Functional Divergence of Two Secreted Immune Proteases of Tomato
Ilyas, M. ; Hörger, A.C. ; Bozkurt, T.O. ; Burg, H.A. van den; Kaschani, F. ; Kaiser, M. ; Belhaj, K. ; Smoker, M. ; Joosten, M. ; Kamoun, S. ; Hoorn, R.A.L. van der - \ 2015
Current Biology 25 (2015)17. - ISSN 0960-9822 - p. 2300 - 2306.
cf-2-dependent disease resistance - pathogen effectors - transcription factors - provides insights - genome sequence - plant-pathogens - gene - defense - target - specialization
Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor [ 1, 2, 3 and 4]. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.
Stepwise artificial evolution of a plant disease resistance gene
Harris, J.H. ; Slootweg, E.J. ; Goverse, A. ; Baulcombe, D.C. - \ 2013
Proceedings of the National Academy of Sciences of the United States of America 110 (2013)52. - ISSN 0027-8424 - p. 21189 - 21194.
nb-lrr protein - tobacco-mosaic-virus - rich repeat domains - cell-death - arabidopsis-thaliana - immune receptors - coiled-coil - hypersensitive response - mediated resistance - pathogen effectors
Genes encoding plant nucleotide-binding leucine-rich repeat (NB-LRR) proteins confer dominant resistance to diverse pathogens. The wild-type potato NB-LRR protein Rx confers resistance against a single strain of potato virus X (PVX), whereas LRR mutants protect against both a second PVX strain and the distantly related poplar mosaic virus (PopMV). In one of the Rx mutants there was a cost to the broad-spectrum resistance because the response to PopMV was transformed from a mild disease on plants carrying wild-type Rx to a trailing necrosis that killed the plant. To explore the use of secondary mutagenesis to eliminate this cost of broad-spectrum resistance, we performed random mutagenesis of the N-terminal domains of this broad-recognition version of Rx and isolated four mutants with a stronger response against the PopMV coat protein due to enhanced activation sensitivity. These mutations are located close to the nucleotide-binding pocket, a highly conserved structure that likely controls the “switch” between active and inactive NB-LRR conformations. Stable transgenic plants expressing one of these versions of Rx are resistant to the strains of PVX and the PopMV that previously caused trailing necrosis. We conclude from this work that artificial evolution of NB-LRR disease resistance genes in crops can be enhanced by modification of both activation and recognition phases, to both accentuate the positive and eliminate the negative aspects of disease resistance.
Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat induced point mutations
Rouxel, T. ; Grandaubert, J. ; Hane, J.K. ; Hoede, C. ; Wouw, A. ; Couloux, A. ; Dominguez, V. ; Anthouard, V. ; Bally, P. ; Bourras, S. ; Cozijnsen, A.J. ; Ciuffetti, L.M. ; Degrave, A. ; Dilmaghani, A. ; Duret, L. ; Fudal, L. ; Goodwin, S.B. ; Gout, L. ; Glaser, N. ; Linglin, J. ; Kema, G.H.J. ; Lapalu, N. ; Lawrence, C.B. ; May, K. ; Meyer, M. ; Ollivier, B. ; Poulain, J. ; Schoch, C.L. ; Simon, A. ; Spatafora, J.W. ; Stachowiak, A. ; Turgeon, B.G. ; Tyler, B.M. ; Vincent, D. ; Weissenbach, J. ; Amselem, J. ; Quesneville, H. ; Oliver, R.P. ; Wincker, P. ; Balesdent, M.H. ; Howlett, B.J. - \ 2011
Nature Communications 2 (2011). - ISSN 2041-1723 - p. 202 - 202.
transposable elements - molecular evolution - pathogen effectors - brassica-napus - gene-transfer - oilseed rape - stem canker - avirulence - plant - fungal
Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints