An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α.
Disease Resistance
Fungal Proteins
/ metabolism
Fusarium
/ immunology
Host-Pathogen Interactions
/ immunology
Plant Diseases
/ immunology
Plant Proteins
/ genetics
Plants, Genetically Modified
Proteasome Endopeptidase Complex
/ metabolism
Protein Serine-Threonine Kinases
/ genetics
Proteolysis
Trichothecenes
/ metabolism
Triticum
/ immunology
Virulence Factors
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
01 09 2020
01 09 2020
Historique:
received:
11
02
2020
accepted:
06
08
2020
entrez:
3
9
2020
pubmed:
3
9
2020
medline:
22
9
2020
Statut:
epublish
Résumé
Fusarium graminearum is a causal agent of Fusarium head blight (FHB) and a deoxynivalenol (DON) producer. In this study, OSP24 is identified as an important virulence factor in systematic characterization of the 50 orphan secreted protein (OSP) genes of F. graminearum. Although dispensable for growth and initial penetration, OSP24 is important for infectious growth in wheat rachis tissues. OSP24 is specifically expressed during pathogenesis and its transient expression suppresses BAX- or INF1-induced cell death. Osp24 is translocated into plant cells and two of its 8 cysteine-residues are required for its function. Wheat SNF1-related kinase TaSnRK1α is identified as an Osp24-interacting protein and shows to be important for FHB resistance in TaSnRK1α-overexpressing or silencing transgenic plants. Osp24 accelerates the degradation of TaSnRK1α by facilitating its association with the ubiquitin-26S proteasome. Interestingly, TaSnRK1α also interacts with TaFROG, an orphan wheat protein induced by DON. TaFROG competes against Osp24 for binding with the same region of TaSnRKα and protects it from degradation. Overexpression of TaFROG stabilizes TaSnRK1α and increases FHB resistance. Taken together, Osp24 functions as a cytoplasmic effector by competing against TaFROG for binding with TaSnRK1α, demonstrating the counteracting roles of orphan proteins of both host and fungal pathogens during their interactions.
Identifiants
pubmed: 32873802
doi: 10.1038/s41467-020-18240-y
pii: 10.1038/s41467-020-18240-y
pmc: PMC7462860
doi:
Substances chimiques
Fungal Proteins
0
Plant Proteins
0
Trichothecenes
0
Virulence Factors
0
SNF1-related protein kinases
EC 2.7.1.-
Protein Serine-Threonine Kinases
EC 2.7.11.1
Proteasome Endopeptidase Complex
EC 3.4.25.1
deoxynivalenol
JT37HYP23V
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4382Références
Plissonneau, C., Sturchler, A. & Croll, D. The evolution of orphan regions in genomes of a fungal pathogen of wheat. MBio 7, e01231–01216 (2016).
pubmed: 27795389
pmcid: 5082898
doi: 10.1128/mBio.01231-16
Domazet-Loso, T. & Tautz, D. An evolutionary analysis of orphan genes in Drosophila. Genome Res. 13, 2213–2219 (2003).
pubmed: 14525923
pmcid: 403679
doi: 10.1101/gr.1311003
Wissler, L., Gadau, J., Simola, D. F., Helmkampf, M. & Bornberg-Bauer, E. Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biol. Evol. 5, 439–455 (2013).
pubmed: 23348040
pmcid: 3590893
doi: 10.1093/gbe/evt009
Giraldo, M. C. & Valent, B. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11, 800–814 (2013).
pubmed: 24129511
doi: 10.1038/nrmicro3119
Stergiopoulos, I. & de Wit, P. J. Fungal effector proteins. Annu. Rev. Phytopathol. 47, 233–263 (2009).
pubmed: 19400631
doi: 10.1146/annurev.phyto.112408.132637
Khang, C. H. et al. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22, 1388–1403 (2010).
pubmed: 20435900
pmcid: 2879738
doi: 10.1105/tpc.109.069666
Skibbe, D. S., Doehlemann, G., Fernandes, J. & Walbot, V. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328, 89–92 (2010).
pubmed: 20360107
doi: 10.1126/science.1185775
Qi, T. et al. Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat. Mol. Plant 12, 1624–1638 (2019).
pubmed: 31606466
doi: 10.1016/j.molp.2019.09.010
Shen, Q., Liu, Y. Y. & Naqvi, N. I. Fungal effectors at the crossroads of phytohormone signaling. Curr. Opin. Microbiol. 46, 1–6 (2018).
pubmed: 29452844
doi: 10.1016/j.mib.2018.01.006
Selin, C., de Kievit, T. R., Belmonte, M. F. & Fernando, W. G. D. Elucidating the role of effectors in plant-fungal interactions: progress and challenges. Front. Microbiol. 7, 110 (2016).
doi: 10.3389/fmicb.2016.00600
Tanaka, S. et al. Neofunctionalization of the secreted Tin2 effector in the fungal pathogen Ustilago maydis. Nat. Microbiol. 4, 251–257 (2019).
pubmed: 30510169
doi: 10.1038/s41564-018-0304-6
Tanaka, S. et al. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. Elife 3, e01355 (2014).
pubmed: 24473076
pmcid: 3904489
doi: 10.7554/eLife.01355
Djamei, A. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398 (2011).
pubmed: 21976020
doi: 10.1038/nature10454
Boenisch, M. J. & Schafer, W. Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol. 11, 110 (2011).
pubmed: 21798058
pmcid: 3166921
doi: 10.1186/1471-2229-11-110
Zhang, X. W. et al. In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell 24, 5159–5176 (2012).
pubmed: 23266949
pmcid: 3556981
doi: 10.1105/tpc.112.105957
Rittenour, W. R. & Harris, S. D. An in vitro method for the analysis of infection-related morphogenesis in Fusarium graminearum. Mol. Plant Pathol. 11, 361–369 (2010).
pubmed: 20447284
pmcid: 6640345
doi: 10.1111/j.1364-3703.2010.00609.x
Wang, C. F. et al. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog. 7, e1002460 (2011).
pubmed: 22216007
pmcid: 3245316
doi: 10.1371/journal.ppat.1002460
Yun, Y. et al. Functional analysis of the Fusarium graminearum phosphatome. New Phytol. 207, 119–134 (2015).
pubmed: 25758923
doi: 10.1111/nph.13374
Son, H. et al. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 7, e1002310 (2011).
pubmed: 22028654
pmcid: 3197617
doi: 10.1371/journal.ppat.1002310
Jiang, C. et al. An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection. Nat. Microbiol. 4, 1582–1591 (2019).
pubmed: 31160822
doi: 10.1038/s41564-019-0468-8
Voigt, C. A., Schafer, W. & Salomon, S. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42, 364–375 (2005).
pubmed: 15842622
doi: 10.1111/j.1365-313X.2005.02377.x
Qi, P. F. et al. Functional analysis of FgNahG clarifies the contribution of salicylic acid to wheat (Triticum aestivum) resistance against Fusarium head blight. Toxins 11, E59 (2019).
pubmed: 30678154
doi: 10.3390/toxins11020059
Jia, L. J. et al. A linear nonribosomal octapeptide from Fusarium graminearum facilitates cell-to-cell invasion of wheat. Nat. Commun. 10, 922 (2019).
pubmed: 30804501
pmcid: 6389888
doi: 10.1038/s41467-019-08726-9
Audenaert, K., Vanheule, A., Hofte, M. & Haesaert, G. Deoxynivalenol: a major player in the multifaceted response of Fusarium to its environment. Toxins 6, 1–19 (2013).
pubmed: 24451843
pmcid: 3920246
doi: 10.3390/toxins6010001
Van de Walle, J. et al. Deoxynivalenol affects in vitro intestinal epithelial cell barrier integrity through inhibition of protein synthesis. Toxicol. Appl. Pharm. 245, 291–298 (2010).
doi: 10.1016/j.taap.2010.03.012
Jansen, C. et al. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl Acad. Sci. USA 102, 16892–16897 (2005).
pubmed: 16263921
doi: 10.1073/pnas.0508467102
pmcid: 1283850
Shin, S. et al. Transgenic Arabidopsis thaliana expressing a barley UDP-glucosyltransferase exhibit resistance to the mycotoxin deoxynivalenol. J. Exp. Bot. 63, 4731–4740 (2012).
pubmed: 22922639
pmcid: 3428005
doi: 10.1093/jxb/ers141
Perochon, A. et al. TaFROG encodes a pooideae orphan protein that interacts with SnRK1 and enhances resistance to the mycotoxigenic fungus Fusarium graminearum. Plant Physiol. 169, 2895–2906 (2015).
pubmed: 26508775
pmcid: 4677899
Perochon, A. et al. A wheat NAC interacts with an orphan protein and enhances resistance to Fusarium head blight disease. Plant Biotechnol. J. 17, 1892–1904 (2019).
pubmed: 30821405
pmcid: 6737021
doi: 10.1111/pbi.13105
Rawat, N. et al. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat. Genet. 48, 1576–1580 (2016).
pubmed: 27776114
doi: 10.1038/ng.3706
Su, Z. et al. A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nat. Genet. 51, 1099–1105 (2019).
pubmed: 31182809
doi: 10.1038/s41588-019-0425-8
Li, G. et al. Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. Nat. Genet. 51, 1106–1112 (2019).
pubmed: 31182810
doi: 10.1038/s41588-019-0426-7
Cuomo, C. A. et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317, 1400–1402 (2007).
pubmed: 17823352
doi: 10.1126/science.1143708
Zhang, S. & Xu, J. R. Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathog. 10, e1003826 (2014).
pubmed: 24391496
pmcid: 3879361
doi: 10.1371/journal.ppat.1003826
Koeck, M., Hardham, A. R. & Dodds, P. N. The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell. Microbiol. 13, 1849–1857 (2011).
pubmed: 21848815
pmcid: 3218205
doi: 10.1111/j.1462-5822.2011.01665.x
Brown, N. A., Antoniw, J. & Hammond-Kosack, K. E. The predicted secretome of the plant pathogenic fungus Fusarium graminearum: a refined comparative analysis. PLoS ONE 7, e33731 (2012).
pubmed: 22493673
pmcid: 3320895
doi: 10.1371/journal.pone.0033731
Hilt, W. & Wolf, D. H. The ubiquitin-proteasome system: past, present and future. Cell. Mol. Life Sci. 61, 1545 (2004).
pubmed: 15224179
doi: 10.1007/s00018-004-4128-6
Li, T. et al. Effects of the Fhb1 gene on Fusarium head blight resistance and agronomic traits of winter wheat. Crop J. 7, 799–808 (2019).
doi: 10.1016/j.cj.2019.03.005
Peng, Z. et al. Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus. PLoS Genet. 15, e1008272 (2019).
pubmed: 31513573
pmcid: 6741851
doi: 10.1371/journal.pgen.1008272
Zhao, M. et al. Candidate effector Pst_8713 impairs the plant immunity and contributes to virulence of Puccinia striiformis f. sp. tritici. Front. Plant Sci. 9, 1294 (2018).
pubmed: 30254653
pmcid: 6141802
doi: 10.3389/fpls.2018.01294
Gietz, R. D., Schiestl, R. H., Willems, A. R. & Woods, R. A. Studies on the transformation of intact yeast-cells by the Liac/S-DNA/Peg procedure. Yeast 11, 355–360 (1995).
pubmed: 7785336
doi: 10.1002/yea.320110408
Zhou, X., Li, G. & Xu, J. R. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol. Biol. 722, 199–212 (2011).
pubmed: 21590423
doi: 10.1007/978-1-61779-040-9_15
Bruno, K. S., Tenjo, F., Li, L., Hamer, J. E. & Xu, J. R. Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot. Cell 3, 1525–1532 (2004).
pubmed: 15590826
pmcid: 539019
doi: 10.1128/EC.3.6.1525-1532.2004
Lin, H. H. et al. Disulfide connectivity prediction based on structural information without a prior knowledge of the bonding state of cysteines. Comput. Biol. Med. 43, 1941–1948 (2013).
pubmed: 24209939
doi: 10.1016/j.compbiomed.2013.09.008
Zhao, G. P. et al. Activation of the proapoptotic Bcl-2 protein bax by a small molecule induces tumor cell apoptosis. Mol. Cell. Biol. 34, 1198–1207 (2014).
pubmed: 24421393
pmcid: 3993561
doi: 10.1128/MCB.00996-13
Kamoun, S. et al. A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant Microbe 10, 13–20 (1997).
doi: 10.1094/MPMI.1997.10.1.13
McHale, L., Tan, X. P., Koehl, P. & Michelmore, R. W. Plant NBS-LRR proteins: adaptable guards. Genome Biol. 7, 212 (2006).
pubmed: 16677430
pmcid: 1557992
doi: 10.1186/gb-2006-7-4-212
Jossier, M. et al. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J. 59, 316–328 (2009).
pubmed: 19302419
doi: 10.1111/j.1365-313X.2009.03871.x
Takahashi, A., Casais, C., Ichimura, K. & Shirasu, K. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 11777–11782 (2003).
pubmed: 14504384
doi: 10.1073/pnas.2033934100
pmcid: 208834
Perochon, A. et al. The wheat SnRK1alpha family and its contribution to Fusarium toxin tolerance. Plant Sci. 288, 110217 (2019).
pubmed: 31521211
doi: 10.1016/j.plantsci.2019.110217
Zou, S. H., Wang, H., Li, Y. W., Kong, Z. S. & Tang, D. Z. The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol. 218, 298–309 (2018).
pubmed: 29281751
doi: 10.1111/nph.14964
Pauli, S., Rothnie, H. M., Gang, C., He, X. Y. & Hohn, T. The cauliflower mosaic virus 35S promoter extends into the transcribed region. J. Virol. 78, 12120–12128 (2004).
pubmed: 15507598
pmcid: 525061
doi: 10.1128/JVI.78.22.12120-12128.2004
Farras, R. et al. SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. Embo J. 20, 2742–2756 (2001).
pubmed: 11387208
pmcid: 125500
doi: 10.1093/emboj/20.11.2742
Bard, J. A. M. et al. Structure and function of the 26S proteasome. Annu. Rev. Biochem. 87, 697–724 (2018).
pubmed: 29652515
pmcid: 6422034
doi: 10.1146/annurev-biochem-062917-011931
Wang, Q. H. et al. Characterization of the two-speed subgenomes of Fusarium graminearum reveals the fast-speed subgenome specialized for adaption and infection. Front. Plant Sci. 8, 140 (2017).
pubmed: 28261228
pmcid: 5306128
Ma, L. J. & Xu, J. R. Shuffling effector genes through mini-chromosomes. PLoS Genet. 15, e1008345 (2019).
pubmed: 31513572
pmcid: 6742211
doi: 10.1371/journal.pgen.1008345
Lyu, X. L. et al. A small secreted virulence-related protein is essential for the necrotrophic interactions of Sclerotinia sclerotiorum with its host plants. PLoS Pathog. 12, e1005435 (2016).
pubmed: 26828434
pmcid: 4735494
doi: 10.1371/journal.ppat.1005435
Liu, Z. et al. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog. 8, e1002467 (2012).
pubmed: 22241993
pmcid: 3252377
doi: 10.1371/journal.ppat.1002467
Emanuelle, S., Doblin, M. S., Stapleton, D. I., Bacic, A. & Gooley, P. R. Molecular insights into the enigmatic metabolic regulator, SnRK1. Trends Plant Sci. 21, 341–353 (2016).
pubmed: 26642889
doi: 10.1016/j.tplants.2015.11.001
Seo, Y. S. et al. Towards establishment of a rice stress response interactome. PLoS Genet. 7, e1002020 (2011).
pubmed: 21533176
pmcid: 3077385
doi: 10.1371/journal.pgen.1002020
Shen, W., Dallas, M. B., Goshe, M. B. & Hanley-Bowdoin, L. SnRK1 phosphorylation of AL2 delays cabbage leaf curl virus infection in Arabidopsis. J. Virol. 88, 10598–10612 (2014).
pubmed: 24990996
pmcid: 4178870
doi: 10.1128/JVI.00761-14
Szczesny, R. et al. Suppression of the AvrBs1-specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol. 187, 1058–1074 (2010).
pubmed: 20609114
doi: 10.1111/j.1469-8137.2010.03346.x
Hulsmans, S., Rodriguez, M., De Coninck, B. & Rolland, F. The SnRK1 energy sensor in plant biotic interactions. Trends Plant Sci. 21, 648–661 (2016).
pubmed: 27156455
doi: 10.1016/j.tplants.2016.04.008
Filipe, O., De Vleesschauwer, D., Haeck, A., Demeestere, K. & Hofte, M. The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice. Sci. Rep. 8, 3864 (2018).
pubmed: 29497084
pmcid: 5832823
doi: 10.1038/s41598-018-22101-6
Kim, C. Y., Vo, K. T. X., An, G. & Jeon, J. S. A rice sucrose non-fermenting-1 related protein kinase 1, OSK35, plays an important role in fungal and bacterial disease resistance. J. Korean Soc. Appl Biol. Chem. 58, 669–675 (2015).
doi: 10.1007/s13765-015-0089-8
Lu, Z. & Hunter, T. Degradation of activated protein kinases by ubiquitination. Annu. Rev. Biochem. 78, 435–475 (2009).
pubmed: 19489726
pmcid: 2776765
doi: 10.1146/annurev.biochem.013008.092711
Chen, G. et al. MG132 proteasome inhibitor upregulates the expression of connexin 43 in rats with adriamycin-induced heart failure. Mol. Med. Rep. 12, 7595–7602 (2015).
pubmed: 26398314
doi: 10.3892/mmr.2015.4337
Mueller, A. N., Ziemann, S., Treitschke, S., Assmann, D. & Doehlemann, G. Compatibility in the Ustilago maydis-Maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog. 9, e1003177 (2013).
pubmed: 23459172
pmcid: 3573112
doi: 10.1371/journal.ppat.1003177
van Esse, H. P. et al. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20, 1948–1963 (2008).
pubmed: 18660430
pmcid: 2518240
doi: 10.1105/tpc.108.059394
Park, C. H. et al. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24, 4748–4762 (2012).
pubmed: 23204406
pmcid: 3531864
doi: 10.1105/tpc.112.105429
Cuzick, A., Urban, M. & Hammond-Kosack, K. Fusarium graminearum gene deletion mutants map1 and tri5 reveal similarities and differences in the pathogenicity requirements to cause disease on Arabidopsis and wheat floral tissue. New Phytol. 177, 990–1000 (2008).
pubmed: 18179606
doi: 10.1111/j.1469-8137.2007.02333.x
Hou, Z. M. et al. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe 15, 1119–1127 (2002).
doi: 10.1094/MPMI.2002.15.11.1119
Kang, Z. S., Buchenauer, H., Huang, L. L., Han, Q. M. & Zhang, H. C. Cytological and immunocytochemical studies on responses of wheat spikes of the resistant Chinese cv. Sumai 3 and the susceptible cv. Xiaoyan 22 to infection by Fusarium graminearum. Eur. J. Plant Pathol. 120, 383–396 (2008).
doi: 10.1007/s10658-007-9230-9
Ding, S. L. et al. Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot. Cell 8, 867–876 (2009).
pubmed: 19377037
pmcid: 2698311
doi: 10.1128/EC.00048-09
Jonkers, W., Dong, Y. H., Broz, K. & Kistler, H. C. The Wor1-like protein Fgp1 regulates pathogenicity, toxin synthesis and reproduction in the phytopathogenic fungus Fusarium graminearum. PLoS Pathog. 8, e1002724 (2012).
pubmed: 22693448
pmcid: 3364952
doi: 10.1371/journal.ppat.1002724
Hu, S. et al. The cAMP-PKA pathway regulates growth, sexual and asexual differentiation, and pathogenesis in Fusarium graminearum. Mol. Plant Microbe 27, 557–566 (2014).
doi: 10.1094/MPMI-10-13-0306-R
Yin, T. et al. The cyclase-associated protein FgCap1 has both protein kinase A-dependent and -independent functions during deoxynivalenol production and plant infection in Fusarium graminearum. Mol. Plant Pathol. 19, 552–563 (2018).
pubmed: 28142217
doi: 10.1111/mpp.12540
Liu, H. et al. Two Cdc2 kinase genes with distinct functions in vegetative and infectious hyphae in Fusarium graminearum. PLoS Pathog. 11, e1004913 (2015).
pubmed: 26083253
pmcid: 4470668
doi: 10.1371/journal.ppat.1004913
Gu, Q., Chen, Y., Liu, Y., Zhang, C. Q. & Ma, Z. H. The transmembrane protein FgSho1 regulates fungal development and pathogenicity via the MAPK module Ste50-Ste11-Ste7 in Fusarium graminearum. New Phytol. 206, 315–328 (2015).
pubmed: 25388878
doi: 10.1111/nph.13158
Urban, M., Daniels, S., Mott, E. & Hammond-Kosack, K. Arabidopsis is susceptible to the cereal ear blight fungal pathogens Fusarium graminearum and Fusarium culmorum. Plant J. 32, 961–973 (2002).
pubmed: 12492838
doi: 10.1046/j.1365-313X.2002.01480.x
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142
pmcid: 4655817
doi: 10.1038/nmeth.3317
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Dimont, E., Shi, J., Kirchner, R. & Hide, W. edgeRun: an R package for sensitive, functionally relevant differential expression discovery using an unconditional exact test. Bioinformatics 31, 2589–2590 (2015).
pubmed: 25900919
pmcid: 4514933
doi: 10.1093/bioinformatics/btv209
Ruepp, A. et al. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32, 5539–5545 (2004).
pubmed: 15486203
pmcid: 524302
doi: 10.1093/nar/gkh894
Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).
doi: 10.1093/bioinformatics/bti610
pubmed: 16081474
Jacobs, K. A. et al. A genetic selection for isolating cDNAs encoding secreted proteins. Gene 198, 289–296 (1997).
pubmed: 9370294
doi: 10.1016/S0378-1119(97)00330-2
Oh, S. K. et al. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21, 2928–2947 (2009).
pubmed: 19794118
pmcid: 2768934
doi: 10.1105/tpc.109.068247
Koschwanez, J. H., Foster, K. R. & Murray, A. W. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol. 9, e1001122 (2011).
pubmed: 21857801
doi: 10.1371/journal.pbio.1001122
Dou, D. et al. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20, 1930–1947 (2008).
pubmed: 18621946
pmcid: 2518231
doi: 10.1105/tpc.107.056093
Han, Z. F., Hunter, D. M., Sibbald, S., Zhang, J. S. & Tian, L. Biological activity of the tzs gene of nopaline Agrobacterium tumefaciens GV3101 in plant regeneration and genetic transformation. Mol. Plant–Microbe Interact. 26, 1359–1365 (2013).
pubmed: 24088018
doi: 10.1094/MPMI-04-13-0106-R
Xu, Q. et al. An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function. Nat. Commun. 10, 5571 (2019).
pubmed: 31804478
pmcid: 6895047
doi: 10.1038/s41467-019-13487-6
Ai, H. W., Shaner, N. C., Cheng, Z., Tsien, R. Y. & Campbell, R. E. Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry 46, 5904–5910 (2007).
pubmed: 17444659
doi: 10.1021/bi700199g
Walter, M. et al. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428–438 (2004).
pubmed: 15469500
doi: 10.1111/j.1365-313X.2004.02219.x
Shen, M. et al. Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PLoS ONE 10, e0123418 (2015).
pubmed: 25884726
pmcid: 4401685
doi: 10.1371/journal.pone.0123418
Qing, G. et al. Cold-shock induced high-yield protein production in Escherichia coli. Nat. Biotechnol. 22, 877–882 (2004).
pubmed: 15195104
doi: 10.1038/nbt984
Peleg, Y. & Unger, T. Resolving bottlenecks for recombinant protein expression in E. coli. Methods Mol. Biol. 800, 173–186 (2012).
pubmed: 21964789
doi: 10.1007/978-1-61779-349-3_12
Swaffield, J. C. & Johnston, S. A. Affinity purification of proteins binding to GST fusion proteins. Curr. Protoc. Mol. Biol. Chapter 20, Unit 20 22 (2001).
Kong, L. et al. A Phytophthora effector manipulates host histone acetylation and reprograms defense gene expression to promote infection. Curr. Biol. 27, 981–991 (2017).
pubmed: 28318979
doi: 10.1016/j.cub.2017.02.044
Wang, F. et al. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21, 2378–2390 (2009).
pubmed: 19717618
pmcid: 2751948
doi: 10.1105/tpc.108.065433
Kong, L. et al. Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat. Commun. 6, 8630 (2015).
pubmed: 26482222
doi: 10.1038/ncomms9630
Mann, D. G. et al. Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species. Plant Biotechnol. J. 10, 226–236 (2012).
pubmed: 21955653
doi: 10.1111/j.1467-7652.2011.00658.x
Zeng, L., Deng, R., Guo, Z., Yang, S. & Deng, X. Genome-wide identification and characterization of Glyceraldehyde-3-phosphate dehydrogenase genes family in wheat (Triticum aestivum). BMC Genomics 17, 240 (2016).
pubmed: 26984398
pmcid: 4793594
doi: 10.1186/s12864-016-2527-3
Li, H. et al. A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility. Elife 7, e40039 (2018).
pubmed: 30346270
pmcid: 6249003
doi: 10.7554/eLife.40039