indicate a connection between the nitrogen starvation response and salicylic acid (SA) signaling. Genetic analyses show that SA may be important for preventing the overgrowth of the root system in low N environments. This work provides new insights on how plants interconnect different pathways, such as defense-related hormonal signaling and the regulation of genomic information by APA, to fine-tune the response to low N availability.Research was supported by grants from the Spanish Government BIO2017-82209-R, and BIO2014-52091-R to J.C.P. and by the “Severo Ochoa Program for Centres of Excellence in R&D” from the Agencia Estatal de Investigación of Spain (grant SEV-2016-0672 (2017-2021) to the CBGP. CMC by a predoctoral fellowship (BES-2017-082152) associated to the Severo Ochoa Program. AS was supported by a Torres Quevedo grant (PTQ-15-07915) from MINECO (Spain).Peer reviewe

Differential Expression of Fungal Genes Determines the Lifestyle of Plectosphaerella Strains During Arabidopsis thaliana Colonization

16 Päg.The fungal genus Plectosphaerella comprises species and strains with different lifestyles on plants, such as P. cucumerina, which has served as model for the characterization of Arabidopsis thaliana basal and nonhost resistance to necrotrophic fungi. We have sequenced, annotated, and compared the genomes and transcriptomes of three Plectosphaerella strains with different lifestyles on A. thaliana, namely, PcBMM, a natural pathogen of wild-type plants (Col-0), Pc2127, a nonpathogenic strain on Col-0 but pathogenic on the immunocompromised cyp79B2 cyp79B3 mutant, and P0831, which was isolated from a natural population of A. thaliana and is shown here to be nonpathogenic and to grow epiphytically on Col-0 and cyp79B2 cyp79B3 plants. The genomes of these Plectosphaerella strains are very similar and do not differ in the number of genes with pathogenesis-related functions, with the exception of secreted carbohydrate-active enzymes (CAZymes), which are up to five times more abundant in the pathogenic strain PcBMM. Analysis of the fungal transcriptomes in inoculated Col-0 and cyp79B2 cyp79B3 plants at initial colonization stages confirm the key role of secreted CAZymes in the necrotrophic interaction, since PcBMM expresses more genes encoding secreted CAZymes than Pc2127 and P0831. We also show that P0831 epiphytic growth on A. thaliana involves the transcription of specific repertoires of fungal genes, which might be necessary for epiphytic growth adaptation. Overall, these results suggest that in-planta expression of specific sets of fungal genes at early stages of colonization determine the diverse lifestyles and pathogenicity of Plectosphaerella strains.This work was supported by the Spanish Ministry of Economy and Competitiveness (MINECO) grant BIO2015-64077-R and the Spanish Research Agency (AEI) grant RTI2018-096975-B-I00 to A. Molina and by the “Severo Ochoa Programme for Centers of Excellence in R&D” grant SEV-2016-0672 (2017-2021) to the CBGP (UPM-INIA). In the frame of SEV-2016-0672 program, H. Mélida was supported with a postdoctoral contract. A. Muñoz-Barrios was financially supported by the Universidad Politécnica de Madrid (UPM) Ph.D. students PIF program, I. del Hierro was a FPU fellow (Spanish Ministry of Education, Culture and Sports grant FPU16/07118), V. Fernández-Calleja was supported by the Consejería de Educacíon e Investigacíon of Comunidad de Madrid YEI program for postdoctoral researchers (PEJD-2016/BIO-3327), and the work was further supported through a Comunidad de Madrid YEI program for laboratory technicians grant (PEJ16/BIO/TL-1570).Peer reviewe

Coevolution between a Family of Parasite Virulence Effectors and a Class of LINE-1 Retrotransposons

Parasites are able to evolve rapidly and overcome host defense mechanisms, but the molecular basis of this adaptation is poorly understood. Powdery mildew fungi (Erysiphales, Ascomycota) are obligate biotrophic parasites infecting nearly 10,000 plant genera. They obtain their nutrients from host plants through specialized feeding structures known as haustoria. We previously identified the AVRk1 powdery mildew-specific gene family encoding effectors that contribute to the successful establishment of haustoria. Here, we report the extensive proliferation of the AVRk1 gene family throughout the genome of B. graminis, with sequences diverging in formae speciales adapted to infect different hosts. Also, importantly, we have discovered that the effectors have coevolved with a particular family of LINE-1 retrotransposons, named TE1a. The coevolution of these two entities indicates a mutual benefit to the association, which could ultimately contribute to parasite adaptation and success. We propose that the association would benefit 1) the powdery mildew fungus, by providing a mechanism for amplifying and diversifying effectors and 2) the associated retrotransposons, by providing a basis for their maintenance through selection in the fungal genome