Hessian fly avirulence gene loss-of-function defeats plant resistance without compromising the larva's ability to induce a gall tissue

Entomologia Experimentalis et Applicata

Volumn 145, Issue 3, 2012, Pages 238-249

  Harris, Marion ^a   Freeman, T P ^a   Anderson, K M ^a   Harmon, J P ^a   Moore, J A ^a   Payne, S A ^a   Rohfritsch, O ^b   Stuart, J J ^c  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b CNRS   (France)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Cecidomyiidae; Diptera; Gall maker; Mechanisms; Plant immunity; R Avr interactions; Resistance gene; SEM; TEM; Triticum aestivum

Indexed keywords

COLONIZATION; FLY; GALL; GENOTYPE; IMMUNITY; LARVA; PATHOGEN; RESISTANCE MANAGEMENT; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; VIRULENCE; WHEAT;

CECIDOMYIIDAE; DIPTERA; MAYETIOLA DESTRUCTOR; TRITICUM AESTIVUM;

EID: 84868214335     PISSN: 00138703     EISSN: 15707458     Source Type: Journal    
DOI: 10.1111/eea.12010     Document Type: Article

References (48)

1. Agrios G (1997) Plant Pathology. Academic Press, San Diego, CA, USA.
2. An Q, Huckelhoven R, Kogel KH & van Bel AJE (2006) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiology 8: 1009-1019.
3. Anderson KG & Harris MO (2006) Does R gene resistance allow wheat to prevent plant growth effects associated with Hessian fly (Diptera: Cecidomyiidae) attack? Journal of Economic Entomology 99: 1842-1853.
4. Anderson KG & Harris MO (2008) Leaf growth signals the onset of effective plant resistance against Hessian fly larvae. Entomologia Experimentalis et Applicata 128: 184-195.
5. Anderson KM, Kang Q, Reber J & Harris MO (2011) No fitness cost for wheat's H gene-mediated resistance to Hessian fly (Diptera: Cecidomyiidae). Journal of Economic Entomology 104: 1393-1405.
6. Bent AF & Mackey D (2007) Elicitors, effectors and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45: 399-436.
7. Bird DM, Williamson VM, Abad PM, McCarter J & Danchin EFJ (2009) The genomes of root-knot nematodes. Annual Review of Phytopathology 47: 333-351.
8. Bronner R (1992) The role of the nutritive tissue in the nutrition of cynipids and cecidomyiids. Biology of Insect-Induced Galls (ed. by J Shorthouse & O Rohfritsch), pp. 118-141. Oxford University Press, New York, NY, USA.
9. Chen MS, Liu X, Yang Z, Zhao H, Shukle RH et al. (2010) Unusual conservation among genes encoding small secreted salivary gland proteins from a gall midge. BMC Evolutionary Biology 10: 296.
10. Dangl JL & McDowell JM (2006) Two modes of pathogen recognition by plants. Proceedings of the National Academy of Sciences of the USA 103: 8575-8576.
11. Dodds PN, Lawrence GJ, Catanzarti A, The T, Wang CA et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust Avirulence genes. Proceedings of the National Academy of Sciences of the USA 103: 8888-8893.
12. Fernandes GW & Negreiro D (2001) The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecological Entomology 26: 46-55.
13. Flor HH (1955) Host-parasite interactions in flax - its genetics and other implications. Phytopathology 45: 680-685.
14. Gagné RJ (1989) The Plant-Feeding Gall Midges of North America. Cornell University Press, Ithaca, NY, USA.
15. Gallun RL (1977) The genetic bases of Hessian fly epidemics. Annals of the New York Academy of Sciences 287: 223-229.
16. Garavaglia BS, Thomas L, Gottig N, Dunger G, Garofalo CG et al. (2010) A eukaryotic-acquired gene by biotrophic phytopathogen allows prolonged survival on the host by counteracting the shut-down of plant photosynthesis. PLoS ONE 5: e8950.
17. Giovanini MP, Puthoff DP, Nemacheck JA, Mittapalli O, Saltzmann KD et al. (2006) Gene-for-gene defense of wheat against the Hessian fly lacks a classical oxidative burst. Molecular Plant Microbe Interactions 19: 1023-1033.
18. Göhre V & Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annual Review of Phytopathology 46: 189-215.
19. Harris MO, Stuart JJ, Mohan M, Nair S, Lamb RJ & Rohfritsch O (2003) Grasses and gall midges: plant defense and insect adaptation. Annual Review of Entomology 45: 549-577.
20. Harris MO, Anderson KG, Anderson KM & Kanno H (2006a) Proximate cues for reduced oviposition on wheat plants attacked by conspecific larvae. Environmental Entomology 35: 83-93.
21. Harris MO, Freeman TP, Rohfritsch O, Anderson KG, Payne SA & Moore JA (2006b) Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Annals of the Entomological Society of America 99: 305-316.
22. Harris MO, Freeman TP, Anderson KG, Moore JA, Payne SA et al. (2010) H gene-mediated resistance to Hessian fly exhibits features of penetration resistance to fungi. Phytopathology 100: 279-289.
23. Hatchett JH, Kreitner GL & Elzinga RJ (1990) Larval mouthparts and feeding mechanism of the Hessian fly (Diptera: Cecidomyiidae). Annals of the Entomological Society of America 83: 1137-1147.
24. Hogenhout SA, van der Hoorn RAL, Teruchi R & Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Molecular Plant-Microbe Interactions 22: 115-122.
25. Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Review of Phytopathology 45: 101-127.
26. Kaloshian I & Walling LL (2005) Hemipterans as plant pathogens. Annual Review of Phytopathology 43: 491-521.
27. Kosma DK, Nemacheck JA, Jenks MA & Williams CE (2010) Changes in properties of wheat leaf cuticle during interactions with Hessian fly. Plant Journal 63: 31-43.
28. 14C-markieter in die Galle. Biochimie und Physiologie der Pflanzen 165: 445-456.
29. Larson KC & Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88: 15-21.
30. Leach JE, Vera Cruz CM, Bai J & Leung H (2001) Pathogen fitness penalty as a predictor for durability of disease resistance genes. Annual Review of Phytopathology 39: 187-224.
31. Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyan S et al. (2010) Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiology 152: 985-999.
32. Patterson FL, Maas FB, Foster JE, Ratcliffe RH, Cambron S et al. (1994) Registration of eight Hessian fly resistant common winter wheat germplasm lines. Crop Science 34: 315-316.
33. Refai FY, Miller BS, Jones ET & Wolfe JE (1956) The feeding mechanism of Hessian fly larvae. Journal of Economic Entomology 49: 182-185.
34. Rohfritsch O (1992) Patterns in gall development. Biology of Insect-Induced Galls (ed. by J Shorthouse & O Rohfritsch), pp. 102-117. Oxford University Press, New York, NY, USA.
35. SAS Institute (2012) JMP Version 9. SAS Institute, Cary, NC, USA.
36. Schouten HJ, Krens FA & Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Reports 7: 750-753.
37. Shukle RH, Subramanyam S, Saltzmann KA & Williams CE (2010) Ultrastructural changes in the midguts of Hessian fly larvae feeding on resistant wheat. Journal of Insect Physiology 56: 754-760.
38. Smith EM (2005) Plant Resistance to Arthropods - Molecular and Conventional Approaches. Springer, Dordrecht, The Netherlands.
39. Stergiopoulos I & de Wit PJGM (2009) Fungal effector proteins. Annual Review of Phytopathology 47: 233-263.
40. Stone GN & Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18: 512-522.
41. Stuart JJ, Chen MS, Shukle R & Harris MO (2012) Gall midges (Hessian flies) as plant pathogens. Annual Review of Phytopathology 50: 339-357.
42. Subramanyam S, Smith DF, Clemens JC, Webb MA, Sardesai N & Williams CE (2008) Functional characterization of Hfr-1, a high mannose N-glycan-specific wheat lectin induced by Hessian fly larvae. Plant Physiology 147: 1412-1426.
43. Vleeshouwers VG, Raffaele S, Vossen J, Champouret N, Olivia R et al. (2011) Understanding and exploiting late blight resistance in the age of effectors. Annual Review of Phytopathology 49: 1-25.
44. Weis AE, Walton R & Crego CL (1988) Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology 33: 467-486.
45. Williams CE, Nemacheck JA, Shukle JT, Subramanyan S, Saltzmann KD & Shukle RH (2011) Induced epidermal permeability modulates resistance and susceptibility of wheat seedlings to herbivory by Hessian fly. Journal of Experimental Botany 62: 4521-4531.
46. Xu SS, Chu CG, Harris MO & Williams CE (2011) Comparative analysis of genetic background in eight near-isogenic wheat lines with different H genes conferring resistance to Hessian fly. Genome 54: 81-89.
47. Yencho G, Cohen M & Byrne P (2000) Applications of tagging and mapping insect resistance loci in plants. Annual Review of Entomology 45: 393-422.
48. Zhang H, Anderson KM, Stuart JJ, Cambron S & Harris MO (2011) A reproductive fitness cost associated with Hessian fly (Diptera: Cecidomyiidae) virulence to gene-for-gene resistance. Journal of Economic Entomology 104: 1055-1064.