Dataset Information

Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.

ABSTRACT: Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen Phytophthora infestans A subclass that includes the conserved effector PcF from Phytophthora cactorum activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to P. infestans and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (G-LecRK) locus in the wild potato Solanum microdontum subsp. gigantophyllum. The G-LecRK locus displays a high diversity in Solanum host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in P. infestans is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants.IMPORTANCE Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of Phytophthora small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen Phytophthora infestans and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized Phytophthora proteins are expected to contribute to disease resistance breeding in potato.

SUBMITTER: Lin X

PROVIDER: S-EPMC7327169 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.

Lin Xiao X Wang Shumei S de Rond Laura L Bertolin Nicoletta N Wouters Roland H M RHM Wouters Doret D Domazakis Emmanouil E Bitew Mulusew Kassa MK Win Joe J Dong Suomeng S Visser Richard G F RGF Birch Paul P Kamoun Sophien S Vleeshouwers Vivianne G A A VGAA

mBio 20200630 3

Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen <i>Phytophth ...[more]

PMID: 32605983

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Project description:BACKGROUND:Retrotransposons comprise a ubiquitous and abundant class of eukaryotic transposable elements. All members of this class rely on reverse transcriptase activity to produce a DNA copy of the element from the RNA template. However, other activities of the retrotransposon-encoded polyprotein may differ between diverse retrotransposons. The polyprotein domains corresponding to each of these activities may have their own evolutionary history independent from that of the reverse transcriptase, thus underlying the modular view on the evolution of retrotransposons. Furthermore, some transposable elements can independently evolve similar domain architectures by acquiring functionally similar but phylogenetically distinct modules. This convergent evolution of retrotransposons may ultimately suggest similar regulatory pathways underlying the lifecycle of the elements. RESULTS:Here, we provide new examples of the convergent evolution of retrotransposons of species from two unrelated taxa: green plants and parasitic protozoan oomycetes. In the present study we first analyzed the available genomic sequences of oomycete species and characterized two groups of Ty3/Gypsy long terminal repeat retrotransposons, namely Chronos and Archon, and a subgroup of L1 non-long terminal repeat retrotransposons. The results demonstrated that the retroelements from these three groups each have independently acquired plant-related ribonuclease H domains. This process closely resembles the evolution of retrotransposons in the genomes of green plants. In addition, we showed that Chronos elements captured a chromodomain, mimicking the process of chromodomain acquisition by Chromoviruses, another group of Ty3/Gypsy retrotransposons of plants, fungi, and vertebrates. CONCLUSIONS:Repeated and strikingly similar acquisitions of ribonuclease H domains and chromodomains by different retrotransposon groups from unrelated taxa indicate similar selection pressure acting on these elements. Thus, there are some major trends in the evolution of the structural composition of retrotransposons, and characterizing these trends may enhance the current understanding of the retrotransposon life cycle.

Project description:Legionella pneumophila governs its interactions with host cells by secreting >300 different "effector" proteins. Some of these effectors contain eukaryotic domains such as the RCC1 (regulator of chromosome condensation 1) repeats promoting the activation of the small GTPase Ran. In this report, we reveal a conserved pattern of L. pneumophila RCC1 repeat genes, which are distributed in two main clusters of strains. Accordingly, strain Philadelphia-1 contains two RCC1 genes implicated in bacterial virulence, legG1 (Legionella eukaryotic gene 1), and ppgA, while strain Paris contains only one, pieG The RCC1 repeat effectors localize to different cellular compartments and bind distinct components of the Ran GTPase cycle, including Ran modulators and the small GTPase itself, and yet they all promote the activation of Ran. The pieG gene spans the corresponding open reading frames of legG1 and a separate adjacent upstream gene, lpg1975 legG1 and lpg1975 are fused upon addition of a single nucleotide to encode a protein that adopts the binding specificity of PieG. Thus, a point mutation in pieG splits the gene, altering the effector target. These results indicate that divergent evolution of RCC1 repeat effectors defines the Ran GTPase cycle targets and that modulation of different components of the cycle might fine-tune Ran activation during Legionella infection.IMPORTANCE Legionella pneumophila is a ubiquitous environmental bacterium which, upon inhalation, causes a life-threatening pneumonia termed Legionnaires' disease. The opportunistic pathogen grows in amoebae and macrophages by employing a "type IV" secretion system, which secretes more than 300 different "effector" proteins into the host cell, where they subvert pivotal processes. The function of many of these effector proteins is unknown, and their evolution has not been studied. L. pneumophila RCC1 repeat effectors target the small GTPase Ran, a molecular switch implicated in different cellular processes such as nucleocytoplasmic transport and microtubule cytoskeleton dynamics. We provide evidence that one or more RCC1 repeat genes are distributed in two main clusters of L. pneumophila strains and have divergently evolved to target different components of the Ran GTPase activation cycle at different subcellular sites. Thus, L. pneumophila employs a sophisticated strategy to subvert host cell Ran GTPase during infection.

Dataset Information

Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.

Publications

Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants.

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