scholarly journals Cause and Effectors: Whole-Genome Comparisons Reveal Shared but Rapidly Evolving Effector Sets among Host-Specific Plant-Castrating Fungi

mBio ◽  
2019 ◽  
Vol 10 (6) ◽  
Author(s):  
William C. Beckerson ◽  
Ricardo C. Rodríguez de la Vega ◽  
Fanny E. Hartmann ◽  
Marine Duhamel ◽  
Tatiana Giraud ◽  
...  

ABSTRACT Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi (Microbotryum), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed in planta; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all Microbotryum species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses. IMPORTANCE Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons.

2015 ◽  
Vol 84 (3) ◽  
pp. 217-235 ◽  
Author(s):  
Camille Meslin ◽  
Michel Laurin ◽  
Isabelle Callebaut ◽  
Xavier Druart ◽  
Philippe Monget

The seminal fluid is a complex substance composed of a variety of secreted proteins and has been shown to play an important role in the fertilisation process in mammals and also in Drosophila. Several genes under positive selection have been documented in some rodents and primates. Our study documents this phenomenon in several other mammalian taxa. We study the evolution of genes that encode for 20 proteins that are quantitatively predominant in the seminal fluid of at least one out of seven domestic animal species. We analyse the amino acid composition of these proteins for positive selection and for the presence of pseudogenes. Genes that disappeared through pseudogenisation include KLK2 in cattle, horse and mice. Traces of positive selection are found in seven genes. The identified amino acids are located in regions exposed to the protein surface, suggesting a role in the interaction of gametes, with possible impact on the process of speciation. Moreover, we found no evidence that the predominance of proteins in seminal fluid and their mode of evolution are correlated, and the uncoupled patterns of change suggest that this result is not due solely to lack of statistical power.


2017 ◽  
Author(s):  
Gabriel Schweizer ◽  
Karin Münch ◽  
Gertrud Mannhaupt ◽  
Jan Schirawski ◽  
Regine Kahmann ◽  
...  

AbstractPlants and fungi display a broad range of interactions in natural and agricultural ecosystems ranging from symbiosis to parasitism. These ecological interactions result in coevolution between genes belonging to different partners. A well-understood example are secreted fungal effector proteins and their host targets, which play an important role in pathogenic interactions. Biotrophic smut fungi (Basidiomycota) are well-suited to investigate the evolution of plant pathogens, because several reference genomes and genetic tools are available for these species. Here, we used the genomes of Sporisorium reilianum f. sp. zeae and S. reilianum f. sp. reilianum, two closely related formae speciales infecting maize and sorghum, respectively, together with the genomes of Ustilago hordei, Ustilago maydis and Sporisorium scitamineum to identify and characterize genes displaying signatures of positive selection. We identified 154 gene families having undergone positive selection during species divergence in at least one lineage, among which 77% were identified in the two investigated formae speciales of S. reilianum. Remarkably, only 29% of positively selected genes encode predicted secreted proteins. We assessed the contribution to virulence of nine of these candidate effector genes in S. reilianum f. sp. zeae by deleting individual genes, including a homologue of the effector gene pit2 previously characterized in U. maydis. Only the pit2 deletion mutant was found to be strongly reduced in virulence. Additional experiments are required to understand the molecular mechanisms underlying the selection forces acting on the other candidate effector genes, as well as the large fraction of positively selected genes encoding predicted cytoplasmic proteins.


2012 ◽  
Vol 25 (7) ◽  
pp. 877-888 ◽  
Author(s):  
David A. Baltrus ◽  
Marc T. Nishimura ◽  
Kevin M. Dougherty ◽  
Surojit Biswas ◽  
M. Shahid Mukhtar ◽  
...  

Biotrophic phytopathogens are typically limited to their adapted host range. In recent decades, investigations have teased apart the general molecular basis of intraspecific variation for innate immunity of plants, typically involving receptor proteins that enable perception of pathogen-associated molecular patterns or avirulence elicitors from the pathogen as triggers for defense induction. However, general consensus concerning evolutionary and molecular factors that alter host range across closely related phytopathogen isolates has been more elusive. Here, through genome comparisons and genetic manipulations, we investigate the underlying mechanisms that structure host range across closely related strains of Pseudomonas syringae isolated from different legume hosts. Although type III secretion-independent virulence factors are conserved across these three strains, we find that the presence of two genes encoding type III effectors (hopC1 and hopM1) and the absence of another (avrB2) potentially contribute to host range differences between pathovars glycinea and phaseolicola. These findings reinforce the idea that a complex genetic basis underlies host range evolution in plant pathogens. This complexity is present even in host–microbe interactions featuring relatively little divergence among both hosts and their adapted pathogens.


2018 ◽  
Author(s):  
Jasper R.L. Depotter ◽  
Fabian van Beveren ◽  
Luis Rodriguez-Moreno ◽  
Grardy C.M. van den Berg ◽  
Thomas A. Wood ◽  
...  

AbstractAllopolyploidization, genome duplication through interspecific hybridization, is an important evolutionary mechanism that can enable organisms to adapt to environmental changes or stresses. The increased adaptive potential of allopolyploids can be particularly relevant for plant pathogens in their ongoing quest for host immune response evasion. To this end, plant pathogens secrete a plethora of molecules that enable host colonization. Allodiploidization has resulted in the new plant pathogen Verticillium longisporum that infects different hosts than haploid Verticillium species. To reveal the impact of allodiploidization on plant pathogen evolution, we studied the genome and transcriptome dynamics of V. longisporum using next-generation sequencing. V. longisporum genome evolution is characterized by extensive chromosomal rearrangements, between as well as within parental chromosome sets, leading to a mosaic genome structure. In comparison to haploid Verticillium species, V. longisporum genes display stronger signs of positive selection. The expression patterns of the two sub-genomes show remarkable resemblance, suggesting that the parental gene expression patterns homogenized upon hybridization. Moreover, whereas V. longisporum genes encoding secreted proteins frequently display differential expression between the parental sub-genomes in culture medium, expression patterns homogenize upon plant colonization. Collectively, our results illustrate of the adaptive potential of allodiploidy mediated by the interplay of two sub-genomes.Author summaryHybridization followed by whole-genome duplication, so-called allopolyploidization, provides genomic flexibility that is beneficial for survival under stressful conditions or invasiveness into new habitats. Allopolyploidization has mainly been studied in plants, but also occurs in other organisms, including fungi. Verticillium longisporum, an emerging fungal pathogen on brassicaceous plants, arose by allodiploidization between two Verticillium spp. We used comparative genomics to reveal the plastic nature of the V. longisporum genomes, showing that parental chromosome sets recombined extensively, resulting in a mosaic genome pattern. Furthermore, we show that non-synonymous substitutions frequently occurred in V. longisporum. Moreover, we reveal that expression patterns of genes encoding secreted proteins homogenized between the V. longisporum sub-genomes upon plant colonization. In conclusion, our results illustrate the large adaptive potential upon genome hybridization for fungi mediated by genomic plasticity and interaction between sub-genomes.


2012 ◽  
Vol 2012 ◽  
pp. 1-7 ◽  
Author(s):  
Phil Grayson ◽  
Alberto Civetta

Most genes linked to male reproductive function have been known to evolve rapidly among species and to show signatures of positive selection. Different male species-specific reproductive strategies have been proposed to underlie positive selection, such as sperm competitive advantage and control over females postmating physiology. However, an underexplored aspect potentially affecting male reproductive gene evolution in mammals is the effect of gene duplications. Here we analyze the molecular evolution of members of the izumo gene family in mammals, a family of four genes mostly expressed in the sperm with known and potential roles in sperm-egg fusion. We confirm a previously reported bout of selection for izumo1 and establish that the bout of selection is restricted to the diversification of species of the superorder Laurasiatheria. None of the izumo genes showed evidence of positive selection in Glires (Rodentia and Lagomorpha), and in the case of the non-testes-specific izumo4, rapid evolution was driven by relaxed selection. We detected evidence of positive selection for izumo3 among Primates. Interestingly, positively selected sites include several serine residues suggesting modifications in protein function and/or localization among Primates. Our results suggest that positive selection is driven by aspects related to species-specific adaptations to fertilization rather than sexual selection.


Horticulturae ◽  
2021 ◽  
Vol 7 (2) ◽  
pp. 16
Author(s):  
Heba Hassan ◽  
Aishah Alatawi ◽  
Awatif Abdulmajeed ◽  
Manal Emam ◽  
Hemmat Khattab

Photosystem II is extremely susceptible to environmental alterations, particularly high temperatures. The maintenance of an efficient photosynthetic system under stress conditions is one of the main issues for plants to attain their required energy. Nowadays, searching for stress alleviators is the main goal for maintaining photosynthetic system productivity and, thereby, crop yield under global climate change. Potassium silicate (K2SiO3, 1.5 mM) and silicon dioxide nanoparticles (SiO2NPs, 1.66 mM) were used to mitigate the negative impacts of heat stress (45 °C, 5 h) on wheat (Triticum aestivum L.) cv. (Shandawelly) seedlings. The results showed that K2SiO3 and SiO2NPs diminished leaf rolling symptoms and electrolyte leakage (EL) of heat-stressed wheat leaves. Furthermore, the maximum quantum yield of photosystem II (Fv/Fm) and the performance index (PIabs), as well as the photosynthetic pigments and organic solutes including soluble sugars, sucrose, and proline accumulation, were increased in K2SiO3 and SiO2NPs stressed leaves. At the molecular level, RT-PCR analysis showed that K2SiO3 and SiO2NPs treatments stimulated the overexpression of PsbH, PsbB, and PsbD genes. Notably, this investigation indicated that K2SiO3 was more effective in improving wheat thermotolerance compared to SiO2NPs. The application of K2SiO3 and SiO2NPs may be one of the proposed approaches to improve crop growth and productivity to tolerate climatic change.


2019 ◽  
Vol 11 (3) ◽  
pp. 954-969 ◽  
Author(s):  
Yann Dussert ◽  
Isabelle D Mazet ◽  
Carole Couture ◽  
Jérôme Gouzy ◽  
Marie-Christine Piron ◽  
...  

Abstract Downy mildews are obligate biotrophic oomycete pathogens that cause devastating plant diseases on economically important crops. Plasmopara viticola is the causal agent of grapevine downy mildew, a major disease in vineyards worldwide. We sequenced the genome of Pl. viticola with PacBio long reads and obtained a new 92.94 Mb assembly with high contiguity (359 scaffolds for a N50 of 706.5 kb) due to a better resolution of repeat regions. This assembly presented a high level of gene completeness, recovering 1,592 genes encoding secreted proteins involved in plant–pathogen interactions. Plasmopara viticola had a two-speed genome architecture, with secreted protein-encoding genes preferentially located in gene-sparse, repeat-rich regions and evolving rapidly, as indicated by pairwise dN/dS values. We also used short reads to assemble the genome of Plasmopara muralis, a closely related species infecting grape ivy (Parthenocissus tricuspidata). The lineage-specific proteins identified by comparative genomics analysis included a large proportion of RxLR cytoplasmic effectors and, more generally, genes with high dN/dS values. We identified 270 candidate genes under positive selection, including several genes encoding transporters and components of the RNA machinery potentially involved in host specialization. Finally, the Pl. viticola genome assembly generated here will allow the development of robust population genomics approaches for investigating the mechanisms involved in adaptation to biotic and abiotic selective pressures in this species.


2012 ◽  
Vol 25 (5) ◽  
pp. 697-708 ◽  
Author(s):  
Adriana Cabral ◽  
Stan Oome ◽  
Nick Sander ◽  
Isabell Küfner ◽  
Thorsten Nürnberger ◽  
...  

The genome of the downy mildew pathogen Hyaloperonospora arabidopsidis encodes necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP). Although NLP are widely distributed in eukaryotic and prokaryotic plant pathogens, it was surprising to find these proteins in the obligate biotrophic oomycete H. arabidopsidis. Therefore, we analyzed the H. arabidopsidis NLP (HaNLP) family and identified 12 HaNLP genes and 15 pseudogenes. Most of the 27 genes form an H. arabidopsidis–specific cluster when compared with other oomycete NLP genes, suggesting this class of effectors has recently expanded in H. arabidopsidis. HaNLP transcripts were mainly detected during early infection stages. Agrobacterium tumefaciens–mediated transient expression and infiltration of recombinant NLP into tobacco and Arabidopsis leaves revealed that all HaNLP tested are noncytotoxic proteins. Even HaNLP3, which is most similar to necrosis-inducing NLP proteins of other oomycetes and which contains all amino acids that are critical for necrosis-inducing activity, did not induce necrosis. Chimeras constructed between HaNLP3 and the necrosis-inducing PsojNIP protein demonstrated that most of the HaNLP3 protein is functionally equivalent to PsojNIP, except for an exposed domain that prevents necrosis induction. The early expression and species-specific expansion of the HaNLP genes is suggestive of an alternative function of noncytolytic NLP proteins during biotrophic infection of plants.


2021 ◽  
Author(s):  
Thomas O. Auer ◽  
Raquel Álvarez-Ocaña ◽  
Steeve Cruchet ◽  
Richard Benton ◽  
J. Roman Arguello

Animals sample their chemical environment using sensory neurons that express diverse chemosensory receptors, which trigger responses when they bind environmental molecules. In addition to modifications in the ligand binding properties of receptors, chemosensory receptor evolution is characterized by copy number changes, often resulting in large gene family size differences between species. Though chemosensory receptor expansions and contractions are frequently described, it is unknown how this is accompanied by changes in the neural circuitry in which they are expressed. Among Drosophila's chemosensory receptor families, the Odorant receptors (Ors) are ideal for addressing this question because, other than an essential co-receptor (Orco), a large majority of Ors are uniquely expressed in single olfactory sensory neuron (OSN) populations. Between-species changes in Or copy number, therefore, may indicate diversification or reduction of peripheral sensory neuron populations. To test this possibility, we focused on a rapidly duplicated/deleted Or subfamily - named Or67a - within Drosophila melanogaster and its most closely-related sister species (D. simulans, D. sechellia, and D. mauritiana). Evolutionary genetic analyses and in vivo physiological assays demonstrate that the common ancestor of these four species possessed three Or67a paralogs that had already diverged adaptively in their odor-evoked responses. Following the group's speciation events, two Or67a paralogs were independently lost in D. melanogaster and D. sechellia, with positive selection continuing to act on the intact genes. Instead of the expected singular expression of each of the functionally diverged Ors in different neurons, we found that the three D. simulans Or67a paralogs are co-expressed in the same cells. Thus, while neuroanatomy is conserved between these species, independent selection on co-expressed receptors has contributed to species-specific peripheral coding of olfactory information. This work reveals a model of adaptive change previously not considered for olfactory evolution and raises the possibility that similar processes may be operating among the largely uninvestigated cases of Or co-expression.


2003 ◽  
pp. 329-338
Author(s):  
Mary N. Burtnick ◽  
Paul J. Brett ◽  
Donald E. Woods

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