Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 7-Day Trial for You or Your Team.

Learn More →

Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes

Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic... [Plant Signaling & Behavior 3:4, 251-253; April 2008]; ©2008 Landes Bioscience Article Addendum Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Joe Win and Sophien Kamoun* Sainsbury Laboratory; Norwich, United Kingdom Key words: plant-microbe interactions, effectors, gene families, positive selection Plant pathogenic microbes deliver effector proteins inside is similar in sequence and position and is functionally interchangeable host cells to modulate plant defense circuitry and enable parasitic with the plasmodial host translocation (HT)/Pexel motif that func- colonization. As genome sequences from plant pathogens become tions in delivery of parasite proteins into the cytoplasm of red blood available, genome‑wide evolutionary analyses will shed light on cells of mammalian hosts. Also, the RXLR motif is not required how pathogen effector genes evolved and adapted to the cellular for the effector activities of P. infestans AVR3a when this protein is environment of their host plants. In the August 2007 issue of Plant directly expressed inside plant cells consistent with a role in targeting Cell, we described adaptive evolution (positive selection) in the rather than effector activity. Altogether these findings led to the cytoplasmic RXLR effectors of three recently sequenced oomycete view that oomycete RXLR effectors are modular proteins with two plant pathogens. Here, we summarize our findings and describe major functional domains. While the N-terminal domain encom- additional data that further validate our approach. passing the signal peptide and RXLR leader functions in secretion and targeting, the remaining C-terminal region carries the effector activity A diverse number of plant pathogens, including bacteria, oomycetes, and operates inside plant cells. fungi and nematodes, deliver effector proteins inside host cells to Ab Initio Identification of RXLR Effectors: Rationale 1-8 modulate plant defense circuitry and enable parasitic colonization. Because these so-called cytoplasmic effectors function inside plant In the initial part of our study, we aimed to develop a method cells and produce phenotypes that extend to plant cells and tissues, for ab initio identification of RXLR effector genes in the sequenced their genes are expected to be the direct target of the evolutionary genomes. Our approach was to first determine the defining features forces that drive the antagonistic interplay between pathogen and of validated oomycete RXLR effectors in order to develop a robust set 9,10 host. In a study published in the August 2007 issue of Plant Cell, of data mining criteria. We therefore, developed an unbiased list of 43 we and our collaborators examined the extent to which positive selec- oomycete RXLR proteins consisting of validated effectors and their tion (adaptive evolution) has shaped the evolution of the cytoplasmic closest homologs. Also, to objectively address the extent to which effectors of three recently sequenced oomycete plant pathogens the tetrapeptide RXLR sequence is overrepresented and positionally Phytophthora sojae, Phytophthora ramorum, and Hyaloperonospora para- constrained in Phytophthora, we examined the distribution of the sitica (Genome Sequencing Center at Washington University). RXLR sequence in the proteomes of these species compared to 46 other eukaryotes. These analyses indicated that the RXLR sequence is Oomycete RXLR Effectors are Modular Proteins significantly overrepresented and positionally constrained in the secre- Four oomycete Avr proteins have been described in the past three tomes of Phytophthora relative to other eukaryotes and formed the years and were found to contain a secretory signal peptide followed basis of the ab initio algorithm. by a conserved domain featuring the motif RXLR, flanked by a high 1,3,12 Ab Initio Identification of RXLR Effectors: Further Validation frequency of acidic (D/E) residues. The RXLR motif defines a domain that functions in delivery of effector proteins into host cells. It Since the publication of our study, two new avirulence genes, PsAvr1a and PsAvr3a, were reported from Phytophthora sojae by Mark *Correspondence to: Sophien Kamoun; Sainsbury Laboratory; John Innes Center; Gijzen laboratory, London, Ontario, Canada (GenBank accessions Colney Lane; Norwich NR4 7UH United Kingdom; Tel: +44.1603.450410; Email: ABQ81647 and ABO47652). Interestingly, PsAvr1a and PsAvr3a [email protected] fulfill our criteria for RXLR effectors and were identified by our Submitted: 10/12/07; Accepted: 10/17/07 ab initio algorithm (Supplemental Table S2 of the Win et al. paper). In Table 1, we list the features of PsAvr1a and PsAvr3a, and their 34 Previously published online as a Plant Signaling & Behavior E-publication: www.landesbioscience.com/journals/psb/article/5182 homologous genes. The mean values for protein size, position of RXLR, and position of EER sequence obtained with this new set of Addendum to: Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, validated RXLR effectors are remarkably similar to those we reported Ammar R, Staskawicz BJ, Kamoun S. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 2007; earlier. 19:2349–69; PMID: 17675403; DoI: 10.1105/tpc.107.051037. www.landesbioscience.com Plant Signaling & Behavior 251 ©2008 Landes Bioscience. Do not distribute. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Table 1 New validated RXLR effectors. The new validated effectors are based on two Phytophthora sojae avirulence proteins, PsAvr1a and PsAvr3a, reported by the laboratory of Mark Gijzen, London, Ontario, Canada ‑4 and their homologs (E value <10 ) a b Description Accession Species Evidence Length Signal SignalP SignalP RXLR EER c c Peptide v2.0 HMM v2.0 NN Position position Length score score ABQ81647, Avirulence effector protein PsAvr3a Ps_scaffold_80_R245 P. sojae Avr effector 111 20 0.998 0.910 43 ABo47652, Avirulence effector protein PsAvr1a Ps_scaffold_1058_F4 P. sojae Avr effector 121 25 0.999 0.813 54 64 Unknown protein similar to PsAvr1a Pr_scaffold_103_F268 P. ramorum homolog 121 21 0.994 0.850 54 Unknown protein similar to PsAvr1a Pr_scaffold_13_F1570 P. ramorum homolog 129 25 0.998 0.880 48 68 Unknown protein similar to PsAvr1a Pr_scaffold_17_F1241 P. ramorum homolog 112 21 0.997 0.815 51 59 Unknown protein similar to PsAvr1a Pr_scaffold_207_F26 P. ramorum homolog 138 23 0.997 0.898 56 69 Unknown protein similar to PsAvr1a Pr_scaffold_251_R3 P. ramorum homolog 139 21 1 0.894 54 73 Unknown protein similar to PsAvr1a Pr_scaffold_26_R566 P. ramorum homolog 141 21 1 0.898 54 75 Unknown protein similar to PsAvr1a Pr_scaffold_26_R615 P. ramorum homolog 152 21 1 0.884 58 86 Unknown protein similar to PsAvr1a Pr_scaffold_34_F586 P. ramorum homolog 293 21 1 0.938 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_50_R933 P. ramorum homolog 140 23 1 0.822 52 Unknown protein similar to PsAvr1a Pr_scaffold_52_F517 P. ramorum homolog 151 22 0.994 0.811 52 70 Unknown protein similar to PsAvr1a Pr_scaffold_64_F233 P. ramorum homolog 293 21 1 0.947 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_64_F343 P. ramorum homolog 294 21 1 0.932 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_65_R231 P. ramorum homolog 162 21 1 0.953 58 83 Unknown protein similar to PsAvr1a Pr_scaffold_75_F477 P. ramorum homolog 136 23 0.999 0.870 53 69 Unknown protein similar to PsAvr1a Pr_scaffold_91_R166 P. ramorum homolog 154 21 0.999 0.892 57 81 Unknown protein similar to PsAvr1a Ps_scaffold_118_R508 P. sojae homolog 98 21 0.998 0.869 54 71 Unknown protein similar to PsAvr1a Ps_scaffold_122_R489 P. sojae homolog 125 25 0.999 0.858 48 68 Unknown protein similar to PsAvr1a Ps_scaffold_27_R1297 P. sojae homolog 305 21 0.996 0.951 51 Unknown protein similar to PsAvr1a Ps_scaffold_3_R4103 P. sojae homolog 130 21 0.994 0.863 54 70 Unknown protein similar to PsAvr1a Ps_scaffold_36_F644 P. sojae homolog 137 23 1 0.856 53 74 Unknown protein similar to PsAvr1a Ps_scaffold_68_F347 P. sojae homolog 162 21 1 0.898 50 61 Unknown protein similar to PsAvr3a Pr_scaffold_1497_R5 P. ramorum homolog 126 19 0.997 0.934 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_F760 P. ramorum homolog 126 19 0.998 0.942 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_F786 P. ramorum homolog 125 19 1 0.932 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_R44 P. ramorum homolog 128 19 0.998 0.942 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_34_R60 P. ramorum homolog 127 19 0.997 0.943 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_6_R2337 P. ramorum homolog 203 20 1 0.941 43 61 Unknown protein similar to PsAvr3a Pr_scaffold_6_R2603 P. ramorum homolog 204 20 1 0.935 43 61 Unknown protein similar to PsAvr3a Ps_scaffold_106_F265 P. sojae homolog 131 20 0.999 0.930 45 Unknown protein similar to PsAvr3a Ps_scaffold_106_R557 P. sojae homolog 131 20 0.999 0.930 45 Unknown protein similar to PsAvr3a Ps_scaffold_24_F382 P. sojae homolog 137 20 1 0.954 44 Unknown protein similar to PsAvr3a Ps_scaffold_31_F1779 P. sojae homolog 167 20 1 0.934 43 56 Unknown protein similar to PsAvr3a Ps_scaffold_31_R1171 P. sojae homolog 120 20 1 0.950 40 58 Unknown protein similar to PsAvr3a Ps_scaffold_87_F189 P. sojae homolog 145 22 1 0.879 43 75 Means 155.94 21.1 0.99 0.90 48.9 66.6 Means 158.3 20.7 0.99 0.86 45.0 62.1 reported by Win et al (2007) The two P. sojae avirulence proteins were reported after we applied the gene mining pipeline described in Win et al (2007) and therefore validate the approach. This list of 36 genes complements the 43 validated effectors a b described in Table 1 of Win et al. (2007). GenBank accession number is provided where available. Otherwise, accession numbers correspond to sequences listed in Table S2 of Win et al (2007). Length in amino acids. Position counting from N-terminus. 252 Plant Signaling & Behavior 2008; Vol. 3 Issue 4 ©2008 Landes Bioscience. Do not distribute. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Figure 1. An example of a paralogous gene group (PGG) with evidence of positive selection focused mainly on the C-terminal effector domain. (A) Multiple sequence alignment of the five Phytophthora ramorum proteins that form PrPGG5. Identical amino acids are indicated by dots. (B) Posterior probabilities estimated by Bayes Empirical Bayes analysis for the model M8 in PAML software package were plotted for each amino acid site in PrPGG5. Positively selected sites are indicated by “*”. *p > 95% and **p > 99%. References Patterns of Positive Selection are Consistent with the Modular 1. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL. Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol 2006; 14:8-11. Structure of RXLR Effectors 2. Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 2006; 124:803-14. The genome-wide catalogs of RXLR effector genes from the three 3. Kamoun S. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev oomycete species revealed complex and diverse sets of RXLR effector Phytopathol 2006; 44:41-60. genes that have undergone relatively rapid birth and death evolution. 4. O’Connell RJ, Panstruga R. Tete a tete inside a plant cell: Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 2006; 171:699-718. We obtained robust evidence of positive selection in more than two 5. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL. Subterfuge and manipulation: Type thirds of the examined paralog families of RXLR effectors. Positive III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 2006; 60:425-49. selection has acted on paralogous RXLR gene families targeting for 6. Jones JD, Dangl JL. The plant immune system. Nature 2006; 444:323-9. the most part the C-terminal region. These findings are consistent with 7. Huang G, Allen R, Davis EL, Baum TJ, Hussey RS. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode the view that RXLR effectors are modular proteins with the N-terminus parasitism gene. Proc Natl Acad Sci USA 2006; 103:14302-6. involved in secretion and host translocation and the C-terminal domain 8. Huang G, Dong R, Allen R, Davis EL, Baum TJ, Hussey RS. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe dedicated to modulating host defenses inside plant cells. In Figure Interact 2006; 19:463-70. 1, we illustrate the remarkably biased distribution of the positively 9. Dawkins R, Krebs JR. Arms Races between and within species. Proc Royal Soc London selected sites towards the C-terminal region for PrPGG5, one of the Series B 1979; 205:489-511. 10. Dawkins R. The Extended Phenotype: The Long reach of the Gene. Oxford, UK: Oxford paralogous gene groups of P. ramorum. University Press, 1999. 11. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Conclusion Bensasson D, Beynon JL, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006; 313:1261-6. In summary, we reported and validated a method for ab initio 12. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, Kamoun S, Tyler mining of RXLR effectors in oomycete genome sequences. We applied BM, Birch PR, Beynon JL. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell this method to develop genome-wide catalogs of RXLR effectors and 2005; 17:1839-50. demonstrate that adaptive evolution has shaped the structure of 13. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong these genes. Future studies will determine the extent to which the MR, Grouffaud S, van West P, Chapman S, et al. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 2007; In press. positively selected genes and residues identified in our study are 14. Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, Young C, Kamoun S, Haldar functionally important. K. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog 2006; 2:e50. 15. Bos JI, Kanneganti TD, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PR, Kamoun S. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 2006; 48:165-76. www.landesbioscience.com Plant Signaling & Behavior 253 ©2008 Landes Bioscience. Do not distribute. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Plant Signaling & Behavior Taylor & Francis

Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes

Win, Joe; Kamoun, Sophien
Plant Signaling & Behavior , Volume 3 (4): 3 – Apr 1, 2008
Download PDF
3 pages

Loading next page...
 
/lp/taylor-francis/adaptive-evolution-has-targeted-the-c-terminal-domain-of-the-rxlr-dCKoM2bKBl

References (80)

Publisher
Taylor & Francis
Copyright
Copyright © 2008 Landes Bioscience
ISSN
1559-2324
DOI
10.4161/psb.3.4.5182
Publisher site
See Article on Publisher Site

Abstract

[Plant Signaling & Behavior 3:4, 251-253; April 2008]; ©2008 Landes Bioscience Article Addendum Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Joe Win and Sophien Kamoun* Sainsbury Laboratory; Norwich, United Kingdom Key words: plant-microbe interactions, effectors, gene families, positive selection Plant pathogenic microbes deliver effector proteins inside is similar in sequence and position and is functionally interchangeable host cells to modulate plant defense circuitry and enable parasitic with the plasmodial host translocation (HT)/Pexel motif that func- colonization. As genome sequences from plant pathogens become tions in delivery of parasite proteins into the cytoplasm of red blood available, genome‑wide evolutionary analyses will shed light on cells of mammalian hosts. Also, the RXLR motif is not required how pathogen effector genes evolved and adapted to the cellular for the effector activities of P. infestans AVR3a when this protein is environment of their host plants. In the August 2007 issue of Plant directly expressed inside plant cells consistent with a role in targeting Cell, we described adaptive evolution (positive selection) in the rather than effector activity. Altogether these findings led to the cytoplasmic RXLR effectors of three recently sequenced oomycete view that oomycete RXLR effectors are modular proteins with two plant pathogens. Here, we summarize our findings and describe major functional domains. While the N-terminal domain encom- additional data that further validate our approach. passing the signal peptide and RXLR leader functions in secretion and targeting, the remaining C-terminal region carries the effector activity A diverse number of plant pathogens, including bacteria, oomycetes, and operates inside plant cells. fungi and nematodes, deliver effector proteins inside host cells to Ab Initio Identification of RXLR Effectors: Rationale 1-8 modulate plant defense circuitry and enable parasitic colonization. Because these so-called cytoplasmic effectors function inside plant In the initial part of our study, we aimed to develop a method cells and produce phenotypes that extend to plant cells and tissues, for ab initio identification of RXLR effector genes in the sequenced their genes are expected to be the direct target of the evolutionary genomes. Our approach was to first determine the defining features forces that drive the antagonistic interplay between pathogen and of validated oomycete RXLR effectors in order to develop a robust set 9,10 host. In a study published in the August 2007 issue of Plant Cell, of data mining criteria. We therefore, developed an unbiased list of 43 we and our collaborators examined the extent to which positive selec- oomycete RXLR proteins consisting of validated effectors and their tion (adaptive evolution) has shaped the evolution of the cytoplasmic closest homologs. Also, to objectively address the extent to which effectors of three recently sequenced oomycete plant pathogens the tetrapeptide RXLR sequence is overrepresented and positionally Phytophthora sojae, Phytophthora ramorum, and Hyaloperonospora para- constrained in Phytophthora, we examined the distribution of the sitica (Genome Sequencing Center at Washington University). RXLR sequence in the proteomes of these species compared to 46 other eukaryotes. These analyses indicated that the RXLR sequence is Oomycete RXLR Effectors are Modular Proteins significantly overrepresented and positionally constrained in the secre- Four oomycete Avr proteins have been described in the past three tomes of Phytophthora relative to other eukaryotes and formed the years and were found to contain a secretory signal peptide followed basis of the ab initio algorithm. by a conserved domain featuring the motif RXLR, flanked by a high 1,3,12 Ab Initio Identification of RXLR Effectors: Further Validation frequency of acidic (D/E) residues. The RXLR motif defines a domain that functions in delivery of effector proteins into host cells. It Since the publication of our study, two new avirulence genes, PsAvr1a and PsAvr3a, were reported from Phytophthora sojae by Mark *Correspondence to: Sophien Kamoun; Sainsbury Laboratory; John Innes Center; Gijzen laboratory, London, Ontario, Canada (GenBank accessions Colney Lane; Norwich NR4 7UH United Kingdom; Tel: +44.1603.450410; Email: ABQ81647 and ABO47652). Interestingly, PsAvr1a and PsAvr3a [email protected] fulfill our criteria for RXLR effectors and were identified by our Submitted: 10/12/07; Accepted: 10/17/07 ab initio algorithm (Supplemental Table S2 of the Win et al. paper). In Table 1, we list the features of PsAvr1a and PsAvr3a, and their 34 Previously published online as a Plant Signaling & Behavior E-publication: www.landesbioscience.com/journals/psb/article/5182 homologous genes. The mean values for protein size, position of RXLR, and position of EER sequence obtained with this new set of Addendum to: Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, validated RXLR effectors are remarkably similar to those we reported Ammar R, Staskawicz BJ, Kamoun S. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 2007; earlier. 19:2349–69; PMID: 17675403; DoI: 10.1105/tpc.107.051037. www.landesbioscience.com Plant Signaling & Behavior 251 ©2008 Landes Bioscience. Do not distribute. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Table 1 New validated RXLR effectors. The new validated effectors are based on two Phytophthora sojae avirulence proteins, PsAvr1a and PsAvr3a, reported by the laboratory of Mark Gijzen, London, Ontario, Canada ‑4 and their homologs (E value <10 ) a b Description Accession Species Evidence Length Signal SignalP SignalP RXLR EER c c Peptide v2.0 HMM v2.0 NN Position position Length score score ABQ81647, Avirulence effector protein PsAvr3a Ps_scaffold_80_R245 P. sojae Avr effector 111 20 0.998 0.910 43 ABo47652, Avirulence effector protein PsAvr1a Ps_scaffold_1058_F4 P. sojae Avr effector 121 25 0.999 0.813 54 64 Unknown protein similar to PsAvr1a Pr_scaffold_103_F268 P. ramorum homolog 121 21 0.994 0.850 54 Unknown protein similar to PsAvr1a Pr_scaffold_13_F1570 P. ramorum homolog 129 25 0.998 0.880 48 68 Unknown protein similar to PsAvr1a Pr_scaffold_17_F1241 P. ramorum homolog 112 21 0.997 0.815 51 59 Unknown protein similar to PsAvr1a Pr_scaffold_207_F26 P. ramorum homolog 138 23 0.997 0.898 56 69 Unknown protein similar to PsAvr1a Pr_scaffold_251_R3 P. ramorum homolog 139 21 1 0.894 54 73 Unknown protein similar to PsAvr1a Pr_scaffold_26_R566 P. ramorum homolog 141 21 1 0.898 54 75 Unknown protein similar to PsAvr1a Pr_scaffold_26_R615 P. ramorum homolog 152 21 1 0.884 58 86 Unknown protein similar to PsAvr1a Pr_scaffold_34_F586 P. ramorum homolog 293 21 1 0.938 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_50_R933 P. ramorum homolog 140 23 1 0.822 52 Unknown protein similar to PsAvr1a Pr_scaffold_52_F517 P. ramorum homolog 151 22 0.994 0.811 52 70 Unknown protein similar to PsAvr1a Pr_scaffold_64_F233 P. ramorum homolog 293 21 1 0.947 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_64_F343 P. ramorum homolog 294 21 1 0.932 52 67 Unknown protein similar to PsAvr1a Pr_scaffold_65_R231 P. ramorum homolog 162 21 1 0.953 58 83 Unknown protein similar to PsAvr1a Pr_scaffold_75_F477 P. ramorum homolog 136 23 0.999 0.870 53 69 Unknown protein similar to PsAvr1a Pr_scaffold_91_R166 P. ramorum homolog 154 21 0.999 0.892 57 81 Unknown protein similar to PsAvr1a Ps_scaffold_118_R508 P. sojae homolog 98 21 0.998 0.869 54 71 Unknown protein similar to PsAvr1a Ps_scaffold_122_R489 P. sojae homolog 125 25 0.999 0.858 48 68 Unknown protein similar to PsAvr1a Ps_scaffold_27_R1297 P. sojae homolog 305 21 0.996 0.951 51 Unknown protein similar to PsAvr1a Ps_scaffold_3_R4103 P. sojae homolog 130 21 0.994 0.863 54 70 Unknown protein similar to PsAvr1a Ps_scaffold_36_F644 P. sojae homolog 137 23 1 0.856 53 74 Unknown protein similar to PsAvr1a Ps_scaffold_68_F347 P. sojae homolog 162 21 1 0.898 50 61 Unknown protein similar to PsAvr3a Pr_scaffold_1497_R5 P. ramorum homolog 126 19 0.997 0.934 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_F760 P. ramorum homolog 126 19 0.998 0.942 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_F786 P. ramorum homolog 125 19 1 0.932 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_33_R44 P. ramorum homolog 128 19 0.998 0.942 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_34_R60 P. ramorum homolog 127 19 0.997 0.943 41 56 Unknown protein similar to PsAvr3a Pr_scaffold_6_R2337 P. ramorum homolog 203 20 1 0.941 43 61 Unknown protein similar to PsAvr3a Pr_scaffold_6_R2603 P. ramorum homolog 204 20 1 0.935 43 61 Unknown protein similar to PsAvr3a Ps_scaffold_106_F265 P. sojae homolog 131 20 0.999 0.930 45 Unknown protein similar to PsAvr3a Ps_scaffold_106_R557 P. sojae homolog 131 20 0.999 0.930 45 Unknown protein similar to PsAvr3a Ps_scaffold_24_F382 P. sojae homolog 137 20 1 0.954 44 Unknown protein similar to PsAvr3a Ps_scaffold_31_F1779 P. sojae homolog 167 20 1 0.934 43 56 Unknown protein similar to PsAvr3a Ps_scaffold_31_R1171 P. sojae homolog 120 20 1 0.950 40 58 Unknown protein similar to PsAvr3a Ps_scaffold_87_F189 P. sojae homolog 145 22 1 0.879 43 75 Means 155.94 21.1 0.99 0.90 48.9 66.6 Means 158.3 20.7 0.99 0.86 45.0 62.1 reported by Win et al (2007) The two P. sojae avirulence proteins were reported after we applied the gene mining pipeline described in Win et al (2007) and therefore validate the approach. This list of 36 genes complements the 43 validated effectors a b described in Table 1 of Win et al. (2007). GenBank accession number is provided where available. Otherwise, accession numbers correspond to sequences listed in Table S2 of Win et al (2007). Length in amino acids. Position counting from N-terminus. 252 Plant Signaling & Behavior 2008; Vol. 3 Issue 4 ©2008 Landes Bioscience. Do not distribute. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes Figure 1. An example of a paralogous gene group (PGG) with evidence of positive selection focused mainly on the C-terminal effector domain. (A) Multiple sequence alignment of the five Phytophthora ramorum proteins that form PrPGG5. Identical amino acids are indicated by dots. (B) Posterior probabilities estimated by Bayes Empirical Bayes analysis for the model M8 in PAML software package were plotted for each amino acid site in PrPGG5. Positively selected sites are indicated by “*”. *p > 95% and **p > 99%. References Patterns of Positive Selection are Consistent with the Modular 1. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL. Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol 2006; 14:8-11. Structure of RXLR Effectors 2. Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 2006; 124:803-14. The genome-wide catalogs of RXLR effector genes from the three 3. Kamoun S. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev oomycete species revealed complex and diverse sets of RXLR effector Phytopathol 2006; 44:41-60. genes that have undergone relatively rapid birth and death evolution. 4. O’Connell RJ, Panstruga R. Tete a tete inside a plant cell: Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 2006; 171:699-718. We obtained robust evidence of positive selection in more than two 5. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL. Subterfuge and manipulation: Type thirds of the examined paralog families of RXLR effectors. Positive III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 2006; 60:425-49. selection has acted on paralogous RXLR gene families targeting for 6. Jones JD, Dangl JL. The plant immune system. Nature 2006; 444:323-9. the most part the C-terminal region. These findings are consistent with 7. Huang G, Allen R, Davis EL, Baum TJ, Hussey RS. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode the view that RXLR effectors are modular proteins with the N-terminus parasitism gene. Proc Natl Acad Sci USA 2006; 103:14302-6. involved in secretion and host translocation and the C-terminal domain 8. Huang G, Dong R, Allen R, Davis EL, Baum TJ, Hussey RS. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe dedicated to modulating host defenses inside plant cells. In Figure Interact 2006; 19:463-70. 1, we illustrate the remarkably biased distribution of the positively 9. Dawkins R, Krebs JR. Arms Races between and within species. Proc Royal Soc London selected sites towards the C-terminal region for PrPGG5, one of the Series B 1979; 205:489-511. 10. Dawkins R. The Extended Phenotype: The Long reach of the Gene. Oxford, UK: Oxford paralogous gene groups of P. ramorum. University Press, 1999. 11. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Conclusion Bensasson D, Beynon JL, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006; 313:1261-6. In summary, we reported and validated a method for ab initio 12. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, Kamoun S, Tyler mining of RXLR effectors in oomycete genome sequences. We applied BM, Birch PR, Beynon JL. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell this method to develop genome-wide catalogs of RXLR effectors and 2005; 17:1839-50. demonstrate that adaptive evolution has shaped the structure of 13. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong these genes. Future studies will determine the extent to which the MR, Grouffaud S, van West P, Chapman S, et al. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 2007; In press. positively selected genes and residues identified in our study are 14. Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, Young C, Kamoun S, Haldar functionally important. K. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog 2006; 2:e50. 15. Bos JI, Kanneganti TD, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PR, Kamoun S. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 2006; 48:165-76. www.landesbioscience.com Plant Signaling & Behavior 253 ©2008 Landes Bioscience. Do not distribute.

Journal

Plant Signaling & Behavior – Taylor & Francis

Published: Apr 1, 2008

There are no references for this article.