Dataset Information

Expression of Castanea crenata Allene Oxide Synthase in Arabidopsis Improves the Defense to Phytophthora cinnamomi.

ABSTRACT: Allene oxide synthase (AOS) is a key enzyme of the jasmonic acid (JA) signaling pathway. The AOS gene was previously found to be upregulated in an Asian chestnut species resistant to infection by the oomycete Phytophthora cinnamomi (Castanea crenata), while lower expression values were detected in the susceptible European chestnut (Castanea sativa). Here, we report a genetic and functional characterization of the C. crenata AOS (CcAOS) upon its heterologous gene expression in a susceptible ecotype of Arabidopsis thaliana, which contains a single AOS gene. It was found that Arabidopsis plants expressing CcAOS delay pathogen progression and exhibit more vigorous growth in its presence. They also show upregulation of jasmonic acid and salicylic acid-related genes. As in its native species, heterologous CcAOS localized to plastids, as revealed by confocal imaging of the CcAOS-eGFP fusion protein in transgenic Arabidopsis roots. This observation was confirmed upon transient expression in Nicotiana benthamiana leaf epidermal cells. To further confirm a specific role of CcAOS in the defense mechanism against the pathogen, we performed crosses between transgenic CcAOS plants and an infertile Arabidopsis AOS knockout mutant line. It was found that plants expressing CcAOS exhibit normal growth, remain infertile but are significantly more tolerant to the pathogen than wild type plants. Together, our results indicate that CcAOS is an important player in plant defense responses against oomycete infection and that its expression in susceptible varieties may be a valuable tool to mitigate biotic stress responses.

SUBMITTER: Serrazina S

PROVIDER: S-EPMC7917121 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Expression of Castanea crenata Allene Oxide Synthase in Arabidopsis Improves the Defense to Phytophthora cinnamomi.

Serrazina Susana S Machado Helena H Costa Rita Lourenço RL Duque Paula P Malhó Rui R

Frontiers in plant science 20210215

Allene oxide synthase (AOS) is a key enzyme of the jasmonic acid (JA) signaling pathway. The AOS gene was previously found to be upregulated in an Asian chestnut species resistant to infection by the oomycete Phytophthora cinnamomi (Castanea crenata), while lower expression values were detected in the susceptible European chestnut (Castanea sativa). Here, we report a genetic and functional characterization of the C. crenata AOS (CcAOS) upon its heterologous gen ...[more]

PMID: 33659016

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Project description:Phytophthora cinnamomi Rands devastates forest species worldwide, causing significant ecological and economic impacts. The European chestnut (Castanea sativa) is susceptible to this hemibiotrophic oomycete, whereas the Asian chestnuts (Castanea crenata and Castanea mollissima) are resistant and have been successfully used as resistance donors in breeding programs. The molecular mechanisms underlying the different disease outcomes among chestnut species are a key foundation for developing science-based control strategies. However, these are still poorly understood. Dual RNA sequencing was performed in C. sativa and C. crenata roots inoculated with P. cinnamomi. The studied time points represent the pathogen's hemibiotrophic lifestyle previously described at the cellular level. Phytophthora cinnamomi expressed several genes related to pathogenicity in both chestnut species, such as cell wall-degrading enzymes, host nutrient uptake transporters, and effectors. However, the expression of effectors related to the modulation of host programmed cell death (elicitins and NLPs) and sporulation-related genes was higher in the susceptible chestnut. After pathogen inoculation, 1,556 and 488 genes were differentially expressed by C. crenata and C. sativa, respectively. The most significant transcriptional changes occur at 2 h after inoculation (hai) in C. sativa and 48 hai in C. crenata. Nevertheless, C. crenata induced more defense-related genes, indicating that the resistant response to P. cinnamomi is controlled by multiple loci, including several pattern recognition receptors, genes involved in the phenylpropanoid, salicylic acid and ethylene/jasmonic acid pathways, and antifungal genes. Importantly, these results validate previously observed cellular responses for C. crenata. Collectively, this study provides a comprehensive time-resolved description of the chestnut-P. cinnamomi dynamic, revealing new insights into susceptible and resistant host responses and important pathogen strategies involved in disease development.

Project description:Phytophthora cinnamomi is one of the most devastating plant pathogens in the world. It infects close to 5000 species of plants, including many of importance in agriculture, forestry and horticulture. The inadvertent introduction of P. cinnamomi into natural ecosystems, including a number of recognized Global Biodiversity Hotspots, has had disastrous consequences for the environment and the biodiversity of flora and fauna. The genus Phytophthora belongs to the Class Oomycetes, a group of fungus-like organisms that initiate plant disease through the production of motile zoospores. Disease control is difficult in agricultural and forestry situations and even more challenging in natural ecosystems as a result of the scale of the problem and the limited range of effective chemical inhibitors. The development of sustainable control measures for the future management of P. cinnamomi requires a comprehensive understanding of the cellular and molecular basis of pathogen development and pathogenicity. The application of next-generation sequencing technologies to generate genomic and transcriptomic data promises to underpin a new era in P. cinnamomi research and discovery. The aim of this review is to integrate bioinformatic analyses of P. cinnamomi sequence data with current knowledge of the cellular and molecular basis of P. cinnamomi growth, development and plant infection. The goal is to provide a framework for future research by highlighting potential pathogenicity genes, shedding light on their possible functions and identifying suitable targets for future control measures.TaxonomyPhytophthora cinnamomi Rands; Kingdom Chromista; Phylum Oomycota or Pseudofungi; Class Oomycetes; Order Peronosporales; Family Peronosporaceae; genus Phytophthora.Host rangeInfects about 5000 species of plants, including 4000 Australian native species. Host plants important for agriculture and forestry include avocado, chestnut, macadamia, oak, peach and pineapple.Disease symptomsA root pathogen which causes rotting of fine and fibrous roots, but which can also cause stem cankers. Root damage may inhibit water movement from roots to shoots, leading to dieback of young shoots. USEFUL WEBSITES: http://fungidb.org/fungidb/; http://genome.jgi.doe.gov/Phyci1/Phyci1.home.html; http://www.ncbi.nlm.nih.gov/assembly/GCA_001314365.1; http://www.ncbi.nlm.nih.gov/assembly/GCA_001314505.1.

Project description:Seaweed extracts are important sources of plant biostimulants that boost agricultural productivity to meet current world demand. The ability of seaweed extracts based on either of the Phaeophyceaean species Ascophyllum nodosum or Durvillaea potatorum to enhance plant growth or suppress plant disease have recently been shown. However, very limited information is available on the mechanisms of suppression of plant disease by such extracts. In addition, there is no information on the ability of a combination of extracts from A. nodosum and D. potatorum to suppress a plant pathogen or to induce plant defense. The present study has explored the transcriptome, using RNA-seq, of Arabidopsis thaliana following treatment with extracts from the two species, or a mixture of both, prior to inoculation with the root pathogen Phytophthora cinnamomi. Following inoculation, five time points (0-24 h post-inoculation) that represented early stages in the interaction of the pathogen with its host were assessed for each treatment and compared with their respective water controls. Wide scale transcriptome reprogramming occurred predominantly related to phytohormone biosynthesis and signaling, changes in metabolic processes and cell wall biosynthesis, there was a broad induction of proteolysis pathways, a respiratory burst and numerous defense-related responses were induced. The induction by each seaweed extract of defense-related genes coincident with the time of inoculation showed that the plants were primed for defense prior to infection. Each seaweed extract acted differently in inducing plant defense-related genes. However, major systemic acquired resistance (SAR)-related genes as well as salicylic acid-regulated marker genes (PR1, PR5, and NPR1) and auxin associated genes were found to be commonly up-regulated compared with the controls following treatment with each seaweed extract. Moreover, each seaweed extract suppressed P. cinnamomi growth within the roots of inoculated A. thaliana by the early induction of defense pathways and likely through ROS-based signaling pathways that were linked to production of ROS. Collectively, the RNA-seq transcriptome analysis revealed the induction by seaweed extracts of suites of genes that are associated with direct or indirect plant defense in addition to responses that require cellular energy to maintain plant growth during biotic stress.

Dataset Information

Expression of Castanea crenata Allene Oxide Synthase in Arabidopsis Improves the Defense to Phytophthora cinnamomi.

Publications

Expression of <i>Castanea crenata</i> Allene Oxide Synthase in Arabidopsis Improves the Defense to <i>Phytophthora cinnamomi</i>.

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