Unraveling the role of effector proteins in Bipolaris oryzae infecting North East Indian rice cultivars through time-course transcriptomics analysis

Ahn, 2004, Extracellular matrix protein gene, EMP1, is required for appressorium formation and pathogenicity of the rice blast fungus, Magnaporthe grisea, Mol. Cell., 17, 166 Almagro Armenteros, 2019, SignalP 5.0 improves signal peptide predictions using deep neural networks, Nat. Biotechnol., 37, 420, 10.1038/s41587-019-0036-z Arya, 2022, The multifaceted roles of fungal cutinases during infection, Journal of Fungi, 8, 10.3390/jof8020199 Bhakta, 2017, Evaluation of rice varieties against multiple diseases under middle IGP of Bihar, J. Pure Appl. Microbiol., 11, 335, 10.22207/JPAM.11.1.42 Bushnell, 2017, BBMerge – accurate paired shotgun read merging via overlap, PLoS One, 12, 10.1371/journal.pone.0185056 Chakraborty, 2020, Dispersal of airborne pathogenic conidia of Bipolaris oryzae inciting brown spot disease of paddy in West Bengal, India, J. Trop. Agric., 58, 199 Channakeshava, 2018, Performance of paddy varieties against Brown leaf spot disease under flooded conditions in mandya district, Karnataka, Int. J. Curr. Microbiol. App. Sci, 7, 33, 10.20546/ijcmas.2018.712.004 Chen, 2013, Identification and characterization of in planta-expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice, Mol. Plant Microbe Interact., 26, 191, 10.1094/MPMI-05-12-0117-R Chittem, 2020, Transcriptome analysis of the plant pathogen Sclerotinia sclerotiorum interaction with resistant and susceptible canola (Brassica napus) lines, PLoS One, 15, 10.1371/journal.pone.0229844 Condon, 2013, Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens, PLoS Genet., 9, 10.1371/journal.pgen.1003233 Corwin, 2017, Quantitative resistance: more than just perception of a pathogen, Plant Cell, 29, 655, 10.1105/tpc.16.00915 Darino, 2021, Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling, New Phytol., 229, 3393, 10.1111/nph.17116 Dariush, 2020, Screening brown spot resistance in rice genotypes at the seedling stage under water stress and irrigated conditions, Arch. Phytopathol. Plant Protect., 53, 247, 10.1080/03235408.2020.1741855 Dhungana, 2020, Screening rice genotypes for Brown spot disease resistance, Tunisian Journal of Plant Protection, 15, 10.52543/tjpp.15.2.1 Doehlemann, 2017, Plant pathogenic fungi, Microbiol. Spectr., 5, 1 Figueroa, 2021, Tactics of host manipulation by intracellular effectors from plant pathogenic fungi, Curr. Opin. Plant Biol., 62, 10.1016/j.pbi.2021.102054 Geoghegan, 2016, Chitosan mediates germling adhesion in Magnaporthe oryzae and is required for surface sensing and germling morphogenesis, PLoS Pathog., 12, 10.1371/journal.ppat.1005703 Guyon, 2014, Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum, BMC Genom., 15, 336, 10.1186/1471-2164-15-336 Jiang, 2020, An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α, Nat. Commun., 11, 4382, 10.1038/s41467-020-18240-y Jiang, H., Cao, Q., Wang, X., Lv, W., Wang, Y., Pectate lyase genes abundantly expressed during the infection regulate morphological development of Colletotrichum camelliae and CcPEL16 is required for full virulence to tea plants. mSphere 0, e00677-00622. Kawahara, 2012, Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction, PLoS One, 7, 10.1371/journal.pone.0049423 Kim, 2015, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, 12, 357, 10.1038/nmeth.3317 Kim, 2016, Kingdom-wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association, Front. Plant Sci., 7, 10.3389/fpls.2016.00186 Kim, 2020, Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming, Nat. Commun., 11, 1, 10.1038/s41467-020-19624-w Kohls, 1987, Wild rice yield losses associated with growth-stage-specific fungal brown spot epidemics, Plant Dis., 71, 419, 10.1094/PD-71-0419 Kubicek, 2014, Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi, Annu. Rev. Phytopathol., 52, 427, 10.1146/annurev-phyto-102313-045831 Laluk, 2010, Necrotroph attacks on plants: wanton destruction or covert extortion?, Arabidopsis Book, 8, e0136, 10.1199/tab.0136 Lanver, 2018, The biotrophic development of Ustilago maydis studied by RNA-seq analysis, Plant Cell, 30, 300, 10.1105/tpc.17.00764 Li, 2003, Molecular evidence that the extracellular cutinase Pbc1 is required for pathogenicity of pyrenopeziza brassicae on oilseed Rape, Mol. Plant Microbe Interact., 16, 545, 10.1094/MPMI.2003.16.6.545 Li, 2020, Apoplastic cell death-inducing proteins of filamentous plant pathogens: roles in plant-pathogen interactions, Front. Genet., 11 Li, 2020, Magnaporthe oryzae auxiliary activity protein MoAa91 functions as chitin-binding protein to induce appressorium formation on artificial inductive surfaces and suppress plant immunity, mBio, 11, 10.1128/mBio.03304-19 Liang, 2018, Mechanisms of broad host range necrotrophic pathogenesis in Sclerotinia sclerotiorum, Phytopathology, 108, 1128, 10.1094/PHYTO-06-18-0197-RVW Liao, 2014, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Liu, 2021, First report of bipolaris oryzae causing leaf spot on cultivated wild rice (oryza rufipogon) in China, Plant Dis., 105, 1857, 10.1094/PDIS-11-20-2529-PDN Lombard, 2013, The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res., 42, D490, 10.1093/nar/gkt1178 Lopez, 2018, Genome-wide analysis of corynespora cassiicola leaf fall disease putative effectors, Front. Microbiol., 9, 10.3389/fmicb.2018.00276 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Ma, 2022, Botrytis cinerea transcription factor BcXyr1 regulates (Hemi-)Cellulase production and fungal virulence, mSystems, 7, 10.1128/msystems.01042-22 Marwein, 2022, Transcriptome-wide analysis of North-East Indian rice cultivars in response to Bipolaris oryzae infection revealed the importance of early response to the pathogen in suppressing the disease progression, Gene, 809, 10.1016/j.gene.2021.146049 Matsumoto, 2017, Identification of QTLs for rice brown spot resistance in backcross inbred lines derived from a cross between Koshihikari and CH45, Breed Sci., 67, 540, 10.1270/jsbbs.17057 Matsumoto, 2021, Breeding and characterization of the world's first practical rice variety with resistance to brown spot (Bipolaris oryzae) bred using marker-assisted selection, Breed Sci., 71, 474, 10.1270/jsbbs.21023 Nyvall, 1999, Development of fungal Brown spot and spot blotch on cultivated wild rice in Minnesota, Plant Dis., 83, 936, 10.1094/PDIS.1999.83.10.936 Ota, 2021, QTL analysis for brown spot resistance in American rice cultivar 'Dawn', Breed Sci., 71, 491, 10.1270/jsbbs.21015 Padmanabhan, 1973, The great bengal famine, Annu. Rev. Phytopathol., 11, 11, 10.1146/annurev.py.11.090173.000303 Peng, 2017, Transcriptome analysis of Sclerotinia sclerotiorum at different infection stages on Brassica napus, Curr. Microbiol., 74, 1237, 10.1007/s00284-017-1309-8 Petit-Houdenot, 2017, Complex interactions between fungal avirulence genes and their corresponding plant resistance genes and consequences for disease resistance management, Front. Plant Sci., 8, 10.3389/fpls.2017.01072 Polonio, 2021, A haustorial-expressed lytic polysaccharide monooxygenase from the cucurbit powdery mildew pathogen Podosphaera xanthii contributes to the suppression of chitin-triggered immunity, Mol. Plant Pathol., 22, 580, 10.1111/mpp.13045 Rafiei, 2021, The role of glycoside hydrolases in phytopathogenic fungi and oomycetes virulence, Int. J. Mol. Sci., 22, 10.3390/ijms22179359 Rajarammohan, 2021, Redefining plant-necrotroph interactions: the thin line between hemibiotrophs and necrotrophs, Front. Microbiol., 12, 10.3389/fmicb.2021.673518 Rajput, 2017, Effect of temperature on growth and sporulation of rice leaf blast pathogen Magnaporthe oryzae, International Journal of Current Microbiology and Applied Sciences, 6, 394, 10.20546/ijcmas.2017.603.045 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Saitoh, 2013, MoST1 encoding a hexose transporter-like protein is involved in both conidiation and mycelial melanization of Magnaporthe oryzae, FEMS Microbiol. Lett., 352 Sato, 2015, Confirming a major QTL and finding additional loci responsible for field resistance to brown spot (Bipolaris oryzae) in rice, Breed Sci., 65, 170, 10.1270/jsbbs.65.170 Schwanck, 2015, Bipolaris oryzae seed borne inoculum and brown spot epidemics in the subtropical lowland rice-growing region of Brazil, Eur. J. Plant Pathol., 142, 875, 10.1007/s10658-015-0659-y Shabbir, 2022, Magnaporthe oryzae chloroplast targeting endo-β-1,4-xylanase I MoXYL1A regulates conidiation, appressorium maturation and virulence of the rice blast fungus, Rice, 15, 44, 10.1186/s12284-022-00584-2 Shao, 2021, Effectors of plant necrotrophic fungi, Front. Plant Sci., 12, 10.3389/fpls.2021.687713 Shoemaker, 1959, Nomenclature of drechslera and bipolaris, grass parasites segregated from ‘helminthosporium’, Can. J. Bot., 37, 879, 10.1139/b59-073 Singh, 2014, 201 Snelders, 2018, Plant pathogen effector proteins as manipulators of host microbiomes?, Mol. Plant Pathol., 19, 257, 10.1111/mpp.12628 Sperschneider, 2021 Stecher, 2020, Molecular Evolutionary Genetics Analysis (MEGA) for macOS, Mol. Biol. Evol., 37, 1237, 10.1093/molbev/msz312 Sunder, 2014, Brown spot of rice: an overview, Indian Phytopathol., 67 Tamura, 2021, MEGA11: molecular evolutionary genetics analysis version 11, Mol. Biol. Evol., 38, 3022, 10.1093/molbev/msab120 Tian, 2017, The biological activities of sesterterpenoid-type ophiobolins, Mar. Drugs, 15, 229, 10.3390/md15070229 Törönen, 2018, PANNZER2: a rapid functional annotation web server, Nucleic Acids Res., 46, W84, 10.1093/nar/gky350 Toruño, 2016, Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners, Annu. Rev. Phytopathol., 54, 419, 10.1146/annurev-phyto-080615-100204 Urban, 2019, PHI-base: the pathogen–host interactions database, Nucleic Acids Res., 48, D613 Van Vu, 2012, Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae, Mol. Plant Microbe Interact., 25, 1135, 10.1094/MPMI-02-12-0043-R Wang, 2021, A bacterial kinase phosphorylates OSK1 to suppress stomatal immunity in rice, Nat. Commun., 12, 5479, 10.1038/s41467-021-25748-4 Wegner, 2022, Gene deletion and constitutive expression of the pectate lyase gene 1 (MoPL1) lead to diminished virulence of Magnaporthe oryzae, J. Microbiol., 60, 79 Westrick, 2019, Gene regulation of Sclerotinia sclerotiorum during infection of Glycine max: on the road to pathogenesis, BMC Genom., 20, 157, 10.1186/s12864-019-5517-4 Zhang, 2018, dbCAN2: a meta server for automated carbohydrate-active enzyme annotation, Nucleic Acids Res., 46, W95, 10.1093/nar/gky418 Zhang, 2018, Novel fungal pathogenicity and leaf defense strategies are revealed by simultaneous transcriptome analysis of colletotrichum fructicola and strawberry infected by this fungus, Front. Plant Sci., 9 Zhang, 2019, Plant-necrotroph co-transcriptome networks illuminate a metabolic battlefield, Elife, 13 Zhang, 2022, An endoglucanase secreted by Ustilago esculenta promotes fungal proliferation, J Fungi, 8 Zuppini, 2005, An endopolygalacturonase from Sclerotinia sclerotiorum induces calcium-mediated signaling and programmed cell death in soybean cells, Mol. Plant Microbe Interact., 18, 849, 10.1094/MPMI-18-0849