Barley yellow dwarf viruses (BYDVs) are one of the most widespread and economically important plant viruses affecting many cereal crops. Growing resistant varieties remains the most promising approach to reduce the impact of BYDVs. A Recent RNA sequencing analysis has revealed potential genes that respond to BYDV infection in resistant barley genotypes. Together with a comprehensive review of the current knowledge on disease resistance in plants, we selected nine putative barley and wheat genes to investigate their involvement in resistance to BYDV-PAV infection. The target classes of genes were (i) nucleotide binding site (NBS) leucine-rich repeat (LRR), (ii) coiled-coil nucleotide-binding leucine-rich repeat (CC-NB-LRR), (iii) LRR receptor-like kinase (RLK), (iv) casein kinase, (v) protein kinase, (vi) protein phosphatase subunits and the transcription factors (TF) (vii) MYB TF, (viii) GRAS (gibberellic acid-insensitive (GAI), repressor of GAI (RGA) and scarecrow (SCR)), and (ix) the MADS-box TF family. Expression of genes was analysed for six genotypes with different levels of resistance. As in previous reports, the highest BYDV-PAV titre was found in the susceptible genotypes Graciosa in barley and Semper and SGS 27-02 in wheat, which contrast with the resistant genotypes PRS-3628 and Wysor of wheat and barley, respectively. Statistically significant changes in wheat show up-regulation of NBS-LRR, CC-NBS-LRR and RLK in the susceptible genotypes and down-regulation in the resistant genotypes in response to BYDV-PAV. Similar up-regulation of NBS-LRR, CC-NBS-LRR, RLK and MYB TF in response to BYDV-PAV was also observed in the susceptible barley genotypes. However, no significant changes in the expression of these genes were generally observed in the resistant barley genotypes, except for the down-regulation of RLK. Casein kinase and Protein phosphatase were up-regulated early, 10 days after inoculation (dai) in the susceptible wheat genotypes, while the latter was down-regulated at 30 dai in resistant genotypes. Protein kinase was down-regulated both earlier (10 dai) and later (30 dai) in the susceptible wheat genotypes, but only in the later dai in the resistant genotypes. In contrast, GRAS TF and MYB TF were up-regulated in the susceptible wheat genotypes while no significant differences in MADS TF expression was observed. Protein kinase, Casein kinase (30 dai), MYB TF and GRAS TF (10 dai) were all up-regulated in the susceptible barley genotypes. However, no significant differences were found between the resistant and susceptible barley genotypes for the Protein phosphatase and MADS FT genes. Overall, our results showed a clear differentiation of gene expression patterns in both resistant and susceptible genotypes of wheat and barley. Therefore, further research on RLK, NBS-LRR, CC-NBS-LRR, GRAS TF and MYB TF can lead to BYDV-PAV resistance in cereals.

Agriculture Health and Environment Department Natural Resources Institute University of Greenwich Medway Campus Chatham Kent ME4 4TB UK

Laboratory of Virology Centre for Plant Virus Research Institute of Experimental Botany of the Czech Academy of Sciences Rozvojová 263 165 02 Prague Czech Republic

Plant Virus and Vector Interactions Centre for Plant Virus Research Crop Research Institute Drnovská 507 161 06 Prague Czech Republic

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Perry K.L., Kolb F.L., Sammons B., Lawson C., Cisar G., Ohm H. Yield effects of barley yellow dwarf virus in soft red winter wheat. Phytopathology. 2000;90:1043–1048. doi: 10.1094/PHYTO.2000.90.9.1043. PubMed DOI

Hewings A.D. Purification and virion characterization of barley yellow dwarf viruses. In: D’Arcy C.J., Burnett P.A., editors. Barley Yellow Dwarf, 40 Years of Progress. APS Press; St. Paul, MN, USA: 1995. pp. 165–179.

Power A., Gray S. Aphid transmission of barley yellow dwarf viruses interactions between viruses, vectors, and host plants. In: D’Arcy J.C., Burnett P.A., editors. Barley Yellow Dwarf, 40 Years of Progress. APS Press; Saint Paul, MN, USA: 1995. pp. 255–291.

Burnett P.A., Comeau A., Qualset C.O. Host plant tolerance or resistance for control of barley yellow dwarf. In: D’Arcy C.J., Burnett P.A., editors. Barley Yellow Dwarf, 40 Years of Progress. APS Press; St. Paul, MN, USA: 1995. pp. 321–344.

Kang C.B., Yeam I., Jahn M.M. Genetics of plant virus resistance. Annu. Rev. Phytopathol. 2005;43:581–621. doi: 10.1146/annurev.phyto.43.011205.141140. PubMed DOI

Cooper J.I., Jones A.T. Responses of plants to viruses: Proposals for the use of terms. Phytopathology. 1983;73:127–128. doi: 10.1094/Phyto-73-127. DOI

Jarošová J., Chrpová J., Šíp V., Kundu J.K. A comparative study of the Barley yellow dwarf virus species PAV and PAS: Distribution, accumulation and host resistance. Plant Pathol. 2013;62:436–443. doi: 10.1111/j.1365-3059.2012.02644.x. DOI

Beoni E., Chrpová J., Jarošová J., Kundu J.K. Survey of barley yellow dwarf virus incidence in winter cereals crops, and assessment of wheat and barley resistance to the virus. Crop Pasture Sci. 2016;67:1054–1063. doi: 10.1071/CP16167. DOI

Choudhury S., Hu H., Larkin P., Meinke1 H., Shabala S., Ahmed I., Zhou M. Agronomical, biochemical and histological response of resistant and susceptible wheat and barley under BYDV stress. Peer J. 2018;6:e4833. doi: 10.7717/peerj.4833. PubMed DOI PMC

Singh R.P., Burnett P.A., Albarran M., Rajaram S. Bdv1: A gene for tolerance to barley yellow dwarf virus in bread wheats. Crop Sci. 1993;33:231–234. doi: 10.2135/cropsci1993.0011183X003300020002x. DOI

Ayala L., Henry M., van Ginkel M., Singh R., Keller B., Khairallah M. Identification of QTLs for BYDV tolerance in bread wheat. Euphytica. 2002;128:249–259. doi: 10.1023/A:1020883414410. DOI

Suneson C.A. Breeding for resistance to barley yellow dwarf virus in barley. Agron. J. 1955;47:283. doi: 10.2134/agronj1955.00021962004700060014x. DOI

Rasmusson D.C., Schaller C.W. The inheritance of resistance in barley to the yellow-dwarf virus. Agron. J. 1959;51:661–664. doi: 10.2134/agronj1959.00021962005100110009x. DOI

Niks R.E., Habekuss A., Bekele B., Ordon F. A novel major gene on chromosome 6H for resistance of barley against the barley yellow dwarf virus. Theor. Appl. Genet. 2004;109:1536–1543. doi: 10.1007/s00122-004-1777-7. PubMed DOI

Scholz M., Ruge-Wehling B., Habekuß A., Schrader O., Pendinen G., Fischer K., Wehling P. Ryd4Hb: A novel resistance gene introgressed from Hordeumbulbosum into barley and conferring complete and dominant resistance to the barley yellow dwarf virus. Theor. Appl. Genet. 2009;119:837–849. doi: 10.1007/s00122-009-1093-3. PubMed DOI

Jarošová J., Beoni E., Kundu J.K. Barley yellow dwarf virus resistance in cereals: Approaches, strategies and prospects. Field Crop Res. 2016;198:200–214. doi: 10.1016/j.fcr.2016.08.030. DOI

Zhang T., Liang Q., Li C., Fu S., Kundu J.K., Zhou X., Wu J. Transcriptome Analysis of Rice Reveals the lncRNA–mRNA Regulatory Network in Response to Rice Black-Streaked Dwarf Virus Infection. Viruses. 2020;12:951. doi: 10.3390/v12090951. PubMed DOI PMC

Postnikova O.A., Nemchinov L.G. Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses. Virol. J. 2012;9:101. doi: 10.1186/1743-422X-9-101. PubMed DOI PMC

Durrant W.E., Dong X. Systemic acquired resistance. Annu. Rev. Phytopathol. 2004;42:185–209. doi: 10.1146/annurev.phyto.42.040803.140421. PubMed DOI

Jones J.D., Dangl J.L. The plant immune system. Nature. 2006;444:323–329. doi: 10.1038/nature05286. PubMed DOI

Carr J.P., Lewsey M.G., Palukaitis P. Signaling in induced resistance. Adv. Virus Res. 2010;76:57–121. PubMed

Kourelis J., van der Hoorn R.A.L. Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function. Plant Cell. 2018;30:285–299. doi: 10.1105/tpc.17.00579. PubMed DOI PMC

Jarošová J., Singh K., Chrpová J., Kundu J.K. Analysis of Small RNAs of Barley Genotypes Associated with Resistance to Barley Yellow Dwarf Virus. Plants. 2020;9:60. doi: 10.3390/plants9010060. PubMed DOI PMC

Jarosová J., Kundu J.K. Validation of reference genes as internal control for studying viral infections in cereals by quantitative real-time RT-PCR. BMC Plant Biol. 2010;10:146. doi: 10.1186/1471-2229-10-146. PubMed DOI PMC

Kundu J.K., Jarošová J., Gadiou S., Červená G. Discrimination of three BYDV species by one-step RT-PCR-RFLP and sequence based methods in cereal plants from the Czech Republic. Cereal Res. Commun. 2009;37:541–550. doi: 10.1556/CRC.37.2009.4.7. DOI

Jarošová J., Ripl J., Fousek J., Kundu J.K. TaqMan Multiplex Real-Time qPCR assays for the detection and quantification of Barley yellow dwarf virus, Wheat dwarf virus and Wheat streak mosaic virus and the study of their interactions. Crop Pasture Sci. 2018;69:755–764. doi: 10.1071/CP18189. DOI

Lee C., Kim J., Shin G.S., Hwang S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J. Biotechnol. 2006;123:273–280. doi: 10.1016/j.jbiotec.2005.11.014. PubMed DOI

Cejnar P., Ohnoutková L., Ripl J., Vlčko T., Kundu J.K. Two mutations in the truncated Rep gene RBR domain delayed the Wheat dwarf virus infection in transgenic barley plants. J. Integr. Agric. 2018;17:2492–2500. doi: 10.1016/S2095-3119(18)62000-3. DOI

Malmstrom C.M., Shu R. Multiplexed RT-PCR for streamlined detection and separation of barley and cereal yellow dwarf viruses. J. Virol. Methods. 2004;120:69–78. doi: 10.1016/j.jviromet.2004.04.005. PubMed DOI

Krattinger S.G., Keller B. Molecular genetics and evolution of disease resistance in cereals. New Phytol. 2016;212:320–332. doi: 10.1111/nph.14097. PubMed DOI

Radonić A., Thulke S., Mackay I.M., Landt O., Siegert W., Nitsche A. Guideline to reference gene selection for quantitative real-time PCR. Biochem. Biophys. Res. Commun. 2004;313:856–862. doi: 10.1016/j.bbrc.2003.11.177. PubMed DOI

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Madsen L.H., Collins N.C., Rakwalska M., Backes G., Sandal N., Krusell L., Jensen J., Waterman E.H., Jahoor A., Ayliffe M., et al. Barley disease resistance gene analogs of the NBS-LRR class: Identification and mapping. Mol. Genet. Genom. 2003;269:150–161. doi: 10.1007/s00438-003-0823-5. PubMed DOI

Liu Y., Zeng Z., Li Q., Jiang X.M., Jiang Z., Tang J.H., Chen D., Wang Q., Chen J.Q., Shao Z.Q. An angiosperm NLR atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion. Mol. Plant. 2021;14:2015–2031. doi: 10.1016/j.molp.2021.08.001. PubMed DOI

Zhang C., Chen H., Cai T., Deng Y., Zhuang R., Zhang N., Zeng Y., Zheng Y., Tang R., Pan R., et al. Overexpression of a novel peanut NBS-LRR gene AhRRS5 enhances disease resistance to Ralstonia solanacearum in tobacco. Plant Biotechnol. J. 2017;15:39–55. doi: 10.1111/pbi.12589. PubMed DOI PMC

Yoshimura S., Yamanouchi U., Katayose Y., Toki S., Wang Z.X., Kono I., Kurata N., Yano M., Iwata N., Sasaki T. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Nat. Acad. Sci. USA. 1998;95:1663–1668. doi: 10.1073/pnas.95.4.1663. PubMed DOI PMC

Zhou X., Liu J., Bao S., Yang Y., Zhuang Y. Molecular cloning and characterization of a wild eggplant Solanum aculeatissimum NBS-LRR gene, involved in plant resistance to Meloidogyne incognita. Int. J. Mol. Sci. 2018;19:583. doi: 10.3390/ijms19020583. PubMed DOI PMC

Xu Y., Liu F., Zhu S., Li X. The Maize NBS-LRR Gene ZmNBS25Enhances Disease Resistance in Rice and Arabidopsis. Front. Plant Sci. 2018;9:1033. doi: 10.3389/fpls.2018.01033. PubMed DOI PMC

Goyala N., Bhatiaa G., Sharmab S., Garewala N., Upadhyayc A., Upadhyayd K.S., Singha K. Genome-wide characterization revealed role of NBS-LRR genes during powdery mildew infection in Vitis vinifera. Genomics. 2020;112:312–322. doi: 10.1016/j.ygeno.2019.02.011. PubMed DOI

Césari S., Kanzaki H., Fujiwara T., Bernoux M., Chalvon V., Kawano Y., Shimamoto K., Dodds P., Terauchi R., Kroj T. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J. 2014;33:1941–1959. doi: 10.15252/embj.201487923. PubMed DOI PMC

Brueggeman R., Druka A., Nirmala J., Cavileer T., Drader T., Rostoks N., Mirlohi A., Bennypaul H., Gill U., Kudrna D., et al. The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. Proc. Nat. Acad. Sci. USA. 2008;105:14970–14975. doi: 10.1073/pnas.0807270105. PubMed DOI PMC

Wang X., Richards J., Gross T., Druka A., Kleinhofs A., Steffenson B., Acevedo M., Brueggeman R. The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol. Plant-Microbe Interact. 2013;26:407–418. doi: 10.1094/MPMI-06-12-0146-R. PubMed DOI

Wang G., Roux B., Feng F., Guy E., Li L., Li N., Zhang X., Lautier M., Jardinaud M.F., Chabannes M., et al. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe. 2015;18:285–295. doi: 10.1016/j.chom.2015.08.004. PubMed DOI

Arora D., Gross T., Brueggeman R. Allele characterization of genes required for rpg4-mediated wheat stem rust resistance identifies Rpg5 as the R gene. Phytopathology. 2013;103:1153–1161. doi: 10.1094/PHYTO-01-13-0030-R. PubMed DOI

Loutre C., Wicker T., Travella S., Galli P., Scofield S., Fahima T., Feuillet C., Keller B. Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant J. 2009;60:1043–1054. doi: 10.1111/j.1365-313X.2009.04024.x. PubMed DOI

Li Q., Jiang X.M., Shao Z.Q. Genome-Wide Analysis of NLR Disease Resistance Genes in an Updated Reference Genome of Barley. Front. Genet. 2021;12:694682. doi: 10.3389/fgene.2021.694682. PubMed DOI PMC

Wu C.H., Krasileva K.V., Banfield M.J., Terauchi R., Kamoun S. The “sensor domains” of plant NLR proteins: More than decoys? Front. Plant Sci. 2015;6:134. doi: 10.3389/fpls.2015.00134. PubMed DOI PMC

Solanki S. Ph.D. Thesis. North Dakota State University of Agriculture and Applied Science; Fargo, ND, USA: 2017. Dissecting the Mystery Behind Rpg5 Mediated Puccinia graminis Resistance in Barley Using Genetics, Molecular And Bioinformatics Approaches.

Dardick C., Schwessinger B., Ronald P. Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Cur. Opin. Plant Biol. 2012;15:358–366. doi: 10.1016/j.pbi.2012.05.002. PubMed DOI

Tang D.Z., Wang G.X., Zhou J.M. Receptor kinases in plant-pathogen interactions: More than pattern recognition. Plant Cell. 2017;29:618–637. doi: 10.1105/tpc.16.00891. PubMed DOI PMC

Zhou J.M., Zhang Y.L. Plant immunity: Danger perception and signalling. Cell. 2020;181:978–989. doi: 10.1016/j.cell.2020.04.028. PubMed DOI

Xia T., Yang V., Zheng H., Han X., Jin H., Xiong Z., Qian W., Xia L., Ji1 X., Li G., et al. Efficient expression and function of a receptor-like kinase in wheat powdery mildew defence require an intron-located MYB binding site. Plant Biotechnol. J. 2021;19:897–909. doi: 10.1111/pbi.13512. PubMed DOI PMC

Thapa G., Gunupuru L.R., Heir J.G., Kahla A., Mullins E., Doohan F.M. A pathogen-responsive leucine rich receptor like kinase contributes to Fusarium resistance in cereals. Front. Plant Sci. 2018;9:867. doi: 10.3389/fpls.2018.00867. PubMed DOI PMC

Zhou H.B., Li S.F., Deng Z.Y., Wang X.P., Chen T., Zhang J.S., Chen S.Y., Ling H., Zhang A., Wang D., et al. Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J. 2007;52:420–434. doi: 10.1111/j.1365-313X.2007.03246.x. PubMed DOI

Hu P., Wise R.P. Diversification of Lrk/Tak kinase gene clusters is associated with subfunctionalization and cultivar-specific transcript accumulation in barley. Funct. Integr. Genom. 2008;8:199–209. doi: 10.1007/s10142-008-0077-8. PubMed DOI

Parrott D.L., Huang L., Fischer M.A. Downregulation of a barley (Hordeum vulgare) leucine-rich repeat, non-arginine-aspartate receptor-like protein kinase reduces expression of numerous genes involved in plant pathogen defense. Plant Physiol. Biochem. 2016;100:130–140. doi: 10.1016/j.plaphy.2016.01.005. PubMed DOI

Javed T., Shabbir R., Ali A., Afzal I., Zaheer U., Gao S.J. Transcription factors in plant stress responses: Challenges and potential for sugarcane improvement. Plants. 2020;9:491. doi: 10.3390/plants9040491. PubMed DOI PMC

Shan T., Rong V., Xu H., Du L., Liu X., Zhang Z. The wheat R2R3-MYB transcription factor TaRIM1 participates in resistance response against the pathogen Rhizoctonia cerealis infection through regulating defense genes. Sci. Rep. 2016;6:28777. doi: 10.1038/srep28777. PubMed DOI PMC

Seo P.J., Park C.M. MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol. 2010;186:471–483. doi: 10.1111/j.1469-8137.2010.03183.x. PubMed DOI

Libault M., Wan J., Czechowski T., Udvardi M., Stacey G. Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Plant-Microbe Interact. 2007;20:900–911. doi: 10.1094/MPMI-20-8-0900. PubMed DOI

Mengiste T., Chen X., Salmeron J., Dietrich R. The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell. 2003;15:2551–2565. doi: 10.1105/tpc.014167. PubMed DOI PMC

Chang C., Yu D., Jiao J., Jing S., Schulze-Lefert P., Shen Q.H. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signalling. Plant Cell. 2013;25:1158–1173. doi: 10.1105/tpc.113.109942. PubMed DOI PMC

Liu H., Zhou X., Dong N., Liu X., Zhang H., Zhang Z. Expression of a wheat MYB gene in transgenic tobacco enhances resistance to Ralstonia solanacearum, and to drought and salt stresses. Funct. Integr. Genom. 2011;11:431–443. doi: 10.1007/s10142-011-0228-1. PubMed DOI

Zhang Z., Liu X., Wang X., Zhou M., Zhou X., Ye X., Wei X. An R2R3 MYB transcription factor in wheat, Ta PIMP 1, mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense-and stress-related genes. New Phytol. 2012;196:1155–1170. doi: 10.1111/j.1469-8137.2012.04353.x. PubMed DOI

Di Laurenzio L., Wysocka-Diller J., Malamy J.E., Pysh L., Helariutta Y., Freshour G., Hahn M.G., Feldmann K.A., Benfey P.N. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell. 1996;86:423–433. doi: 10.1016/S0092-8674(00)80115-4. PubMed DOI

Bolle C. The role of GRAS proteins in plant signal transduction and development. Planta. 2004;218:683–692. doi: 10.1007/s00425-004-1203-z. PubMed DOI

Fode B., Siemsen T., Thurow C., Weigel R., Gatz C. The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress inducible promoters. Plant Cell. 2008;20:3122–3135. doi: 10.1105/tpc.108.058974. PubMed DOI PMC

Zhang S., Li X., Fan S., Zhou L., Wang Y. Overexpression of HcSCL13, a Halostachys caspica GRAS transcription factor, enhances plant growth and salt stress tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 2020;151:243–254. doi: 10.1016/j.plaphy.2020.03.020. PubMed DOI

To V.T., Shi Q., Zhang Y., Shi J., Shen C., Zhang D., Cai W. Genome-Wide Analysis of the GRAS Gene Family in Barley (Hordeum vulgare L.) Genes. 2020;11:553. doi: 10.3390/genes11050553. PubMed DOI PMC

Kumar B., Bhalothia P. Evolutionary analysis of GRAS gene family for functional and structural insights into hexaploid bread wheat (Triticum aestivum) J. Biosci. 2021;45:46. doi: 10.1007/s12038-021-00163-5. PubMed DOI

Claeys H., De Bodt S., Inzé D. Gibberellins and DELLAs: Central nodes in growth regulatory networks. Trends Plant Sci. 2014;19:231–239. doi: 10.1016/j.tplants.2013.10.001. PubMed DOI

Rong W., Wang X., Wang X., Massart S., Zhang Z. Molecular and Ultrastructural Mechanisms Underlying Yellow Dwarf Symptom Formation in Wheat after Infection of Barley Yellow Dwarf Virus. Int. J. Mol. Sci. 2018;19:1187. doi: 10.3390/ijms19041187. PubMed DOI PMC

Schilling S., Pan S., Kennedy A., Melzer R. MADS-Box genes and crop domestication: The jack of all traits. J. Exp. Bot. 2018;69:1447–1469. doi: 10.1093/jxb/erx479. PubMed DOI

Zhang H., Teng W., Liang J., Liu X., Zhang H., Zhang Z., Zheng X. MADS1, a novel MADS-box protein, is involved in the response of Nicotiana benthamiana to bacterial harpinXoo. J. Exp. Bot. 2016;67:131–141. doi: 10.1093/jxb/erv448. PubMed DOI

Li W., Zhu Z., Chern M., Yin J., Yang C., Ran L.I., Cheng M., He M., Wang K., Wang J., et al. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell. 2017;170:114–126. doi: 10.1016/j.cell.2017.06.008. PubMed DOI

Wang H., Jiao X., Kong X., Hamera S., Wu Y., Chen X., Fang R., Yan Y. A signalling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol. 2016;170:2365–2377. doi: 10.1104/pp.15.01283. PubMed DOI PMC

Ren Q., Jiang H., Xiang W., Nie Y., Xue S., Zhi H., Li K., Gai J. A MADS-box gene is involved in soybean resistance to multiple Soybean mosaic virus strains. Crop J. 2022;10:802–808. doi: 10.1016/j.cj.2021.10.003. DOI