Bioinformatic Characterisation of the Effector Repertoire of the Strawberry Pathogen Phytophthora Cactorum

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2018 Oct 3

PMID 30278048

Citations 20

Authors

Andrew D Armitage

Erik Lysoe

Charlotte F Nellist

Laura A Lewis

Liliana M Cano

Richard J Harrison

May B Brurberg

Affiliations

Soon will be listed here.

Abstract

The oomycete pathogen Phytophthora cactorum causes crown rot, a major disease of cultivated strawberry. We report the draft genome of P. cactorum isolate 10300, isolated from symptomatic Fragaria x ananassa tissue. Our analysis revealed that there are a large number of genes encoding putative secreted effectors in the genome, including nearly 200 RxLR domain containing effectors, 77 Crinklers (CRN) grouped into 38 families, and numerous apoplastic effectors, such as phytotoxins (PcF proteins) and necrosis inducing proteins. As in other Phytophthora species, the genomic environment of many RxLR and CRN genes differed from core eukaryotic genes, a hallmark of the two-speed genome. We found genes homologous to known Phytophthora infestans avirulence genes including Avr1, Avr3b, Avr4, Avrblb1 and AvrSmira2 indicating effector sequence conservation between Phytophthora species of clade 1a and clade 1c. The reported P. cactorum genome sequence and associated annotations represent a comprehensive resource for avirulence gene discovery in other Phytophthora species from clade 1 and, will facilitate effector informed breeding strategies in other crops.

Citing Articles

Functional genomics identifies a small secreted protein that plays a role during the biotrophic to necrotrophic shift in the root rot pathogen .

Coles D, Bithell S, Jeffries T, Cuddy W, Plett J Front Plant Sci. 2024; 15:1439020.

PMID: 39224851 PMC: 11366588. DOI: 10.3389/fpls.2024.1439020.

Genomic and transcriptomic analyses of reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles.

Shands A, Xu G, Belisle R, Seifbarghi S, Jackson N, Bombarely A Front Microbiol. 2024; 15:1341803.

PMID: 39211322 PMC: 11357935. DOI: 10.3389/fmicb.2024.1341803.

Transcriptome analysis of infecting strawberry identified RXLR effectors that induce cell death when transiently expressed in .

Ghimire B, Gogoi A, Poudel M, Stensvand A, Brurberg M Front Plant Sci. 2024; 15:1379970.

PMID: 38855473 PMC: 11157022. DOI: 10.3389/fpls.2024.1379970.

Genome analysis of strains associated with crown- and leather-rot in strawberry.

Gogoi A, Rossmann S, Lysoe E, Stensvand A, Brurberg M Front Microbiol. 2023; 14:1214924.

PMID: 37465018 PMC: 10351607. DOI: 10.3389/fmicb.2023.1214924.

Comparative Transcriptome Analysis Reveals Novel Candidate Resistance Genes Involved in Defence against in Strawberry.

Gogoi A, Lysoe E, Eikemo H, Stensvand A, Davik J, Brurberg M Int J Mol Sci. 2023; 24(13).

PMID: 37446029 PMC: 10341869. DOI: 10.3390/ijms241310851.

References

Fry W, Birch P, Judelson H, Grunwald N, Danies G, Everts K . Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen. Phytopathology. 2015; 105(7):966-81. DOI: 10.1094/PHYTO-01-15-0005-FI. View

Jones P, Binns D, Chang H, Fraser M, Li W, McAnulla C . InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014; 30(9):1236-40. PMC: 3998142. DOI: 10.1093/bioinformatics/btu031. View

Kamoun S . Molecular genetics of pathogenic oomycetes. Eukaryot Cell. 2003; 2(2):191-9. PMC: 154851. DOI: 10.1128/EC.2.2.191-199.2003. View

Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, Canut H . The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog. 2011; 7(3):e1001327. PMC: 3068997. DOI: 10.1371/journal.ppat.1001327. View

Torto T, Li S, Styer A, Huitema E, Testa A, Gow N . EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res. 2003; 13(7):1675-85. PMC: 403741. DOI: 10.1101/gr.910003. View

Hirakawa H, Shirasawa K, Kosugi S, Tashiro K, Nakayama S, Yamada M . Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res. 2013; 21(2):169-81. PMC: 3989489. DOI: 10.1093/dnares/dst049. View

Sperisen P, Schmid C, Bucher P, Zilian O . Stealth proteins: in silico identification of a novel protein family rendering bacterial pathogens invisible to host immune defense. PLoS Comput Biol. 2005; 1(6):e63. PMC: 1285062. DOI: 10.1371/journal.pcbi.0010063. View

Winnenburg R, Baldwin T, Urban M, Rawlings C, Kohler J, Hammond-Kosack K . PHI-base: a new database for pathogen host interactions. Nucleic Acids Res. 2005; 34(Database issue):D459-64. PMC: 1347410. DOI: 10.1093/nar/gkj047. View

Kourelis J, van der Hoorn R . Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function. Plant Cell. 2018; 30(2):285-299. PMC: 5868693. DOI: 10.1105/tpc.17.00579. View

10.

Du Y, Mpina M, Birch P, Bouwmeester K, Govers F . Phytophthora infestans RXLR Effector AVR1 Interacts with Exocyst Component Sec5 to Manipulate Plant Immunity. Plant Physiol. 2015; 169(3):1975-90. PMC: 4634092. DOI: 10.1104/pp.15.01169. View

11.

Brunner F, Rosahl S, Lee J, Rudd J, Geiler C, Kauppinen S . Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J. 2002; 21(24):6681-8. PMC: 139088. DOI: 10.1093/emboj/cdf667. View

12.

Kong G, Zhao Y, Jing M, Huang J, Yang J, Xia Y . The Activation of Phytophthora Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b. PLoS Pathog. 2015; 11(8):e1005139. PMC: 4552650. DOI: 10.1371/journal.ppat.1005139. View

13.

Orsomando G, Brunetti L, Pucci K, Ruggeri B, Ruggieri S . Comparative structural and functional characterization of putative protein effectors belonging to the PcF toxin family from Phytophthora spp. Protein Sci. 2011; 20(12):2047-59. PMC: 3302648. DOI: 10.1002/pro.742. View

14.

Fankhauser N, Maser P . Identification of GPI anchor attachment signals by a Kohonen self-organizing map. Bioinformatics. 2005; 21(9):1846-52. DOI: 10.1093/bioinformatics/bti299. View

15.

Testa A, Hane J, Ellwood S, Oliver R . CodingQuarry: highly accurate hidden Markov model gene prediction in fungal genomes using RNA-seq transcripts. BMC Genomics. 2015; 16:170. PMC: 4363200. DOI: 10.1186/s12864-015-1344-4. View

16.

Davik J, Sargent D, Brurberg M, Lien S, Kent M, Alsheikh M . A ddRAD Based Linkage Map of the Cultivated Strawberry, Fragaria xananassa. PLoS One. 2015; 10(9):e0137746. PMC: 4580419. DOI: 10.1371/journal.pone.0137746. View

17.

Chen X, Zhang B, Xing Y, Li Q, Li Y, Tong Y . Transcriptomic analysis of the phytopathogenic oomycete Phytophthora cactorum provides insights into infection-related effectors. BMC Genomics. 2014; 15:980. PMC: 4289400. DOI: 10.1186/1471-2164-15-980. View

18.

Thines M, Kamoun S . Oomycete-plant coevolution: recent advances and future prospects. Curr Opin Plant Biol. 2010; 13(4):427-33. DOI: 10.1016/j.pbi.2010.04.001. View

19.

Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C, Heupink A . Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol Plant Microbe Interact. 2009; 22(12):1535-45. DOI: 10.1094/MPMI-22-12-1535. View

20.

Nellist C, Vickerstaff R, Sobczyk M, Marina-Montes C, Wilson F, Simpson D . Quantitative trait loci controlling resistance in the cultivated octoploid strawberry ( ). Hortic Res. 2019; 6:60. PMC: 6491645. DOI: 10.1038/s41438-019-0136-4. View