The Ins and Outs of Rust Haustoria

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Garnica, Diana P ^a   Nemri, Adnane ^b   Upadhyaya, Narayana M ^b   Rathjen, John P ^a   Dodds, Peter N ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ARTICLE; CONFOCAL MICROSCOPY; CYTOPLASM; DNA POLYMORPHISM; FUNGAL VIRULENCE; FUNGUS; HAUSTORIUM; LIFESTYLE MODIFICATION; METABOLISM; NONHUMAN; BASIDIOMYCETES; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE;

BASIDIOMYCOTA; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES;

EID: 84907587719     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004329     Document Type: Article

References (34)

1. Mendgen K, Struck C, Voegele RT, Hahn M, (2000) Biotrophy and rust haustoria. Physiol Mol Plant Pathol 56: 141–145.
2. Voegele RT, Struck C, Hahn M, Mendgen K, (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci U S A 98: 8133–8138.
3. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG, (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18: 243–256.
4. Voegele RT, Mendgen K, (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159: 93–100.
5. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S, (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15: 483–492.
6. Rafiqi M, Ellis JG, Ludowici VA, Hardham AR, Dodds PN, (2012) Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr Opin Plant Biol 15: 477–482.
7. Littlefield LJ, Heath MC (1979) Ultrastructure of rust fungi. New York: Academic Press.
8. Hahn M, Mendgen K, (1997) Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact 10: 427–437.
9. Struck C, Ernst M, Hahn M, (2002) Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol 3: 23–30.
10. Struck C, Mueller E, Martin H, Lohaus G, (2004) The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol Plant Pathol 5: 183–189.
11. Garnica DP, Upadhyaya NM, Dodds PN, Rathjen JP, (2013) Strategies for Wheat Stripe Rust Pathogenicity Identified by Transcriptome Sequencing. Plos One 8: e67150.
12. Link TI, Lang P, Scheffler BE, Duke MV, Graham MA, et al. (2013) The haustorial transcriptomes of Uromyces appendiculatus and Phakopsora pachyrhizi and their candidate effector families. Mol Plant Pathol 15: 379–393.
13. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108: 9166–9171.
14. Upadhyaya NM, Garnica DP, Karaoglu H, Nemri A, Sperschneider J, et al. (2014) Comparative genomics of Australian stem rust (Puccinia graminis f. sp. tritici) isolates reveals extensive polymorphism in candidate effector genes. Front Plant Sci In press.
15. Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X, et al. (2011) Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS ONE 6: e24230.
16. Zheng W, Huang L, Huang J, Wang X, Chen X, et al. (2013) High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat Commun 4: 2673.
17. Nemri A, Saunders DGO, Anderson C, Upadhyaya NM, Win J, et al. (2014) The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Front Plant Sci 5: 98.
18. Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, et al. (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact 18: 1130–1139.
19. Pretsch K, Kemen A, Kemen E, Geiger M, Mendgen K, et al. (2013) The rust transferred proteins-a new family of effector proteins exhibiting protease inhibitor function. Mol Plant Pathol 14: 96–107.
20. Kemen E, Kemen A, Ehlers A, Voegele R, Mendgen K, (2013) A novel structural effector from rust fungi is capable of fibril formation. Plant J 75: 767–780.
21. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG, (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755–768.
22. Barrett LG, Thrall PH, Dodds PN, van der Merwe M, Linde CC, et al. (2009) Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Mol Biol Evol 26: 2499–2513.
23. Rafiqi M, Gan P, Ravensdale M, Lawrence G, Ellis J, et al. (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22: 2017–2032.
24. Ve T, Williams SJ, Catanzariti AM, Rafiqi M, Rahman M, et al. (2013) Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity. Proc Nat Acad Sci U S A 110: 17594–17599.
25. Saunders DGO, Win J, Cano LM, Szabo LJ, Kamoun S, et al. (2012) Using Hierarchical Clustering of Secreted Protein Families to Classify and Rank Candidate Effectors of Rust Fungi. PLoS ONE 7: e29847.
26. Cantu D, Segovia V, Maclean D, Bayles R, Chen X, et al. (2013) Genome analyses of the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics 14: 270.
27. Link TI, Voegele RT, (2008) Secreted proteins of Uromyces fabae: similarities and stage specificity. Mol Plant Pathol 9: 59–66.
28. Sperschneider J, Ying E, Dodds PN, Upadhyaya NM, Gardiner DM, et al. (2014) Adaptative Evolution in Expanded Pathogen-Associated, Effector-like Gene Families in the Stem Rust Fungus. Front Plant Sci 5: 372.
29. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Nat Acad Sci U S A 103: 8888–8893.
30. Wang CIA, Guncar G, Forwood JK, Teh T, Catanzariti AM, et al. (2007) Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19: 2898–2912.
31. Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, et al. (2010) The AvrM Effector from Flax Rust Has a Structured C-Terminal Domain and Interacts Directly with the M Resistance Protein. Mol Plant Microbe Interact 23: 49–57.
32. Bruce M, Neugebauer KA, Joly DL, Migeon P, Cuomo CA, et al. (2014) Using transcription of six Puccinia triticina races to identify the effective secretome during infection of wheat. Front Plant Sci 4: 520.
33. Upadhyaya NM, Mago R, Staskawicz BJ, Ayliffe MA, Ellis JG, et al. (2014) A Bacterial Type III Secretion Assay for Delivery of Fungal Effector Proteins into Wheat. Mol Plant Microbe Interact 27: 255–264.
34. Garnica DP, Rathjen JP, (2014) Purification of fungal haustoria from infected plant tissue by flow cytometry. Methods Mol Biol 1127: 103–110.