1. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. (2006) Hostmicrobe interactions: Shaping the evolution of the plant immune
response. Cell 124, 803–814
2. Jones, J. D., and Dangl, J. L. (2006) The plant immune system. Nature 444,
323–329
3. Win, J., Chaparro-Garcia, A., Belhaj, K., Saunders, D. G., Yoshida, K.,
Dong, S., Schornack, S., Zipfel, C., Robatzek, S., Hogenhout, S. A., and
Kamoun, S. (2012) Effector biology of plant-associated organisms:
Concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77,
235–247
4. Cui, H., Tsuda, K., and Parker, J. E. (2015) Effector-triggered immunity:
From pathogen perception to robust defense. Annu. Rev. Plant Biol. 66,
487–511
5. Gan, P., Ikeda, K., Irieda, H., Narusaka, M., O’Connell, R. J., Narusaka, Y.,
Takano, Y., Kubo, Y., and Shirasu, K. (2013) Comparative genomic and
transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol. 197, 1236–1249
6. O’Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J.,
Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmuller, J.,
Alvarado-Balderrama, L., Bauser, C. A., Becker, C., Birren, B. W., et al.
(2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi
deciphered by genome and transcriptome analyses. Nat. Genet. 44, 1060–
1065
7. Perfect, S. E., Hughes, H. B., O’Connell, R. J., and Green, J. R. (1999)
Colletotrichum: A model genus for studies on pathology and fungal-plant
interactions. Fungal Genet. Biol. 27, 186–198
8. Kubo, Y., Nakamura, H., Kobayashi, K., Okuno, T., and Furusawa, I.
(1991) Cloning of a melanin biosynthetic gene essential for appressorial
penetration of Colletotrichum lagenarium. Mol. Plant Microbe Interact. 4,
440–445
9. Kubo, Y., and Takano, Y. (2013) Dynamics of infection-related morphogenesis and pathogenesis in Colletotrichum orbiculare. J. Gen. Plant
Pathol. 79, 233–242
10. Cannon, P. F., Damm, U., Johnston, P. R., and Weir, B. S. (2012) Colletotrichum - current status and future directions. Stud. Mycol. 73, 181–
213
11. Liu, B., Wasilwa, L. A., Morelock, T. E., O’Neill, N. R., and Correll, J. C.
(2007) Comparison of Colletotrichum orbiculare and several allied Colletotrichum spp. for mtDNA RFLPs, intron RFLP and sequence variation,
vegetative compatibility, and host specificity. Phytopathology 97, 1305–
1314
12. Goodin, M. M., Zaitlin, D., Naidu, R. A., and Lommel, S. A. (2008)
Nicotiana benthamiana: Its history and future as a model for plantpathogen interactions. Mol. Plant Microbe Interact. 21, 1015–1026
13. Shen, S., Goodwin, P. H., and Hsiang, T. (2001) Infection of Nicotiana
species by the anthracnose fungus, Colletotrichum orbiculare. Eur. J. Plant
Pathol. 107, 767–773
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Effector with unique structure suppresses plant immunity
14. Takano, Y., Takayanagi, N., Hori, H., Ikeuchi, Y., Suzuki, T., Kimura, A.,
and Okuno, T. (2006) A gene involved in modifying transfer RNA is
required for fungal pathogenicity and stress tolerance of Colletotrichum
lagenarium. Mol. Microbiol. 60, 81–92
15. Irieda, H., Maeda, H., Akiyama, K., Hagiwara, A., Saitoh, H., Uemura, A.,
Terauchi, R., and Takano, Y. (2014) Colletotrichum orbiculare secretes
virulence effectors to a biotrophic interface at the primary hyphal neck via
exocytosis coupled with SEC22-mediated traffic. Plant Cell 26, 2265–
2281
16. Yoshino, K., Irieda, H., Sugimoto, F., Yoshioka, H., Okuno, T., and
Takano, Y. (2012) Cell death of Nicotiana benthamiana is induced by
secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a
homologue of CgDN3. Mol. Plant Microbe Interact. 25, 625–636
17. Isozumi, N., Inoue, Y., Imamura, T., Mori, M., Takano, Y., and Ohki, S.
(2019) Ca2+-dependent interaction between calmodulin and CoDN3, an
effector of Colletotrichum orbiculare. Biochem. Biophys. Res. Commun.
514, 803–808
18. Irieda, H., Inoue, Y., Mori, M., Yamada, K., Oshikawa, Y., Saitoh, H.,
Uemura, A., Terauchi, R., Kitakura, S., Kosaka, A., Singkaravanit-Ogawa,
S., and Takano, Y. (2019) Conserved fungal effector suppresses PAMPtriggered immunity by targeting plant immune kinases. Proc. Natl.
Acad. Sci. U. S. A. 116, 496–505
19. Shimada, C., Lipka, V., O’Connel, R., Okuno, T., Schulze-Lefert, P., and
Takano, Y. (2006) Nonhost resistance in Arabidopsis-colletotrichum interactions acts at the cell periphery and requires actin filament function.
Mol. Plant Microbe Interact. 19, 270–279
20. Inagaki, A., Takano, Y., Kubo, Y., Mise, K., and Furusawa, I. (2000)
Construction of an equalized cDNA library from Colletotrichum lagenarium and its application to the isolation of differentially expressed
genes. Can. J. Microbiol. 46, 150–158
21. Armenteros, J. J. A., Tsirigos, K. D., Sonderby, C. K., Petersen, T. N.,
Winther, O., Brunak, S., von Heijne, G., and Nielsen, H. (2019) SignalP 5.
0 improves signal peptide predictions using deep neural networks. Nat.
Biotechnol. 37, 420–423
22. Ramachandran, S. R., Yin, C. T., Kud, J., Tanaka, K., Mahoney, A. K.,
Xiao, F. M., and Hulbert, S. H. (2017) Effectors from wheat rust fungi
suppress multiple plant defense responses. Phytopathology 107, 75–83
23. Kanneganti, T. D., Huitema, E., Cakir, C., and Kamoun, S. (2006) Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nep1-like protein PiNPP1.1 and INF1 elicitin. Mol.
Plant Microbe Interact. 19, 854–863
24. Ninomiya, Y., Suzuki, K., Ishii, C., and Inoue, H. (2004) Highly efficient
gene replacements in Neurospora strains deficient for nonhomologous
end-joining. Proc. Natl. Acad. Sci. U. S. A. 101, 12248–12253
25. Dohi, K., and Mori, M. (2007) Expression of active enzymes from an
inducible tomato-mosaic-virus-based vector in cultured transgenic tobacco BY-2 cells. Plant Biotechnol. 24, 367–373
26. Dohi, K., Nishikiori, M., Tamai, A., Ishikawa, M., Meshi, T., and Mori, M.
(2006) Inducible virus-mediated expression of a foreign protein in
suspension-cultured plant cells. Arch. Virol. 151, 1075–1084
27. Costa, L. M., Marshall, E., Tesfaye, M., Silverstein, K. A. T., Mori, M.,
Umetsu, Y., Otterbach, S. L., Papareddy, R., Dickinson, H. G., Boutiller,
K., VandenBosch, K. A., Ohki, S., and Gutierrez-Marcos, J. F. (2014)
Central cell–derived peptides regulate early embryo patterning in flowering plants. Science 344, 168–172
28. Imamura, T., Isozumi, N., Higashimura, Y., Ohki, S., and Mori, M. (2021)
Production of ORF8 protein from SARS-CoV-2 using an inducible virusmediated expression system in suspension-cultured tobacco BY-2 cells.
Plant Cell Rep. 40, 433–436
29. Ohki, S., Dohi, K., Tamai, A., Takeuchi, M., and Mori, M. (2008) Stableisotope labeling using an inducible viral infection system in suspensioncultured plant cells. J. Biomol. NMR 42, 271–277
30. Ohki, S., Takeuchi, M., and Mori, M. (2011) The NMR structure of
stomagen reveals the basis of stomatal density regulation by plant peptide
hormones. Nat. Commun. 2, 512
31. Ito, K., Ikemasu, T., and Ishikawa, T. (1992) Cloning and sequencing of
the xynA gene encoding xylanase A of Aspergillus kawachii. Biosci. Biotechnol. Biochem. 56, 906–912
32. Liao, Y. D., Wang, S. C., Leu, Y. J., Wang, C. F., Chang, S. T., Hong, Y. T.,
Pan, Y. R., and Chen, C. P. (2003) The structural integrity exerted by
N-terminal pyroglutamate is crucial for the cytotoxicity of frog ribonuclease from Rana pipiens. Nucleic Acids Res. 31, 5247–5255
33. Lopez-Mendez, B., and Guntert, P. (2006) Automated protein structure
determination from NMR spectra. J. Am. Chem. Soc. 128, 13112–13122
34. Lee, W., Stark, J. L., and Markley, J. L. (2014) PONDEROSA-C/S: Clientserver based software package for automated protein 3D structure
determination. J. Biomol. NMR 69, 73–75
35. Rieping, W., Habeck, M., Bardiaux, B., Bernard, A., Malliavin, T. E., and
Nilges, M. (2007) ARIA2: Automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23, 381–382
36. Schwieters, C., Kuszewski, J., Tjandra, N., and Clore, M. (2003) The
Xplor-NIH NMR molecular structure determination package. J. Magn.
Reson. 160, 65–73
37. Gan, P., Tsushima, A., Narusaka, M., Narusaka, Y., Takano, Y., Kubo, Y.,
and Shirasu, K. (2019) Genome sequence resources for four phytopathogenic fungi from the Colletotrichum orbiculare species complex. Mol.
Plant Microbe Interact. 32, 1088–1090
38. Marino, D., Dunand, C., Puppo, A., and Pauly, N. (2012) A burst of plant
NADPH oxidases. Trends Plant Sci. 17, 9–15
39. Asai, S., Ohta, K., and Yoshioka, H. (2008) MAPK signaling regulates
nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana
benthamiana. Plant Cell 20, 1390–1406
40. Segonzac, C., Feike, D., Gimenez-Ibanez, S., Hann, D. R., Zipfel, C., and
Rathjen, J. P. (2011) Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol.
156, 687–699
41. Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland,
O., Jones, J. D., and Doke, N. (2003) Nicotiana benthamiana gp91phox
homologs NbrbohA and NbrbohB participate in H2O2 accumulation and
resistance to Phytophthora infestans. Plant Cell 15, 706–718
42. Campos-Olivas, R., Bruix, M., Santoro, J., Lacadena, J., Martiz del Pozo,
A., Gavilanes, J. G., and Rico, M. (1995) NMR solution structure of the
antifungal protein from Aspergillus giganeteus: Evidence for cysteine
pairing isomerism. Biochemistry 34, 3009–3021
43. Batta, G., Barna, T., Gaspari, Z., Sandor, S., Kover, K. E., Binder, U., Sarg,
B., Kaiserer, L., Chhilar, A. K., Eigentler, A., Leiter, E., Hefedus, N., Pocsi,
I., Linder, H., and Marx, F. (2009) Functional aspects of the solution
structure and dynamics of PAF - a highly-stable antifungal protein from
Penicillium chrysogenum. FEBS J. 276, 2875–2890
44. Caldwell, J. E., Abildgaard, F., Dzakula, Z., Ming, D., Hellekant, G., and
Markley, J. L. (1998) Solution structure of the thermostable sweet-tasting
protein brazzein. Nat. Struct. Mol. Biol. 5, 427–431
45. Graciet, E., Walter, F., O’Maoileidigh, D., Pollmann, S., Meyerowitz, E.
M., Varshavsky, A., and Wellmer, F. (2009) The N-end rule pathway
controls multiple functions during Arabidopsis shoot and leaf development. Proc. Natl. Acad. Sci. U. S. A. 106, 13618–13623
46. Namiki, F., Matsunaga, M., Okuda, M., Inoue, I., Nishi, K., Fujita, Y., and
Tsuge, T. (2001) Mutation of an arginine biosynthesis gene causes
reduced pathogenicity in Fusarium oxysporum f. sp melonis. Mol. Plant
Microbe Interact. 14, 580–584
47. Asakura, M., Ninomiya, S., Sugimoto, M., Oku, M., Yamashita, S.,
Okuno, T., Sakai, Y., and Takano, Y. (2009) Atg26-mediated pexophagy is
required for host invasion by the plant pathogenic fungus Colletotrichum
orbiculare. Plant Cell 21, 1291–1304
48. Sweigard, J. A., Chumley, F. G., Carroll, A. M., Farrall, L., and Valent, B.
(1997) A series of vectors for fungal transformation. Fungal Genet. Newsl.
44, 52–53
49. Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S.,
Batut, P., Chaisson, M., and Gingeras, T. R. (2013) Star: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21
50. Liao, Y., Smyth, G. K., and Shi, W. (2019) The R package Rsubread is
easier, faster, cheaper and better for alignment and quantification of RNA
sequencing reads. Nucleic Acids Res. 47, e47
51. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B.
(2008) Mapping and quantifying mammalian transcriptomes by RNASeq. Nat. Methods 5, 621–628
J. Biol. Chem. (2021) 297(6) 101370
13
A Self-archived copy in
Kyoto University Research Information Repository
https://repository.kulib.kyoto-u.ac.jp
Effector with unique structure suppresses plant immunity
52. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010) edgeR: A
bioconductor package for differential expression analysis of digital gene
expression data. Bioinformatics 26, 139–140
53. Keppler, L. D., Baker, C. J., and Atkinson, M. M. (1989) Active oxygen
production during a bacteria-induced hypersensitive reaction in tobacco
suspension cells. Phytopathology 79, 974–978
54. Nagata, T., Nemoto, Y., and Hasezawa, S. (1992) Tobacco BY-2 cell line
as the “HeLa” cell in the cell biology of higher plants. Int. Rev. Cyt. 132,
1–30
55. Hagiwara, Y., Komoda, K., Yamanaka, T., Tamai, A., Meshi, T., Funada,
R., Tsuchiya, T., Naito, S., and Ishikawa, M. (2003) Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J. 22, 344–353
56. Takano, Y., Komeda, K., Kojima, K., and Okuno, T. (2001) Proper
regulation of cyclic AMP-dependent protein kinase is required for
growth, conidiation, and appressorium function in the anthracnose fungus Colletotrichum lagenarium. Mol. Plant Microbe Interact. 14, 1149–
1157
57. Rappsilber, J., Mann, M., and Ishihama, Y. (2007) Protocol for micropurification, enrichment, pre-fractionation and storage of peptides for
proteomics using StageTips. Nat. Protoc. 2, 1896–1906
58. Isozumi, N., Masubuchi, Y., Imamura, T., Mori, M., Koga, H., and Ohki,
S. (2021) Structure and antimicrobial activity of NCR169, a nodulespecific cysteine-rich peptide of Medicago truncatula. Sci. Rep. 11, 9923
59. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance nitrogen-15
NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 69,
185–189
60. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient
enhanced heteronuclear single quantum correlation spectroscopy with
improved sensitivity. J. Am. Chem. Soc. 114, 10663–10665
61. Fesik, S., and Zuiderwerg, E. R. P. (1988) Heteronuclear threedimensional NMR spectroscopy. A strategy for the simplification of homonuclear two-dimensional NMR spectra. J. Magn. Reson. 78, 588–593
62. Marion, D., Driscoll, P. C., Kay, L. E., Wingfield, P. T., Bax, A., Gronenborn, A. M., and Clore, G. M. (1989) Overcoming the overlap
problem in the assignment of 1H NMR spectra of larger proteins by use of
14 J. Biol. Chem. (2021) 297(6) 101370
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
three-dimensional heteronuclear 1H-15N Hartmann-Hahn-multiple
quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: Application to interleukin 1 beta. Biochemistry 28,
6150–6156
Jeener, J., Meier, B. H., Bachman, P., and Ernst, R. R. (1979) Investigation
of exchange processes by two-dimensional NMR spectroscopy. J. Chem.
Phys. 71, 45–46
Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355–
360
Kay, L. E., Torchia, D. A., and Bax, A. (1989) Backbone dynamics of
proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28, 8972–
8979
Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation
for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol.
NMR 2, 661–665
Grzesiek, S., and Bax, A. (1993) The importance of not saturating water in
protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115, 12593–12594
Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A.
(1995) NMRPipe: A multidimensional spectral processing system based
on UNIX pipes. J. Biomol. NMR 6, 277–293
Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: A
hybrid method for predicting protein backbone torsion angles from NMR
chemical shifts. J. Biomol. NMR 44, 213–223
Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program
for display and analysis of macromolecular structures. J. Mol. Graph. 14,
29–32
Delano, W. L. (2002) Pymol: An open-source molecular graphics tool.
CCP4 Newslett. Pro. Crystallogr. 40, 82–92
Buck, M., Boyd, J., Redfield, C., MacKenzie, D. A., Jeenes, D. J., Archer, D.
B., and Dobson, C. M. (1995) Structural determinants of protein dynamics: Analysis of 15N NMR relaxation measurements for main-chain
and side-chain nuclei of hen egg white lysozyme. Biochemistry 34,
4041–4055
...