Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif

Autor: Kyle Fletcher, Brigitte Maisonneuve, Kelsey J. Wood, Sanye Naqvi, Richard W Michelmore, Tina Khuu, Ayumi Gothberg, Mathieu A. Pel, Juliana Gil, Jennifer Kopetzky, Archana Pandya, Munir Nur, Dasan Gann, Chi Zhang, Kim Lakeman
Přispěvatelé: Banfield, Mark J, Genome Center [UC Davis], University of California [Davis] (UC Davis), University of California-University of California, University of California [Irvine] (UCI), University of California, Wageningen University and Research [Wageningen] (WUR), Enza Zaden, Partenaires INRAE, Génétique et Amélioration des Fruits et Légumes (GAFL), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Department of Biological and Agricultural Engineering [Davis], NSF Graduate Research Fellowship and a USDA Fellowship #2018-67011-28053 to KW and the NSF/USDA AFRI Microbial Sequencing Programaward #2009-65109-05925 to RWM.
Rok vydání: 2020
Předmět:
0106 biological sciences
Leaves
Plant Science
Biochemistry
01 natural sciences
Database and Informatics Methods
2.1 Biological and endogenous factors
2.2 Factors relating to the physical environment
Biology (General)
Post-Translational Modification
Aetiology
Plant Proteins
Disease Resistance
2. Zero hunger
Oomycete
Genetics
0303 health sciences
Bremia lactucae
Genome
Cell Death
Effector
Plant Anatomy
Eukaryota
Lettuce
Infectious Diseases
Oomycetes
Cell Processes
Medical Microbiology
Proteome
Host-Pathogen Interactions
Sequence motif
Infection
Sequence Analysis
Signal Peptides
Research Article
Biotechnology
Signal peptide
Architecture domain
QH301-705.5
Bioinformatics
Phytophthora infestans
Immunology
Plant Pathogens
Plant disease resistance
Biology
Protein Sorting Signals
Research and Analysis Methods
Microbiology
Vaccine Related
03 medical and health sciences
Sequence Motif Analysis
Virology
[SDV.BV]Life Sciences [q-bio]/Vegetal Biology
Amino Acid Sequence
Molecular Biology Techniques
Molecular Biology
030304 developmental biology
Plant Diseases
Organisms
Fungi
Biology and Life Sciences
Proteins
Cell Biology
RC581-607
Plant Pathology
biology.organism_classification
Downy Mildew
Parasitology
Immunologic diseases. Allergy
Sequence Alignment
Cloning
010606 plant biology & botany
Zdroj: PLoS pathogens, vol 16, iss 10
PLoS Pathogens
PLoS Pathogens, Public Library of Science, 2020, 16 (10), pp.e1009012. ⟨10.1371/journal.ppat.1009012⟩
PLoS Pathogens, Vol 16, Iss 10, p e1009012 (2020)
ISSN: 1553-7366
1553-7374
DOI: 10.1371/journal.ppat.1009012⟩
Popis: Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens.
Author summary There is a molecular battle that takes place during infection of plants and animals by pathogens. Some of the weapons in the pathogen’s arsenal are known as “effectors;” these are secreted proteins that enter host cells to alter their physiology and suppress the immune system. Effectors can also be a liability for pathogens because potential hosts have evolved ways to recognize these effectors, triggering a defense response leading to localized cell death, preventing the spread of the pathogen. Here we computationally predicted effectors encoded in the genome of Bremia lactucae, the pathogen causing the downy mildew disease of lettuce and tested 21 of these proteins in the lab to see what effects they would have on the host plant. Five effectors were demonstrated to suppress the basal immune system of lettuce. Eleven effectors caused programmed cell death when introduced to certain lettuce lines, which indicates recognition of these proteins by the host immune system. In addition to contributing to our understanding of the mechanisms of pathogenesis, this study of effectors facilitates breeding for disease resistant lettuce, which will decrease agricultural reliance on fungicides.
Databáze: OpenAIRE