vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJGB-23-115vavilov-4011Research ArticleИММУНИТЕТ РАСТЕНИЙ К БОЛЕЗНЯМPLANT IMMUNITYВлияние салициловой и жасмоновой кислот на активность генов SnAGO гриба Stagonospora nodorum Berk. в культуре и при инфицировании растений пшеницыThe effect of salicylic and jasmonic acids on the activity of SnAGO genes in the fungus Stagonospora nodorum Berk. in in vitro culture and during infection of wheat plantshttps://orcid.org/0000-0002-3743-9928ШеинМ. Ю.SheinM. Yu.

Уфа

Ufa

https://orcid.org/0000-0003-2346-3502БурхановаГ. Ф.BurkhanovaG. F.

Уфа

Ufa

https://orcid.org/0000-0002-5707-3265МаксимовИ. В.MaksimovI. V.

Уфа

Ufa

igor.mak2011@yandex.ruИнститут биохимии и генетики – обособленное структурное подразделение Уфимского федерального исследовательского центра Российской академии наукРоссияInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre of the Russian Academy of SciencesRussian Federation2023291220232781000-­1009Copyright © Шеин М.Ю., Бурханова Г.Ф., Максимов И.В., 20232023Шеин М.Ю., Бурханова Г.Ф., Максимов И.В.Shein M.Y., Burkhanova G.F., Maksimov I.V.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4011

РНК-­интерференция представляет собой механизм подавления генов, играющий важную роль в генетической регуляции у эукариот. Белки Argonaute (AGO) занимают центральное место в сложной системе явления РНК-­интерференции. Однако их роль в этом механизме, как в организме растения-­хозяина, так и у патогена, до сих пор полностью не исследована. Мы провели идентификацию и филогенетический анализ генов SnAGO1, SnAGO2, SnAGO3 и SnAGO18 патогенного гриба Stagonospora nodorum Berk., возбудителя септориоза пшеницы, и проанализировали их экспрессию в условиях инфицирования растений с различной степенью устойчивости к патогену. Уровень экспрессии оценивали на фоне иммунизации растений индукторами устойчивости: салициловой и жасмоновой кислотами. Также изучена активность указанных генов в культуре гриба при непосредственном воздействии индукторов устойчивости на мицелий гриба. Выявленная более ранняя активация генов SnAGO в культуре под влиянием салициловой и жасмоновой кислот указывает на их чувствительность к ним. В системе in vivo обнаружено, что иммунизация растений индуцирует накопление транскриптов SnAGO патогена. При этом гены SnAGO гриба S. nodorum при взаимодействии с растительными клетками реагировали в зависимости от степени устойчивости хозяина: наиболее высокий уровень транскриптов наблюдался в устойчивом сорте. Таким образом, полученные данные доказывают, что гены SnAGO гриба S. nodorum эффективно взаимодействуют с системой защиты хозяина в прямой зависимости от степени устойчивости последнего к патогену. Предложено использовать отношение транскрипционной активности грибного референсного гена SnTub к хозяйскому гену TaRLI в качестве маркера развития болезни в начальный период инфекционного процесса.

RNA interference is a gene silencing mechanism that plays an important role in genetic regulation in a number of eukaryotes. Argonaute (AGO) proteins are central to the complex RNA interference system. However, their role in this mechanism, both in the host plant organism and in the pathogen, has not yet been fully elucidated. In this work, we identified and phylogenetically analyzed the SnAGO1, SnAGO2, SnAGO3, and SnAGO18 genes of the pathogenic fungus Stagonospora nodorum Berk., and analyzed their expression under conditions of infection of plants with varying degrees of resistance to the pathogen. The expression level against the background of plant immunization with the resistance inducers salicylic and jasmonic acids was assessed. In addition, the activity of these genes in the culture of the fungus in vitro was studied under the direct influence of resistance inducers on the mycelium of the fungus. Earlier activation of the SnAGO genes in in vitro culture under the influence of salicylic and jasmonic acids suggests their sensitivity to it. In an in vivo system, plant immunization to induce the accumulation of pathogen SnAGO transcripts was found. At the same time, the SnAGO genes of the fungus S. nodorum, when interacting with plant cells, reacted depending on the degree of host resistance: the highest level of transcripts in the resistant variety was observed. Thus, our data prove that the SnAGO genes of the fungus S. nodorum effectively interact with the host defense system in direct proportion to the degree of resistance of the latter to the pathogen. It was proposed to use the ratio of the transcriptional activity of the fungal reference gene SnTub to the host TaRLI gene as a marker of disease development in the initial period of the infectious process.

РНК­интерференциягены SnAGOгриб Stagonospora nodorumмягкая пшеницапатогенезсалициловая кислотажасмоновая кислотаRNA interferenceSnAGO genesfungus Stagonospora nodorumcommon wheatpathogenesissalicylic acidjasmonic acidThis work was supported by the Russian Foundation for Basic Research, project No. 20­34­90004.ReferencesAhmed F.F., Hossen M.I., Sarkar M.A.R., Konak J.N., Zohra F.T., Shoyeb M., Mondal S. Genome-wide identification of DCL, AGO and RDR gene families and their associated functional regulatory elements analyses in banana (Musa acuminata). PLoS One. 2021; 16(9):e0256873. DOI 10.1371/journal.pone.0256873Ahmed F.F., Hossen M.I., Sarkar M.A.R., Konak J.N., Zohra F.T., Shoyeb M., Mondal S. Genome-wide identification of DCL, AGO and RDR gene families and their associated functional regulatory elements analyses in banana (Musa acuminata). PLoS One. 2021; 16(9):e0256873. DOI 10.1371/journal.pone.0256873Campo S., Gilbert K.B., Carrington J.C. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLoS Pathog. 2016;12:e1005640. DOI 10.1371/journal.ppat.1005640Campo S., Gilbert K.B., Carrington J.C. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLoS Pathog. 2016;12:e1005640. DOI 10.1371/journal.ppat.1005640Chen Y., Gao Q., Huang M., Liu Y., Liu Z., Liu X., Ma Z. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci. Rep. 2015;5:12500. DOI 10.1038/srep12500Chen Y., Gao Q., Huang M., Liu Y., Liu Z., Liu X., Ma Z. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci. Rep. 2015;5:12500. DOI 10.1038/srep12500Choi J., Kim T., Jeon J., Wu J., Song H., Asiegbu F.O., Lee Y.H. funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genomics. 2014;15(Suppl. 9):S14. DOI 10.1186/1471-2164-15-S9-S14Choi J., Kim T., Jeon J., Wu J., Song H., Asiegbu F.O., Lee Y.H. funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genomics. 2014;15(Suppl. 9):S14. DOI 10.1186/1471-2164-15-S9-S14Dunker F., Trutzenberg A., Rothenpieler J.S., Kuhn S., Pröls R., Schreiber T., Tissier A., Kemen A., Kemen E., Hückelhoven R., Weiberg A. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. Elife. 2020;9:e56096. DOI 10.7554/eLife.56096Dunker F., Trutzenberg A., Rothenpieler J.S., Kuhn S., Pröls R., Schreiber T., Tissier A., Kemen A., Kemen E., Hückelhoven R., Weiberg A. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. Elife. 2020;9:e56096. DOI 10.7554/eLife.56096Giménez M.J., Pistón F., Atienza S.G. Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta. 2011;233(1):163-173. DOI 10.1007/s00425-010-1290-yGiménez M.J., Pistón F., Atienza S.G. Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta. 2011;233(1):163-173. DOI 10.1007/s00425-010-1290-yFeng H., Xu M., Liu Y., Gao X., Yin Z., Voegele R.T., Huang L. The distinct roles of Argonaute protein 2 in the growth, stress responses and pathogenicity of the apple tree canker pathogen. Forest Pathol. 2017;47(5):e12354. DOI 10.1111/efp.12354Feng H., Xu M., Liu Y., Gao X., Yin Z., Voegele R.T., Huang L. The distinct roles of Argonaute protein 2 in the growth, stress responses and pathogenicity of the apple tree canker pathogen. Forest Pathol. 2017;47(5):e12354. DOI 10.1111/efp.12354Fraaije B.A., Lovel D.J., Baldwin S. Septoria epidemics on wheat: combined use of visual assessment and PCR-based diagnostics of identity mechanism of diseases escape. Plant Protect. Sci. 2002; 38(11):421-424. DOI 10.17221/10512-PPSFraaije B.A., Lovel D.J., Baldwin S. Septoria epidemics on wheat: combined use of visual assessment and PCR-based diagnostics of identity mechanism of diseases escape. Plant Protect. Sci. 2002; 38(11):421-424. DOI 10.17221/10512-PPSHane J.K., Lowe R.G., Solomon P.S., Tan K.C., Schoch C.L., Spatafora J.W., Crous P.W., Kodira C., Birren B.W., Galagan J.E., Torriani S.F., McDonald B.A., Oliver R.P. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell. 2007;19(11): 3347-3368. DOI 10.1105/tpc.107.052829Hane J.K., Lowe R.G., Solomon P.S., Tan K.C., Schoch C.L., Spatafora J.W., Crous P.W., Kodira C., Birren B.W., Galagan J.E., Torriani S.F., McDonald B.A., Oliver R.P. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell. 2007;19(11): 3347-3368. DOI 10.1105/tpc.107.052829Jeseničnik T., Štajner N., Radišek S., Jakše J. RNA interference core components identified and characterized in Verticillium nonalfalfae, a vascular wilt pathogenic plant fungi of hops. Sci. Rep. 2019; 9(1):8651. DOI 10.1038/s41598-019-44494-8Jeseničnik T., Štajner N., Radišek S., Jakše J. RNA interference core components identified and characterized in Verticillium nonalfalfae, a vascular wilt pathogenic plant fungi of hops. Sci. Rep. 2019; 9(1):8651. DOI 10.1038/s41598-019-44494-8Jo S.M., Ayukawa Y., Yun S.H., Komatsu K., Arie T. A putative RNA silencing component protein FoQde-2 is involved in virulence of the tomato wilt fungus Fusarium oxysporum f. sp. lycopersici. J. Gen. Plant Pathol. 2018;84:395-398. DOI 10.1007/s10327-018-0800-9Jo S.M., Ayukawa Y., Yun S.H., Komatsu K., Arie T. A putative RNA silencing component protein FoQde-2 is involved in virulence of the tomato wilt fungus Fusarium oxysporum f. sp. lycopersici. J. Gen. Plant Pathol. 2018;84:395-398. DOI 10.1007/s10327-018-0800-9Kettles G.J., Hofinger B.J., Hu P., Bayon C., Rudd J.J., Balmer D., Courbot M., Hammond-Kosack K.E., Scalliet G., Kanyuka K. sRNA profiling combined with gene function analysis reveals a lack of evidence for cross-kingdom RNAi in the wheat – Zymoseptoria tritici pathosystem. Front. Plant Sci. 2019;10:892. DOI 10.3389/fpls.2019.00892Kettles G.J., Hofinger B.J., Hu P., Bayon C., Rudd J.J., Balmer D., Courbot M., Hammond-Kosack K.E., Scalliet G., Kanyuka K. sRNA profiling combined with gene function analysis reveals a lack of evidence for cross-kingdom RNAi in the wheat – Zymoseptoria tritici pathosystem. Front. Plant Sci. 2019;10:892. DOI 10.3389/fpls.2019.00892Lee W.S., Fu S.F., Li Z., Murphy A.M., Dobson E.A., Garland L., Chaluvadi S.R., Lewsey M.G., Nelson R.S., Carr J.P. Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana. BMC Plant Biol. 2016;16:15. DOI 10.1186/s12870-016-0705-8Lee W.S., Fu S.F., Li Z., Murphy A.M., Dobson E.A., Garland L., Chaluvadi S.R., Lewsey M.G., Nelson R.S., Carr J.P. Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana. BMC Plant Biol. 2016;16:15. DOI 10.1186/s12870-016-0705-8Ma X., Wiedmer J., Palma-Guerrero J. Small RNA bidirectional crosstalk during the interaction between wheat and Zymoseptoria tritici. Front. Plant Sci. 2020;10:1669. DOI 10.3389/fpls.2019.01669Ma X., Wiedmer J., Palma-Guerrero J. Small RNA bidirectional crosstalk during the interaction between wheat and Zymoseptoria tritici. Front. Plant Sci. 2020;10:1669. DOI 10.3389/fpls.2019.01669Maksimov I.V., Valeev A.Sh., Safin R.F. Acetylation degree of chitin in the protective response of wheat plants. Biochemistry (Moscow). 2011;76(12):1342-1346. DOI 10.1134/S0006297911120078Maksimov I.V., Valeev A.Sh., Safin R.F. Acetylation degree of chitin in the protective response of wheat plants. Biochemistry (Moscow). 2011;76(12):1342-1346. DOI 10.1134/S0006297911120078Marchenkova A.A., Nettevich E.D., Tushinsky T.Yu. Resistance of spring wheat to septoria blight. Vestnik Selskokhozyaystvennoy Nauki = Herald of Agricultural Sciences. 1991;7:110-115 (in Russian)Marchenkova A.A., Nettevich E.D., Tushinsky T.Yu. Resistance of spring wheat to septoria blight. Vestnik Selskokhozyaystvennoy Nauki = Herald of Agricultural Sciences. 1991;7:110-115 (in Russian)Meng H., Wang Z., Wang Y., Zhu H., Huang B. Dicer and Argonaute genes involved in RNA interference in the entomopathogenic fungus Metarhizium robertsii. Appl. Environ. Microbiol. 2017;83(7): e03230-16. DOI 10.1128/AEM.03230-16Meng H., Wang Z., Wang Y., Zhu H., Huang B. Dicer and Argonaute genes involved in RNA interference in the entomopathogenic fungus Metarhizium robertsii. Appl. Environ. Microbiol. 2017;83(7): e03230-16. DOI 10.1128/AEM.03230-16McCombe C.L., Greenwood J.R., Solomon P.S., Williams S.J. Molecular plant immunity against biotrophic, hemibiotrophic, and necrotrophic fungi. Essays Biochem. 2022;66(5):581-593. DOI 10.1042/EBC20210073McCombe C.L., Greenwood J.R., Solomon P.S., Williams S.J. Molecular plant immunity against biotrophic, hemibiotrophic, and necrotrophic fungi. Essays Biochem. 2022;66(5):581-593. DOI 10.1042/EBC20210073Neupane A., Feng C., Mochama P.K., Saleem H., Lee Marzano S.Y. Roles of Argonautes and Dicers on Sclerotinia sclerotiorum antiviral RNA silencing. Front. Plant Sci. 2019;10:976. DOI 10.3389/fpls.2019.00976Neupane A., Feng C., Mochama P.K., Saleem H., Lee Marzano S.Y. Roles of Argonautes and Dicers on Sclerotinia sclerotiorum antiviral RNA silencing. Front. Plant Sci. 2019;10:976. DOI 10.3389/fpls.2019.00976Oliver R.P., Friesen T.L., Faris J.D., Solomon P.S. Stagonospora nodorum: From pathology to genomics and host resistance. Annu. Rev. Phytopathol. 2012;50:23-43. DOI 10.1146/annurev-phyto-081211-173019Oliver R.P., Friesen T.L., Faris J.D., Solomon P.S. Stagonospora nodorum: From pathology to genomics and host resistance. Annu. Rev. Phytopathol. 2012;50:23-43. DOI 10.1146/annurev-phyto-081211-173019Pradhan M., Pandey P., Baldwin I.T., Pandey S.P. Argonaute 4 modulates resistance to Fusarium brachygibbosum infection by regulating Jasmonic acid signaling. Plant Physiol. 2020;184(2):1128-1152. DOI 10.1104/pp.20.00171Pradhan M., Pandey P., Baldwin I.T., Pandey S.P. Argonaute 4 modulates resistance to Fusarium brachygibbosum infection by regulating Jasmonic acid signaling. Plant Physiol. 2020;184(2):1128-1152. DOI 10.1104/pp.20.00171Raman V., Simon S.A., Demirci F., Nakano M., Meyers B.C., Donofrio N.M. Small RNA functions are required for growth and development of Magnaporthe oryzae. Mol. Plant Microbe Interact. 2017;30(7):517-530. DOI 10.1094/MPMI-11-16-0236-RRaman V., Simon S.A., Demirci F., Nakano M., Meyers B.C., Donofrio N.M. Small RNA functions are required for growth and development of Magnaporthe oryzae. Mol. Plant Microbe Interact. 2017;30(7):517-530. DOI 10.1094/MPMI-11-16-0236-RShein M.Yu., Burkhanova G.F., Merzlyakova A.Yu., Maksimov I.V. Changes in transcriptional activity of TaAGO2 and TaAGO4 genes in wheat plants at infection with Stagonospora nodorum Berk. Trudy Kubanskogo Gosudarstvennogo Agrarnogo Universiteta = Works of the Kuban State Agrarian University. 2021;5(92):196-200. DOI 10.21515/1999-1703-92-196-200 (in Russian)Shein M.Yu., Burkhanova G.F., Merzlyakova A.Yu., Maksimov I.V. Changes in transcriptional activity of TaAGO2 and TaAGO4 genes in wheat plants at infection with Stagonospora nodorum Berk. Trudy Kubanskogo Gosudarstvennogo Agrarnogo Universiteta = Works of the Kuban State Agrarian University. 2021;5(92):196-200. DOI 10.21515/1999-1703-92-196-200 (in Russian)Shen D., Suhrkamp I., Wang Y., Liu S., Menkhaus J., Verreet J.A., Fan L., Cai D. Identification and characterization of microRNAs in oilseed rape (Brassica napus) responsive to infection with the pathogenic fungus Verticillium longisporum using Brassica AA (Brassica rapa) and CC (Brassica oleracea) as refer. New Phytol. 2014; 204(3):577-594. DOI 10.1111/nph.12934Shen D., Suhrkamp I., Wang Y., Liu S., Menkhaus J., Verreet J.A., Fan L., Cai D. Identification and characterization of microRNAs in oilseed rape (Brassica napus) responsive to infection with the pathogenic fungus Verticillium longisporum using Brassica AA (Brassica rapa) and CC (Brassica oleracea) as refer. New Phytol. 2014; 204(3):577-594. DOI 10.1111/nph.12934Tamura K., Stecher G., Kumar S. MEGA 11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021;38(7):30223027. DOI 10.1093/molbev/msab120Tamura K., Stecher G., Kumar S. MEGA 11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021;38(7):30223027. DOI 10.1093/molbev/msab120Troshina N.B., Surina O.B., Cherepanova E.A., Yarullina L.G., Maksimov I.V. Comparative evaluation of H2O2-degrading activity of aggressive Septoria nodorum strains. Mikologiya i Fitopatologiya = Mycology and Phytopathology. 2010;44(3):273-279 (in Russian)Troshina N.B., Surina O.B., Cherepanova E.A., Yarullina L.G., Maksimov I.V. Comparative evaluation of H2O2-degrading activity of aggressive Septoria nodorum strains. Mikologiya i Fitopatologiya = Mycology and Phytopathology. 2010;44(3):273-279 (in Russian)Veselova S., Nuzhnaya T., Burkhanova G., Rumyantsev S., Maksimov I. Reactive oxygen species in host plant are required for an early defense response against attack of Stagonospora nodorum Berk. necrotrophic effectors SnTox. Plants. 2021;10(8):1586. DOI 10.3390/plants10081586Veselova S., Nuzhnaya T., Burkhanova G., Rumyantsev S., Maksimov I. Reactive oxygen species in host plant are required for an early defense response against attack of Stagonospora nodorum Berk. necrotrophic effectors SnTox. Plants. 2021;10(8):1586. DOI 10.3390/plants10081586Wang Q., An B., Hou X., Guo Y., Luo H., He C. Dicer-like proteins regulate the growth, conidiation, and pathogenicity of Colletotrichum gloeosporioides from Hevea brasiliensis. Front Microbiol. 2018;8: 2621. DOI 10.3389/fmicb.2017.02621Wang Q., An B., Hou X., Guo Y., Luo H., He C. Dicer-like proteins regulate the growth, conidiation, and pathogenicity of Colletotrichum gloeosporioides from Hevea brasiliensis. Front Microbiol. 2018;8: 2621. DOI 10.3389/fmicb.2017.02621Weiberg A., Wang M., Lin F.M., Zhao H., Zhang Z., Kaloshian I., Huang H.D., Jin H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013; 342(6154):118-123. DOI 10.1126/science.1239705Weiberg A., Wang M., Lin F.M., Zhao H., Zhang Z., Kaloshian I., Huang H.D., Jin H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013; 342(6154):118-123. DOI 10.1126/science.1239705Yang Z., Huang Y., Yang J., Yao S., Zhao K., Wang D., Qin Q., Bian Z., Li Y., Lan Y., Zhou T., Wang H., Liu Ch., Wang W., Qi Y., Xu Z., Li Y. Jasmonate signaling enhances RNA silencing and antiviral defense in rice. Cell Host Microbe. 2020;28(1):89 103.e8. DOI 10.1016/j.chom.2020.05.001Yang Z., Huang Y., Yang J., Yao S., Zhao K., Wang D., Qin Q., Bian Z., Li Y., Lan Y., Zhou T., Wang H., Liu Ch., Wang W., Qi Y., Xu Z., Li Y. Jasmonate signaling enhances RNA silencing and antiviral defense in rice. Cell Host Microbe. 2020;28(1):89 103.e8. DOI 10.1016/j.chom.2020.05.001Yarullina L.G., Troshina N.B., Cherepanova E.A., Zaikina E.A., Maksimov I.V. Salicylic and Jasmonic acids in regulation of the proantioxidant state in wheat leaves infected by Septoria nodorum Berk. Prikladnaya Biokhimiya i Mikrobiologiya = Applied Biochemistry and Microbiology. 2011;47:549-555. DOI 10.1134/S0003683811050176 (in Russian)Yarullina L.G., Troshina N.B., Cherepanova E.A., Zaikina E.A., Maksimov I.V. Salicylic and Jasmonic acids in regulation of the proantioxidant state in wheat leaves infected by Septoria nodorum Berk. Prikladnaya Biokhimiya i Mikrobiologiya = Applied Biochemistry and Microbiology. 2011;47:549-555. DOI 10.1134/S0003683811050176 (in Russian)Zhang H., Xia R., Meyers B.C., Walbot V. Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr. Opin. Plant Biol. 2015;27:84-90. DOI 10.1016/j.pbi.2015.06.011Zhang H., Xia R., Meyers B.C., Walbot V. Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr. Opin. Plant Biol. 2015;27:84-90. DOI 10.1016/j.pbi.2015.06.011Zeng W., Wang J., Wang Y., Lin J., Fu Y., Xie J., Jiang D., Chen T., Liu H., Cheng J. Dicer-Like proteins regulate sexual development via the biogenesis of perithecium-specific MicroRNAs in a plant pathogenic fungus Fusarium graminearum. Front Microbiol. 2018; 9:818. DOI 10.3389/fmicb.2018.00818Zeng W., Wang J., Wang Y., Lin J., Fu Y., Xie J., Jiang D., Chen T., Liu H., Cheng J. Dicer-Like proteins regulate sexual development via the biogenesis of perithecium-specific MicroRNAs in a plant pathogenic fungus Fusarium graminearum. Front Microbiol. 2018; 9:818. DOI 10.3389/fmicb.2018.00818

The authors declare that there are no conflicts of interest present.