Establishing compatibility between plants and obligate biotrophic pathogens

Current Opinion in Plant Biology

Volumn 6, Issue 4, 2003, Pages 320-326

  Panstruga, Ralph ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; PERONOSPORA FARINOSA;

EID: 0041569855     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(03)00043-8     Document Type: Review

References (56)

1. Perfect SE, Green JR: Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2001, 2:101-108.
2. Mendgen K, Hahn M: Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 2002, 7:352-356.
3. Heath MC, Skalamera D: Cellular interactions between plants and biotrophic fungal parasites. In Advances in Botanical Research Incorporating Advances in Plant Pathology, Vol 24. Edited by Tommerup IC, Andrews JH. London: Academic Press Ltd; 1997:195-225.
4. Szabo LJ, Bushnell WR: Hidden robbers: the role of fungal haustoria in parasitism of plants. Proc Natl Acad Sci USA 2001, 98:7654-7655.
5. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR: Random GFP: cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 2000, 97:3718-3723.
6. Koh S, Ehrhardt D, André A, Somerville S: Subcellular dynamics in the early stages of the compatible interaction between Arabidopsis thaliana and the powdery mildew Erysiphe cichoracearum. Abstract 7-33, XIII International Conference on Arabidopsis Research, June 28-July 2 2002, Seville, Spain. (http://www.Arabidopsis2002.com/)
7. Spencer-Phillips PTN: Function of fungal haustoria in epiphytic and endophytic infections. In Advances in Botanical Research Advances in Plant Pathology, Vol 24. Edited by Tommerup IC, Andrews JH. London: Academic Press Ltd; 1997:309-333.
8. Mendgen K, Struck C, Voegele RT, Hahn M: Biotrophy and rust haustoria. Physiol Mol Plant Pathol 2000, 56:141-145.
9. Hahn M, Mendgen K: Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact 1997, 10:427-437.
10. Hahn M, Neef U, Struck C, Gottfert M, Mendgen K: A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 1997, 10:438-445.
11. Voegele RT, Struck C, Hahn M, Mendgen K: The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 2001, 98:8133-8138. For the first time, this study provides convincing evidence that the uptake of host sugars in plant-biotrophic interactions is likely to occur via fungal haustoria. The authors describe the molecular analysis of HXT1, which encodes a bean rust fungus hexose transporter. They demonstrate the haustorium-specific expression of the HXT1 protein by northern blot analysis and immunocytology. Transport specificity of HXT1p upon heterologous expression of HXT1 was convincingly demonstrated in two different organisms (Saccharomyces cerevisiae and Xenopus oocytes) by two distinct methods (competition experiments and electrophysiological studies).
12. Struck C, Ernst M, Hahn M: Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol 2002, 3:23-30.
13. +-ATPase from the biotrophic rust fungus Uromyces fabae: molecular characterization of the gene (PMA1) and functional expression of the enzyme in yeast. Mol Plant Microbe Interact 1998, 11:458-465.
14. Shirasu K, Nielsen K, Piffanelli P, Oliver R, Schulze-Lefert P: Cell-autonomous complementation of mlo resistance using a biolistic transient expression system. Plant J 1999, 17:293-299.
15. Sohn J, Voegele RT, Mendgen T, Hahn M: High level activation of vitamin B1 biosynthesis genes in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact 2000, 13:629-636.
16. Thara VK, Fellers JP, Zhou JM: In planta induced genes of Puccinia triticina. Mol Plant Pathol 2003, 4:51-56. This study provides the second example (following that in U. fabae [9]) of the analysis of genes of an obligate biotrophic pathogen that are induced in planta. The availability of a second dataset (although small at present) will allow the first comparative analysis of genes that are induced in planta in different biotrophic phytopathogens. It will be interesting to broaden this comparison and to include non-ascomycetes, such as powdery or downy mildews, for which equivalent data are currently lacking.
17. Bushnell WR, Rowell JB: Suppressors of defense reactions: a model for roles in specificity. Phytopathology 1981, 71:1012-1014.
18. Heath MC: Cellular interactions between biotrophic fungal pathogens and host or nonhost plants. Can J Plant Pathol 2002, 24:259-264.
19. Mellersh DG, Heath MC: Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 2001, 13:413-424. The authors describe their beautiful cytological study, which provided two major novel findings. First, they provide evidence that cell-wall-associated host defense responses (e.g. the generation of reactive oxygen species) depend on adhesion between the plant cell wall and the PM via cytoplasmic strands (known as Hechtian strands). Second, analysis by sucrose-induced plasmolysis of the state of Hechtian strands during fungal penetration revealed that rust fungi (in contrast to powdery mildews) might have evolved a means to decrease PM-cell-wall adhesion during compatible interactions.
20. Wäspi U, Schweizer P, Dudler R: Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew. Plant Cell 2001, 13:153-161. This paper has two aspects of outstanding interest. First, the authors describe a study that provides direct evidence for reversible pathogen-mediated defense suppression in the course of a compatible wheat-powdery mildew interaction. Second, it demonstrates the potency of a bacterial elicitor to override installed fungal defense suppression effectively, possibly by synergism with mildew-derived elicitors.
21. Lyngkjaer MF, Carver TLW: Induced accessibility and inaccessibility to Blumeria graminis f. sp. hordei in barley epidermal cells attacked by a compatible isolate. Physiol Mol Plant Pathol 1999, 55:151-162.
22. Lyngkjaer HF, Carver TLW: Modification of mlo5 resistance to Blumeria graminis attack in barley as a consequence of induced accessibility and inaccessibility. Physiol Mol Plant Pathol 1999, 55:163-174.
23. Lyngkjaer MF, Carver TLW, Zeyen RJ: Virulent Blumeria graminis infection induces penetration susceptibility and suppresses race-specific hypersensitive resistance against avirulent attack in Mla1-barley. Physiol Mol Plant Pathol 2001, 59:243-256.
24. Kunoh H, Hayashimoto A, Harui M, Ishizaki H: Induced susceptibility and enhanced inaccessibility at the cellular level in barley coleoptiles. I. The significance of timing fungal invasion. Physiol Plant Pathol 1985, 27:43-54.
25. Gregersen PL, Thordal-Christensen H, Forster H, Collinge DB: Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f. sp. hordei (syn. Erysiphe graminis f. sp. hordei). Physiol Mol Plant Pathol 1997, 51:85-97.
26. Ayliffe MA, Roberts JK, Mitchell HJ, Zhang R, Lawrence GJ, Ellis JG, Pryor TJ: A plant gene up-regulated at rust infection sites. Plant Physiol 2002, 129:169-180. To my knowledge, this is the first report to describe a host gene that is locally upregulated at compatible biotroph infection sites. Upregulation of fis1 homologues upon rust infection was found to be conserved in maize and barley. The protein encoded by this gene is involved in proline metabolism and might play an indirect role in the suppression of defense and/or cell death.
27. Rai VK: Role of amino acids in plant responses to stresses. Biol Plant 2002, 45:481-487.
28. Scholes JD, Rolfe SA: Photosynthesis in localized regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta 1996, 199:573-582.
29. Abramovitch RB, Kim YJ, Chen SR, Dickman MB, Martin GB: Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 2003, 22:60-69.
30. Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R: Overexpression of bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J 2003, 33:425-434.
31. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J et al.: The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 1997, 88:695-705.
32. Tiwari KR, Penner GA, Warkentin TD: Identification of coupling and repulsion phase RAPD markers for powdery mildew resistance gene er-1 in pea. Genome 1998, 41:440-444.
33. Ciccarese F, Amenduni M, Ambrico A, Cirulli M: The resistance to Oidium lycopersici conferred by ol-2 gene in tomato. Acta Physiol Plant 2000, 22:266.
34. Vogel J, Somerville S: Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc Natl Acad Sci USA 2000, 97:1897-1902.
35. Vogel JP, Raab TK, Schiff C, Somerville SC: PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 2002, 14:2095-2106. This study provides the first example of the molecular isolation of a gene that encodes a presumptive host compatibility factor. The gene was isolated by a targeted search for host mutants that had enhanced pathogen (in this case, powdery mildew) resistance that was not associated with a constitutive activation of host defense responses [34]. The exact role of the encoded protein, PMR6, during a compatible interaction remains speculative, but map-based cloning of further candidate compatibility genes promises to shed more light on the basis of biotrophic interactions.
36. Li ZK, Sanchez A, Angeles E, Singh S, Domingo J, Huang N, Khush GS: Are the dominant and recessive plant disease resistance genes similar? A case study of rice R genes and Xanthomonas oryzae pv. oryzae races. Genetics 2001, 159:757-765.
37. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y: Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA 2002, 99:2404-2409.
38. Miklas PN, Larsen RC, Riley R, Kelly JD: Potential marker-assisted selection for bc-1(2) resistance to bean common mosaic potyvirus in common bean. Euphytica 2000, 116:211-219.
39. Ehlers JD, Matthews WC, Hall AE, Roberts PA: Inheritance of a broad-based form of root-knot nematode resistance in cowpea. Crop Sci 2000, 40:611-618.
40. Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P: Topology, subcellular localization, and sequence diversity of the Mlo family in plants. J Biol Chem 1999, 274:34993-35004.
41. Panstruga R, Schulze-Lefert P: Live and let live: insights into powdery mildew disease and resistance. Mol Plant Pathol 2002, 3:495-502.
42. Panstruga R, Schulze-Lefert P: Corruption of host seven-transmembrane proteins by pathogenic microbes: a common theme in animals and plants? Microbes Infect 2003, in press.
43. 2+-triggered binding of CaM to MLO enhances the penetration success of the powdery mildew fungus.
44. Mithöfer A, Ebel J, Bhagwat AA, Boller T, Neuhaus-Url G: Transgenic aequorin monitors cytosolic calcium transients in soybean cells challenged with beta-glucan or chitin elicitors. Planta 1999, 207:566-574.
45. Blume B, Nürnberger T, Nass N, Scheel D: Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 2000, 12:1425-1440.
46. Romeis T, Ludwig AA, Martin R, Jones JDG: Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 2001, 20:5556-5567.
47. Skou JP: Callose formation responsible for the powdery mildew resistance in barley with genes in the ml-o locus. Phytopathol Z - J Phytopathol 1982, 104:90-95.
48. Idnurm A, Howlett BJ: Pathogenicity genes of phytopathogenic fungi. Mol Plant Pathol 2001, 2:241-255.
49. Kahmann R, Basse C: Fungal gene expression during pathogenesis-related development and host plant colonization. Curr Opin Microbiol 2001, 4:374-380.
50. Chaure P, Gurr SJ, Spanu P: Stable transformation of Erysiphe graminis, an obligate biotrophic pathogen of barley. Nat Biotechnol 2000, 18:205-207.
51. Schillberg S, Tiburzy R, Fischer R: Transient transformation of the rust fungus Puccinia graminis f. sp. tritici. Mol Gen Genet 2000, 262:911-915.
52. Arabi MIE, Jawhar M: The ability of barley powdery mildew to grow in vitro. J Phytopathol - Phytopathol Z 2002, 150:305-307.
53. Fasters MK, Daniels U, Moerschbacher BM: A simple and reliable method for growing the wheat stem rust fungus, Puccinia graminis f. sp. tritici, in liquid culture. Physiol Mol Plant Pathol 1993, 42:259-265.
54. Hall JL, Williams LE: Assimilate transport and portioning in biotrophic interactions. Aust J Plant Physiol 2000, 27:549-560.
55. Kehr J: High resolution spatial analysis of plant systems. Curr Opin Plant Biol 2001, 4:197-201.
56. Nakazono M, Qiu F, Borsuk LA, Schnable PS: Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes differently expressed in epidermal cells or vascular tissues of maize. Plant Cell 2003, 15:583-596. Laser-capture microdissection is a novel and powerful technique that enables high-throughput single-cell sampling of particular plant cell types (e.g. pathogen-infected epidermal and/or mesophyll cells). Single cells are captured from frozen tissue sections by means of a laser beam. This technique might pave the way for a thorough molecular analysis of changes that take place in individual pathogen-infected cells. In this study, laser-capture microdissection was used to study the expression profile of particular maize cell types.