Contingency rules for pathogen competition and antagonism in a genetically based,plant defense hierarchy

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The Problems of Specific Phytoimmunity

Recent studies established that the specificity of phytoimmunity is shaped at the initial stages of genic interactions between a pathogen and its plant host. While elicitors, the products of pathogen avirulence genes (avr-genes), have been already investigated in great detail, there are few studies on the products of plant resistance genes (R-genes) recognizing these elicitors. This review deals with examples of nonspecific and specific elicitors of some R-genes as well as the systems that transduce the elicited signals to the plant genome and evoke immune responses in the plant cells. Several types of immunosuppressors characteristic of pathogens are considered. The molecular-genetic studies of the relations between the pathogens and their plant hosts supplement the already existing arsenal for plant protection with new technologies, such as the genetically engineered plant resistance and the resistance induced by biogenic elicitors.     

Exogenous double-stranded RNA inhibits the infection physiology of rust fungi to reduce symptoms in planta

Rust fungi (Pucciniales) are a diverse group of plant pathogens in natural and agricultural systems. They pose ongoing threats to the diversity of native flora and cause annual crop yield losses. Agricultural rusts are predominantly managed with fungicides and breeding for resistance, but new control strategies are needed on non-agricultural plants and in fragile ecosystems. RNA interference (RNAi) induced by exogenous double-stranded RNA (dsRNA) has promise as a sustainable approach for managing plant-pathogenic fungi, including rust fungi. We investigated the mechanisms and impact of exogenous dsRNA on rust fungi through in vitro and whole-plant assays using two species as models, Austropuccinia psidii (the cause of myrtle rust) and Coleosporium plumeriae (the cause of frangipani rust). In vitro, dsRNA either associates externally or is internalized by urediniospores during the early stages of germination. The impact of dsRNA on rust infection architecture was examined on artificial leaf surfaces. dsRNA targeting predicted essential genes significantly reduced germination and inhibited development of infection structures, namely appressoria and penetration pegs. Exogenous dsRNA sprayed onto 1-year-old trees significantly reduced myrtle rust symptoms. Furthermore, we used comparative genomics to assess the wide-scale amenability of dsRNA to control rust fungi. We sequenced genomes of six species of rust fungi, including three new families (Araucariomyceaceae, Phragmidiaceae, and Skierkaceae) and identified key genes of the RNAi pathway across 15 species in eight families of Pucciniales. Together, these findings indicate that dsRNA targeting essential genes has potential for broad-use management of rust fungi across natural and agricultural systems.     

Resistance and Susceptibility of Plants to Fungal Pathogens

Plants are under continuous threat of infection by pathogens endowed with diverse strategies to colonize their host. Comprehensive biochemical and genetic approaches are now starting to reveal the complex signaling pathways that mediate plant disease resistance. Initiation of defense signaling often involves specific recognition of invading pathogens by the products of specialized host resistance (R) genes. Potential resistance signaling components have been identified by mutational analyses to be required for specific resistance in the model Arabidopsis and some crop species. Strikingly, many of the components share similarity to that of innate immune systems in animals. Evidence is also accumulating that plant pathogens have a number of ways to evade host defenses during the early stages of infection, similar to animal pathogens. These strategies are becoming much better understood in a number of plant–pathogen interactions. In this review, we focus on the current knowledge of host factors that control plant resistance and susceptibility to fungal pathogens. The knowledge accumulated in these studies will serve a fundamental basis for combating diseases in strategic molecular agriculture.     

DNA markers linked to the <Emphasis Type="Italic">R</Emphasis><Subscript><Emphasis Type="Italic">2</Emphasis></Subscript> rust resistance gene in sunflower (<Emphasis Type="Italic">Helianthus annuus</Emphasis> L.) facilitate anticipatory breeding for this disease variant

Pre-emptive breeding for host disease resistance is an effective strategy for combating and managing devastating incursions of plant pathogens. Comprehensive, long-term studies have revealed that virulence to the R ₂ sunflower (Helianthus annuus L.) rust resistance gene in the line MC29 does not exist in the Australian rust (Puccinia helianthi) population. We report in this study the identification of molecular markers linked to this gene. The three simple sequence repeat (SSR) markers ORS795, ORS882, and ORS938 were linked in coupling to the gene, while the SSR marker ORS333 was linked in repulsion. Reliable selection for homozygous-resistant individuals was efficient when the three markers, ORS795, ORS882, and ORS333, were used in combination. Phenotyping for this resistance gene is not possible in Australia without introducing a quarantinable race of the pathogen. Therefore, the availability of reliable and heritable DNA-based markers will enable the efficient deployment of this gene, permitting a more effective strategy for generating sustainable commercial cultivars containing this rust resistance gene.     

Plant Innate Immune Response: Qualitative and Quantitative Resistance

Plant diseases, caused by microbes, threaten world food, feed, and bioproduct security. Plant resistance has not been effectively deployed to improve resistance in plants for lack of understanding of biochemical mechanisms and genetic bedrock of resistance. With the advent of genome sequencing, the forward and reverse genetic approaches have enabled deciphering the riddle of resistance. Invading pathogens produce elicitors and effectors that are recognized by the host membrane-localized receptors, which in turn induce a cascade of downstream regulatory and resistance metabolite and protein biosynthetic genes (R) to produce resistance metabolites and proteins, which reduce pathogen advancement through their antimicrobial and cell wall enforcement properties. The resistance in plants to pathogen attack is expressed as reduced susceptibility, ranging from high susceptibility to hypersensitive response, the shades of gray. The hypersensitive response or cell death is considered as qualitative resistance, while the remainder of the reduced susceptibility is considered as quantitative resistance. The resistance is due to additive effects of several resistance metabolites and proteins, which are produced through a network of several hierarchies of plant R genes. Plants recognize the pathogen elicitors or receptors and then induce downstream genes to eventually produce resistance metabolites and proteins that suppress the pathogen advancement in plant. These resistance genes (R), against qualitative and quantitative resistance, can be identified in germplasm collections and replaced in commercial cultivars, if nonfunctional, based on genome editing to improve plant resistance.     

Variation in resistance to multiple pathogen species: anther smuts of Silene uniflora

The occurrence of multiple pathogen species on a shared host species is unexpected when they exploit the same micro‐niche within the host individual. One explanation for such observations is the presence of pathogen‐specific resistances segregating within the host population into sites that are differentially occupied by the competing pathogens. This study used experimental inoculations to test whether specific resistances may contribute to the maintenance of two species of anther‐smut fungi, Microbotryum silenes‐inflatae and Microbotryum lagerheimii, in natural populations of Silene uniflora in England and Wales. Overall, resistance to the two pathogens was strongly positively correlated among host populations and to a lesser degree among host families within populations. A few instances of specific resistance were also observed and confirmed by replicated inoculations. The results suggest that selection for resistance to one pathogen may protect the host from the emergence via host shifts of related pathogen species, and conversely that co‐occurrence of two species of pathogens may be dependent on the presence of host genotypes susceptible to both.     

Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation

The extent and speed at which pathogens adapt to host resistance varies considerably. This presents a challenge for predicting when—and where—pathogen evolution may occur. While gene flow and spatially heterogeneous environments are recognized to be critical for the evolutionary potential of pathogen populations, we lack an understanding of how the two jointly shape coevolutionary trajectories between hosts and pathogens. The rust pathogen Melampsora lini infects two ecotypes of its host plant Linum marginale that occur in close proximity yet in distinct populations and habitats. In this study, we found that within-population epidemics were different between the two habitats. We then tested for pathogen local adaptation at host population and ecotype level in a reciprocal inoculation study. Even after controlling for the effect of spatial structure on infection outcome, we found strong evidence of pathogen adaptation at the host ecotype level. Moreover, sequence analysis of two pathogen infectivity loci revealed strong genetic differentiation by host ecotype but not by distance. Hence, environmental variation can be a key determinant of pathogen population genetic structure and coevolutionary dynamics and can generate strong asymmetry in infection risks through space.     

Phenotypic and genetic patterns of resistance to the pathogen Phakopsora pachyrhizi in populations of Glycine canescens

Summary Phenotypic patterns of resistance to nine races of the pathogen Phakopsora pachyrhizi (soybean rust) in two natural populations of Glycine canescens were determined. In both populations there was considerable variability both within and between different host lines in their resistance or susceptibility to the nine different pathogen races. The genetic basis of these patterns of resistance was analyzed through an extensive series of crosses. In both host populations resistance was conditioned by single dominant genes with major phenotypic effects. One, two or three such genes were present in each host line. Using the principles of the gene-for-gene hypothesis, knowledge about the number of resistance genes present in each host line and by cross comparison of the phenotypic patterns of disease resistance detected in each line, estimates were made of the number of resistance genes or alleles present in each population of G. canescens. The two populations contained a minimum of 10 and 12 resistance genes. The relevance of these results to agriculture is discussed briefly.     

Climate change accelerates local disease extinction rates in a long‐term wild host–pathogen association

Pathogens are a significant component of all plant communities. In recent years, the potential for existing and emerging pathogens of agricultural crops to cause increased yield losses as a consequence of changing climatic patterns has raised considerable concern. In contrast, the response of naturally occurring, endemic pathogens to a warming climate has received little attention. Here, we report on the impact of a signature variable of global climate change – increasing temperature – on the long‐term epidemiology of a natural host–pathogen association involving the rust pathogen Triphragmium ulmariae and its host plant Filipendula ulmaria. In a host–pathogen metapopulation involving approximately 230 host populations growing on an archipelago of islands in the Gulf of Bothnia we assessed changes in host population size and pathogen epidemiological measures over a 25‐year period. We show how the incidence of disease and its severity declines over that period and most importantly demonstrate a positive association between a long‐term trend of increasing extinction rates in individual pathogen populations of the metapopulation and increasing temperature. Our results are highly suggestive that changing climatic patterns, particularly mean monthly growing season (April‐November) temperature, are markedly influencing the epidemiology of plant disease in this host–pathogen association. Given the important role plant pathogens have in shaping the structure of communities, changes in the epidemiology of pathogens have potentially far‐reaching impacts on ecological and evolutionary processes. For these reasons, it is essential to increase understanding of pathogen epidemiology, its response to warming, and to invoke these responses in forecasts for the future.     

Infection assays in Arabidopsis reveal candidate effectors from the poplar rust fungus that promote susceptibility to bacteria and oomycete pathogens

Fungi of the Pucciniales order cause rust diseases which, altogether, affect thousands of plant species worldwide and pose a major threat to several crops. How rust effectors—virulence proteins delivered into infected tissues to modulate host functions—contribute to pathogen virulence remains poorly understood. Melampsora larici‐populina is a devastating and widespread rust pathogen of poplar, and its genome encodes 1184 identified small secreted proteins that could potentially act as effectors. Here, following specific criteria, we selected 16 candidate effector proteins and characterized their virulence activities and subcellular localizations in the leaf cells of Arabidopsis thaliana. Infection assays using bacterial (Pseudomonas syringae) and oomycete (Hyaloperonospora arabidopsidis) pathogens revealed subsets of candidate effectors that enhanced or decreased pathogen leaf colonization. Confocal imaging of green fluorescent protein‐tagged candidate effectors constitutively expressed in stable transgenic plants revealed that some protein fusions specifically accumulate in nuclei, chloroplasts, plasmodesmata and punctate cytosolic structures. Altogether, our analysis suggests that rust fungal candidate effectors target distinct cellular components in host cells to promote parasitic growth.     

The potential for rust infection to cause natural selection in apomictic Arabis holboellii (Brassicaceae)

Few studies have examined the potential for pathogens with complex life cycles to cause selection on their required alternate (=intermediate) hosts. Here we examine the effects of two fungal pathogens on an herbaceous mustard, Arabis holboellii. One pathogen species uses A. holboellii as a primary host, the other uses it as an alternate host. This plant-pathogen system is especially interesting because the host, A. holboellii, is apomictic; thus individuals reproduce exact copies of themselves. Despite this mode of reproduction, A. holboellii populations are surprisingly genetically diverse. Could frequency dependent selection by pathogens be maintaining clonal diversity? This study assesses the potential for selection by pathogens. In a controlled greehouse experiment we show that there is heritable variation in A. holboellii's resistance to the rust, Puccinia monoica, and that host fitness is severely reduced by P. monoica infection in both the greenhouse and under natural conditions. Field observations indicate that host clones are also differentially susceptible to the short-cycled rust, P. thlaspeos, and that host fitness is reduced by infection to this pathogen as well. Although the preconditions for pathogen-mediated selection are present, frequency-dependent selection by pathogens is unlikely to be important in structuring populations of Arabis holboellii because multiple host genotypes are susceptible to the same inoculum and the pathogen has a long generation time.     

TaAbc1, a Member of Abc1-Like Family Involved in Hypersensitive Response against the Stripe Rust Fungal Pathogen in Wheat

To search for genes involved in wheat (Triticum aestivum L.) defense response to the infection of stripe rust pathogen Puccinia striiformis f. sp. tritici (Pst), we identified and cloned a new wheat gene similar to the genes in the Abc1-like gene family. The new gene, designated as TaAbc1, encodes a 717-amino acid, 80.35 kD protein. The TaAbc1 protein contains two conserved domains shared by Abc1-like proteins, two trans-membrane domains at the C-terminal, and a 36-amino acid chloroplast targeting presequence at the N-terminal. Characterization of TaAbc1 expression revealed that gene expression was tissue-specific and could be up-regulated by biotic agents (e.g., stripe rust pathogen) and/or by an abiotic stress like wounding. High-fold induction was associated with the hypersensitive response (HR) triggered only by avirulent stripe rust pathotypes, suggesting that TaAbc1 is a rust-pathotype specific HR-mediator. Down-regulating TaAbc1 reduced HR but not the overall resistance level in Suwon11 to CYR23, suggesting TaAbc1 was involved in HR against stripe rust, but overall host resistance is not HR-dependent.     

High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1

Several new races of the stripe rust pathogen have become frequent throughout the wheat growing regions of the United States since 2000. These new races are virulent to most of the wheat seedling resistance genes limiting the resistance sources that can be used to combat this pathogen. High-temperature adult-plant (HTAP) stripe rust resistance has proven to be more durable than seedling resistance due to its non-race-specific nature, but its use is limited by the lack of mapping information. We report here the identification of a new HTAP resistance gene from Triticum turgidum ssp. dicoccoides (DIC) designated as Yr36. Lines carrying this gene were susceptible to almost all the stripe rust pathogen races tested at the seedling stage but showed adult-plant resistance to the prevalent races in California when tested at high diurnal temperatures. Isogenic lines for this gene were developed by six backcross generations. Field tests in two locations showed increased levels of field resistance to stripe rust and increased yields in isogenic lines carrying the Yr36 gene compared to those without the gene. Recombinant substitution lines of chromosome 6B from DIC in the isogenic background of durum cv. Langdon were used to map the Yr36 gene on the short arm of chromosome 6B completely linked to Xbarc101, and within a 2-cM interval defined by PCR-based markers Xucw71 and Xbarc136. Flanking locus Xucw71 is also closely linked to the grain protein content locus Gpc-B1 (0.3-cM). Marker-assisted selection strategies are presented to improve stripe rust resistance and simultaneously select for high or low Gpc-B1 alleles.     

Suppression of NB-LRR genes by miRNAs promotes nitrogen-fixing nodule development in Medicago truncatula

Plant genomes contain two major classes of innate immune receptors to recognize different pathogens. The pattern recognition receptors perceive conserved pathogen-associated molecular patterns and the resistance genes with nucleotide-binding (NB) and leucine-rich repeat (LRR) domains recognize specific pathogen effectors. The precise regulation of resistance genes is important since the unregulated expression of NB-LRR genes can inhibit growth and may result in autoimmunity in the absence of pathogen infection. It was shown that a subset of miRNAs could target NB-LRR genes and act as an important regulator of plant immunity in the absence of pathogens. Plants not only interact with pathogens, but they can also establish symbiotic interactions with microbes. Nitrogen-fixing symbiotic interaction and nodule formation of legumes may also require the suppression of host defence to prevent immune responses. We found that upon symbiotic interactions, miRNAs repressing NB-LRR expression are upregulated in the developing nodules of Medicago truncatula. Furthermore, we show that the suppression of the activity of the NB-LRR genes targeted by these miRNAs is important during nodule development. Our results suggest that the downregulation of NB-LRR resistance genes in the developing nodule produces a suitable niche that facilitates bacterial colonization and the development of an N-fixing nodule.     

Interspecies gene transfer provides soybean resistance to a fungal pathogen

Fungal pathogens pose a major challenge to global crop production. Crop varieties that resist disease present the best defence and offer an alternative to chemical fungicides. Exploiting durable nonhost resistance (NHR) for crop protection often requires identification and transfer of NHR‐linked genes to the target crop. Here, we identify genes associated with NHR of Arabidopsis thaliana to Phakopsora pachyrhizi, the causative agent of the devastating fungal disease called Asian soybean rust. We transfer selected Arabidopsis NHR‐linked genes to the soybean host and discover enhanced resistance to rust disease in some transgenic soybean lines in the greenhouse. Interspecies NHR gene transfer thus presents a promising strategy for genetically engineered control of crop diseases.     

Mutation to Wider Virulence in Puccinia graminis f. sp. tritici: Evidence for the Existence of Loci Which Allow the Fungus To Overcome Several Host Stem Rust Resistance Genes Simultaneously

Mutants of Puccinia graminis f. sp. tritici were obtained which were able to overcome simultaneously several host stem rust resistance (Sr) genes effective against the wild-type culture. These results suggest that, in addition to those Psr loci which relate specifically to host Sr genes in a “gene for gene” manner, one or more general loci may be present in this pathogen. The product(s) of these general genes may be necessary for the expression of various host Sr genes. The evolution of a super race capable of overcoming many Sr genes for resistance seems likely, as such a pathogen would not have to give up the many proteins predicted by the gene-for-gene relationship. Moreover, it appears that specificity in the wheat rust system is more complicated than suggested by the gene-for-gene concept.