Altschul SF, Madden TL, Sch€a ffer AA, Zhang J, Zhang Z, Miller W, Lipman
DJ. 1997. GAPPED BLAST and PSI-BLAST: a new generation of protein database
search programs. Nucleic Acids Research 25: 3389–3402.
Ayukawa Y, Asai S, Gan P, Tsushima A, Ichihashi Y, Shibata A, Komatsu K,
Houterman PM, Rep M, Shirasu K et al. 2021. A pair of effectors encoded on
a conditionally dispensable chromosome of Fusarium oxysporum suppress hostspecific immunity. Communications Biology 4: 1–12.
Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S, Mitchell A,
Nuka G, Paysan-Lafosse T, Qureshi M, Raj S et al. 2021. The INTERPRO
protein families and domains database: 20 years on. Nucleic Acids Research 49:
D344–D354.
Cannon PF, Damm U, Johnston PR, Weir BS. 2012. Colletotrichum – current
status and future directions. Studies in Mycology 73: 181–213.
van Dam P, Fokkens L, Ayukawa Y, van der Gragt M, ter Horst A, Brankovics
B, Houterman PM, Arie T, Rep M. 2017. A mobile pathogenicity
chromosome in Fusarium oxysporum for infection of multiple cucurbit species.
Scientific Reports 7: 9042.
Damm U, Cannon PF, Liu F, Barreto RW, Guatimosim E, Crous PW. 2013.
The Colletotrichum orbiculare species complex: important pathogens of field
crops and weeds. Fungal Diversity 61: 29–59.
Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of
plant–pathogen interactions. Nature Reviews Genetics 11: 539–548.
Duplessis S, Lorrain C, Petre B, Figueroa M, Dodds PN, Aime MC. 2021. Host
adaptation and virulence in heteroecious rust fungi. Annual Review of
Phytopathology 59: 403–422.
Eddy SR. 2011. Accelerated profile HMM searches. PLoS Computational Biology
7: e1002195.
Gan P, Ikeda K, Irieda H, Narusaka M, O’Connell RJ, Narusaka Y, Takano Y,
Kubo Y, Shirasu K. 2013. Comparative genomic and transcriptomic analyses
reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytologist
197: 1236–1249.
Gan P, Tsushima A, Narusaka M, Narusaka Y, Takano Y, Kubo Y, Shirasu K.
2019. Genome sequence resources for four phytopathogenic fungi from the
Colletotrichum orbiculare species complex. Molecular Plant–Microbe Interactions
32: 1088–1090.
Gawehns F, Houterman PM, Ichou FA, Michielse CB, Hijdra M, Cornelissen
BJC, Rep M, Takken FLW. 2014. The Fusarium oxysporum effector Six6
contributes to virulence and suppresses I-2-mediated cell death. Molecular
Plant–Microbe Interactions 27: 336–348.
Gong Z, Ning N, Li Z, Xie X, Wilson RA, Liu W. 2022. Two Magnaporthe
appressoria-specific (MAS) proteins, MoMas3 and MoMas5, are required for
suppressing host innate immunity and promoting biotrophic growth in rice
cells. Molecular Plant Pathology 23: 1290–1302.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis
X, Fan L, Raychowdhury R, Zeng Q et al. 2011. TRINITY: reconstructing a
full-length transcriptome without a genome from RNA-Seq data. Nature
Biotechnology 29: 644–652.
Gu Z, Eils R, Schlesner M. 2016. Complex heatmaps reveal patterns
and correlations in multidimensional genomic data. Bioinformatics 32: 2847–
2849.
Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, Hannick LI, Maiti
R, Ronning CM, Rusch DB, Town CD et al. 2003. Improving the Arabidopsis
New Phytologist (2023) 238: 1578–1592
www.newphytologist.com
New
Phytologist
genome annotation using maximal transcript alignment assemblies. Nucleic
Acids Research 31: 5654–5666.
Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR,
Wortman JR. 2008. Automated eukaryotic gene structure annotation using
EVIDENCEMODELER and the program to assemble spliced alignments. Genome
Biology 9: R7.
Heath MC. 1981. A generalized concept of host-parasite specificity.
Phytopathology 71: 1121.
Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M. 2016. BRAKER1:
unsupervised RNA-Seq-based genome annotation with GENEMARK-ET and
AUGUSTUS. Bioinformatics 32: 767–769.
Huang W, Hong S, Tang G, Lu Y, Wang C. 2019. Unveiling the function and
regulation control of the DUF3129 family proteins in fungal infection of hosts.
Philosophical Transactions of the Royal Society of London. Series B: Biological
Sciences 374: 20180321.
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC,
Rattei T, Mende DR, Sunagawa S, Kuhn M et al. 2016. EGGNOG 4.5: a
hierarchical orthology framework with improved functional annotations for
eukaryotic, prokaryotic and viral sequences. Nucleic Acids Research 44: D286–
D293.
Irieda H, Inoue Y, Mori M, Yamada K, Oshikawa Y, Saitoh H, Uemura A,
Terauchi R, Kitakura S, Kosaka A et al. 2019. Conserved fungal effector
suppresses PAMP-triggered immunity by targeting plant immune kinases.
Proceedings of the National Academy of Sciences, USA 116: 496–505.
Irieda H, Maeda H, Akiyama K, Hagiwara A, Saitoh H, Uemura A, Terauchi R,
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.
Isozumi N, Inoue Y, Imamura T, Mori M, Takano Y, Ohki S. 2019. Ca2+dependent interaction between calmodulin and CoDN3, an effector of
Colletotrichum orbiculare. Biochemical and Biophysical Research Communications
514: 803–808.
Jayawardena R. 2016. Notes on currently accepted species of Colletotrichum.
Mycosphere 7: 1192–1260.
K€a ll L, Krogh A, Sonnhammer ELL. 2004. A combined transmembrane
topology and signal peptide prediction method. Journal of Molecular Biology
338: 1027–1036.
Kanja C, Hammond-Kosack KE. 2020. Proteinaceous effector discovery and
characterization in filamentous plant pathogens. Molecular Plant Pathology 21:
1353–1376.
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. 2019. Graph-based genome
alignment and genotyping with HISAT2 and HISAT-genotype. Nature
Biotechnology 37: 907–915.
Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, van Themaat EVL,
van der Does HC, Hacquard S, St€
uber K, Will I, Schmalenbach W et al.
2012. Sequential delivery of host-induced virulence effectors by appressoria and
intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS
Pathogens 8: e1002643.
Kleemann J, Takahara H, St€
uber K, O’Connell R. 2008. Identification of
soluble secreted proteins from appressoria of Colletotrichum higginsianum by
analysis of expressed sequence tags. Microbiology 154: 1204–1217.
Kubo Y, Takano Y. 2013. Dynamics of infection-related morphogenesis and
pathogenesis in Colletotrichum orbiculare. Journal of General Plant Pathology 79:
233–242.
Lanver D, Tollot M, Schweizer G, Lo Presti L, Reissmann S, Ma L-S,
Schuster M, Tanaka S, Liang L, Ludwig N et al. 2017. Ustilago maydis
effectors and their impact on virulence. Nature Reviews Microbiology 15:
409–421.
Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq
data with or without a reference genome. BMC Bioinformatics 12: 323.
Li J, Fokkens L, van Dam P, Rep M. 2020. Related mobile pathogenicity
chromosomes in Fusarium oxysporum determine host range on cucurbits.
Molecular Plant Pathology 21: 761–776.
Liao Y, Smyth GK, Shi W. 2019. The R package RSUBREAD is easier, faster,
cheaper and better for alignment and quantification of RNA sequencing reads.
Nucleic Acids Research 47: e47.
Ó 2023 The Authors
New Phytologist Ó 2023 New Phytologist Foundation
14698137, 2023, 4, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.18790 by Cochrane Japan, Wiley Online Library on [13/04/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1590 Research
Liu B, Wasilwa LA, Morelock TE, O’Neill NR, Correll JC. 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.
Lomsadze A, Burns PD, Borodovsky M. 2014. Integration of mapped RNA-Seq
reads into automatic training of eukaryotic gene finding algorithm. Nucleic
Acids Research 42: e119.
Lorrain C, Marchal C, Hacquard S, Delaruelle C, Petrowski J, Petre B, Hecker
A, Frey P, Duplessis S. 2018. The rust fungus Melampsora larici-populina
expresses a conserved genetic program and distinct sets of secreted protein genes
during infection of its two host plants, larch and poplar. Molecular Plant–
Microbe Interactions 31: 695–706.
Matsuo H, Ishiga Y, Kubo Y, Yoshioka Y. 2022. Colletotrichum orbiculare strains
distributed in Japan: race identification and evaluation of virulence to
cucurbits. Breeding Science 72: 306–315.
McCarthy DJ, Chen Y, Smyth GK. 2012. Differential expression analysis of
multifactor RNA-Seq experiments with respect to biological variation. Nucleic
Acids Research 40: 4288–4297.
McCarthy DJ, Smyth GK. 2009. Testing significance relative to a fold-change
threshold is a TREAT. Bioinformatics 25: 765–771.
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA,
Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ et al.
2021. PFAM: the protein families database in 2021. Nucleic Acids Research
49: D412–D419.
M€
unch S, Lingner U, Floss DS, Ludwig N, Sauer N, Deising HB. 2008. The
hemibiotrophic lifestyle of Colletotrichum species. Journal of Plant Physiology
165: 41–51.
Nielsen H. 2017. Predicting secretory proteins with SignalP. In: Kihara D, ed.
Methods in molecular biology. Protein function prediction: methods and protocols.
New York, NY, USA: Springer, 59–73.
Niks RE, Marcel TC. 2009. Nonhost and basal resistance: how to explain
specificity? New Phytologist 182: 817–828.
Niu X, Zhao X, Ling K-S, Levi A, Sun Y, Fan M. 2016. The FonSIX6 gene acts
as an avirulence effector in the Fusarium oxysporum f. sp. niveum – watermelon
pathosystem. Scientific Reports 6: 28146.
O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF,
Damm U, Buiate EA, Epstein L, Alkan N et al. 2012. Lifestyle transitions in
plant pathogenic Colletotrichum fungi deciphered by genome and
transcriptome analyses. Nature Genetics 44: 1060–1065.
Panstruga R, Moscou MJ. 2020. What is the molecular basis of nonhost
resistance? Molecular Plant–Microbe Interactions 33: 1253–1264.
Perfect SE, Hughes HB, O’Connell RJ, Green JR. 1999. Colletotrichum: a model
genus for studies on pathology and fungal–plant interactions. Fungal Genetics
and Biology 27: 186–198.
de Queiroz CB, Correia HLN, Menicucci RP, Vidigal PMP, de Queiroz MV.
2017. Draft genome sequences of two isolates of Colletotrichum
lindemuthianum, the causal agent of anthracnose in common beans. Genome
Announcements 5: e00214-17.
Rawlings ND, Barrett AJ, Thomas PD, Huang X, Bateman A, Finn RD. 2018.
The MEROPS database of proteolytic enzymes, their substrates and inhibitors in
2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids
Research 46: D624–D632.
Ristaino JB, Anderson PK, Bebber DP, Brauman KA, Cunniffe NJ,
Fedoroff NV, Finegold C, Garrett KA, Gilligan CA, Jones CM et al.
2021. The persistent threat of emerging plant disease pandemics to global
food security. Proceedings of the National Academy of Sciences, USA 118:
e2022239118.
Robinson MD, McCarthy DJ, Smyth GK. 2010. EDGER: a BIOCONDUCTOR
package for differential expression analysis of digital gene expression data.
Bioinformatics 26: 139–140.
Robinson MD, Oshlack A. 2010. A scaling normalization method for differential
expression analysis of RNA-seq data. Genome Biology 11: R25.
Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H,
Yoshino K, Yoshida K, Matsumura H et al. 2012. Large-scale gene disruption
in Magnaporthe oryzae identifies MC69, a secreted protein required for
infection by monocot and dicot fungal pathogens. PLoS Pathogens 8:
e1002711.
Ó 2023 The Authors
New Phytologist Ó 2023 New Phytologist Foundation
14698137, 2023, 4, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.18790 by Cochrane Japan, Wiley Online Library on [13/04/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
New
Phytologist
Research 1591
Schulze-Lefert P, Panstruga R. 2011. A molecular evolutionary concept
connecting nonhost resistance, pathogen host range, and pathogen speciation.
Trends in Plant Science 16: 117–125.
Shen S, Goodwin PH, Hsiang T. 2001. Infection of Nicotiana species by the
anthracnose fungus, Colletotrichum orbiculare. European Journal of Plant
Pathology 107: 767–773.
Shivas RG, Tan YP, Edwards J, Dinh Q, Maxwell A, Andjic V, Liberato JR,
Anderson C, Beasley DR, Bransgrove K et al. 2016. Colletotrichum species in
Australia. Australasian Plant Pathology 45: 447–464.
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. 2006.
AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Research
34: W435–W439.
Sweigard J, Chumley F, Carroll A, Farrall L, Valent B. 1997. A series of vectors
for fungal transformation. Fungal Genetics Reports 44: 52–53.
Takano Y, Komeda K, Kojima K, 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.
Molecular Plant–Microbe Interactions 14: 1149–1157.
Takano Y, Takayanagi N, Hori H, Ikeuchi Y, Suzuki T, Kimura A, Okuno T.
2006. A gene involved in modifying transfer RNA is required for fungal
pathogenicity and stress tolerance of Colletotrichum lagenarium. Molecular
Microbiology 60: 81–92.
Thordal-Christensen H, Birch PRJ, Spanu PD, Panstruga R. 2018. Why did
filamentous plant pathogens evolve the potential to secrete hundreds of
effectors to enable disease? Molecular Plant Pathology 19: 781–785.
Toru~
no TY, Stergiopoulos I, Coaker G. 2016. Plant-pathogen effectors: cellular
probes interfering with plant defenses in spatial and temporal manners. Annual
Review of Phytopathology 54: 419–441.
Valette N, Renou J, Boutilliat A, Ferna ndez-Gonza lez AJ, Gautier V, Silar P,
Guyeux C, Charr J-C, Cuenot S, Rose C et al. 2021. OSIP1 is a selfassembling DUF3129 protein required to protect fungal cells from toxins and
stressors. Environmental Microbiology 23: 1594–1607.
Xue C, Park G, Choi W, Zheng L, Dean RA, Xu J-R. 2002. Two novel fungal
virulence genes specifically expressed in appressoria of the rice blast fungus.
Plant Cell 14: 2107–2119.
Yamada K, Yamamoto T, Uwasa K, Osakabe K, Takano Y. 2023. The
establishment of multiple knockout mutants of Colletotrichum orbiculare
by CRISPR-Cas9 and Cre-loxP systems. Fungal Genetics and Biology 165:
103777.
Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. 2012. DBCAN: a web resource for
automated carbohydrate-active enzyme annotation. Nucleic Acids Research 40:
W445–W451.
Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, 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.
Molecular Plant–Microbe Interactions 25: 625–636.
Zhang R, Isozumi N, Mori M, Okuta R, Singkaravanit-Ogawa S, Imamura T,
Gan P, Shirasu K, Ohki S, Takano Y. 2021. Fungal effector SIB1 of
Colletotrichum orbiculare has unique structural features and can suppress plant
immunity in Nicotiana benthamiana. Journal of Biological Chemistry 297: 101370.
Supporting Information
Additional Supporting Information may be found online in the
Supporting Information section at the end of the article.
Dataset S1 Amico acid sequences of 13 287 protein-coding genes
of Colletotrichum orbiculare 104-T predicted in this study.
Fig. S1 Cytological observation of cucumber infection by Colletotrichum orbiculare 104-T.
Fig. S2 Differentially expressed genes between in vitro and in
planta conditions.
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Fig. S3 Schematic representation of the experimental design for
quantification of virulence effect on cucumber.
Fig. S19 Appressoria formation of the Top5 quintuple knockout
mutants on different hosts.
Fig. S4 Virulence of isolates from the Colletotrichum orbiculare
species complex on Nicotiana benthamiana.
Fig. S20 Hyphal growth of the Top5 quintuple knockout
mutants on PDA medium.
Fig. S5 Lesion development by Colletotrichum orbiculare on
cucurbit hosts and Nicotiana benthamiana.
Fig. S21 Amino acid sequence of g_04549.
Fig. S6 Cytological observation of Nicotiana benthamiana infection by Colletotrichum orbiculare 104-T.
Fig. S7 Amino acid sequence of EPC1 and comparisons with its
homologs.
Fig. S8 Amino acid sequence of EPC2 and phylogenetic relationships of its homologs.
Fig. S9 Alignment of amino acid sequences of EPC4 homologs.
Fig. S10 Amino acid sequence of EPC3 and phylogenetic relationships and virulence contribution of its homologs.
Fig. S22 Alignment of amino acid sequences of g_09965 homologs from Colletotrichum species.
Fig. S23 Alignment of amino acid sequences of g_13573 homologs from Colletotrichum species.
Fig. S24 Amino acid sequence and phylogenetic relationships of
g_01264 homologs.
Fig. S25 Amino acid sequence and phylogenetic relationships of
g_01222 homologs.
Table S1 Colletotrichum orbiculare isolates used in this study.
Table S2 Primers used in this study.
Fig. S11 Knockout (KO) vectors for generation of EPC multigene KO mutants and maps of genomic regions around the target
genes.
Table S3 Colletotrichum orbiculare strains used in this study.
Table S4 Summary of RNA-seq reads and mapping statistics.
Fig. S12 Quantification of fungal biomass by qPCR.
Table S5 Plasmids used in this study.
Fig. S13 Appressorium formation ratio of EPC knockout strains.
Fig. S14 Measurement of appressorial penetration of inert cellophane membranes by EPC quadruple knockout mutants.
Fig. S15 Differentially expressed genes of Colletotrichum orbiculare during infection of two distantly related host species, cucumber and Nicotiana benthamiana.
Fig. S16 Knockout (KO) vectors for generation of the Top5
multigene KO mutants and maps of genomic regions around the
target genes.
Fig. S17 Genetic complementation of the Top5 quintuple
knockout mutant.
Table S6 List of in planta-induced core secreted protein genes of
Colletotrichum orbiculare.
Table S7 Significantly upregulated Colletotrichum orbiculare
genes on cucumber compared with on Nicotiana benthamiana at
24 hpi.
Table S8 Significantly upregulated Colletotrichum orbiculare
genes on Nicotiana benthamiana compared with on cucumber at
24 hpi.
Please note: Wiley is not responsible for the content or functionality of any Supporting Information supplied by the authors. Any
queries (other than missing material) should be directed to the
New Phytologist Central Office.
Fig. S18 Quantification of host penetration and invasive hyphal
growth of the Top5 quintuple knockout mutants.
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Ó 2023 The Authors
New Phytologist Ó 2023 New Phytologist Foundation
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