Transcriptome-based discovery of genes and networks related to RSC3Q-mediated resistance to Soybean mosaic virus in soybean
Yuan Yuan A B , Yongqing Yang A , Jinlong Yin A , Yingchao Shen A , Bowen Li A , LiLiqun Wang A and Haijian Zhi A CA National Center for Soybean Improvement, National Key Laboratory for Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Genetic Improvement of Soybean, Ministry of Agriculture, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People’s Republic of China.
B Horticultural Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai 201106, People’s Republic of China.
C Corresponding author. Email: zhj@njau.edu.cn
Crop and Pasture Science 71(12) 987-995 https://doi.org/10.1071/CP20253
Submitted: 18 July 2020 Accepted: 14 October 2020 Published: 7 December 2020
Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND
Abstract
Soybean mosaic virus (SMV) is a worldwide disease of soybean (Glycine max (L.) Merr.) that can cause serious reduction in yield and seed quality. Soybean cv. Qihuang-1 is an important source of resistance to SMV in China, carrying a resistance gene (RSC3Q) against SMV strain SC3. In order to discover genes and networks regulated by RSC3Q-mediated resistance in Qihuang-1, we analysed transcriptome data of a pair of near-isogenic lines, R (RSC3Q) and S (rSC3Q), from the cross Qihuang-1 × Nannong 1138-2 (rSC3Q), after SC3 inoculation. Many differentially expressed genes (DEGs) were identified in the R and S lines at 6, 20 and 48 h post-inoculation. Based on pathway-enrichment analysis of DEGs, three genes encoding calmodulin-like protein (Glyma03g28650, Glyma19g31395 and Glyma11g33790) with downregulated expression in the S line were identified in the plant–pathogen interaction pathway at 6 h post-inoculation. Analyses by quantitative real-time PCR were performed to verify that these three genes were not beneficial for SMV infection. Our results also revealed a complex plant-hormone signal network in RSC3Q-mediated resistance during the early stage of SMV infection. Expression of jasmonic acid repressor genes (TIFY/JAZ) and abscisic acid-induced genes (PP2C3a) was upregulated in the R line but not the S line. More DEGs related to indole-3-acetic acid were found in the R line than the S line, and no salicylic acid-related DEGs were identified. These results suggest that suppression of jasmonic acid or promotion of abscisic acid is important for RSC3Q-mediated resistance against SC3, and that salicylic acid may not act as a main regulator of RSC3Q-mediated resistance during early stages of SC3 infection. Growth and development were greatly affected through RSC3Q-mediated resistance responses after SC3 infection. Our understanding would be enhanced by identification of factors associated with RSC3Q that help to trigger the resistance response.
Keywords: CML, Glycine max, NILs, plant-hormone signal-transduction pathway, Soybean mosaic virus.
References
Adams MJ, Antoniw JF, Fauquet CM (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Archives of Virology 150, 459–479.| Molecular criteria for genus and species discrimination within the family Potyviridae.Crossref | GoogleScholarGoogle Scholar | 15592889PubMed |
Alamillo JM, Saénz P, García JA (2006) Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. The Plant Journal 48, 217–227.
| Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco.Crossref | GoogleScholarGoogle Scholar | 17018032PubMed |
Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host–virus interactions. Molecular Plant Pathology 16, 529–540.
| Roles of plant hormones in the regulation of host–virus interactions.Crossref | GoogleScholarGoogle Scholar | 25220680PubMed |
Alazem M, Tseng KC, Chang WC, Seo JK, Kim KH (2018) Elements involved in the Rsv3-mediated extreme resistance against an avirulent strain of soybean mosaic virus. Viruses 10, 581
| Elements involved in the Rsv3-mediated extreme resistance against an avirulent strain of soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar |
Alazem M, Widyasari K, Kim KH (2019) An avirulent strain of soybean mosaic virus reverses the defensive effect of abscisic acid in a susceptible soybean cultivar. Viruses 11, 879
| An avirulent strain of soybean mosaic virus reverses the defensive effect of abscisic acid in a susceptible soybean cultivar.Crossref | GoogleScholarGoogle Scholar |
Aldon D, Mbengue M, Mazars C, Galaud JP (2018) Calcium signalling in plant biotic interactions. International Journal of Molecular Sciences 19, 665
| Calcium signalling in plant biotic interactions.Crossref | GoogleScholarGoogle Scholar |
Baebler Š, Witek K, Petek M, Stare K, Tušek-Žnidarič M, Pompe-Novak M, Renaut J, Szajko K, Strzelczyk-Żyta D, Marczewski W, Morgiewicz K, Gruden K, Hennig J (2014) Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato. Journal of Experimental Botany 65, 1095–1109.
| Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato.Crossref | GoogleScholarGoogle Scholar | 24420577PubMed |
Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garciacasado G, Lopezvidriero L, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671.
| The JAZ family of repressors is the missing link in jasmonate signalling.Crossref | GoogleScholarGoogle Scholar | 17637675PubMed |
Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69, 467–470.
| Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars.Crossref | GoogleScholarGoogle Scholar |
Cho EK, Goodman RM (1982) Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Science 22, 1133–1136.
| Evaluation of resistance in soybeans to soybean mosaic virus strains.Crossref | GoogleScholarGoogle Scholar |
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5, 344–350.
| (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate.Crossref | GoogleScholarGoogle Scholar | 19349968PubMed |
Fu DQ, Ghabrial S, Kachroo A (2009) GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Molecular Plant–Microbe Interactions 22, 86–95.
| GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean.Crossref | GoogleScholarGoogle Scholar | 19061405PubMed |
Garcia-Marcos A, Pacheco R, Manzano A, Aguilar E, Tenllado F (2013) Oxylipin biosynthesis genes positively regulate programmed cell death during compatible infections with the synergistic pair Potato virus X–Potato virus Y and Tomato spotted wilt virus. Journal of Virology 87, 5769–5783.
| Oxylipin biosynthesis genes positively regulate programmed cell death during compatible infections with the synergistic pair Potato virus X–Potato virus Y and Tomato spotted wilt virus.Crossref | GoogleScholarGoogle Scholar | 23487466PubMed |
Gordon A, Hannon GJ (2010) FASTX-toolkit. FASTQ/A short-reads preprocessing tools. Hannon Laboratory, CSHL, NY, USA. Available at: http://hannonlab.cshl.edu/fastx_toolkit/[Verified 4 November 2020]
Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Current Biology 21, R346–R355.
| Evolution of abscisic acid synthesis and signaling mechanisms.Crossref | GoogleScholarGoogle Scholar | 21549957PubMed |
Hayes AJ, Ma G, Buss GR, Saghai Maroof MA (2000) Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Science 40, 1434–1437.
| Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar |
Hu CH, Wang PQ, Zhang PP, Nie XM, Li BB, Tai L, Liu WT, Li WQ, Chen KM (2020) NADPH oxidases: the vital performers and center hubs during plant growth and signaling. Cells 9, 437
| NADPH oxidases: the vital performers and center hubs during plant growth and signaling.Crossref | GoogleScholarGoogle Scholar |
Hunter LJR, Westwood JH, Heath G, Macaulay K, Smith AG, MacFarlane SA, Palukaitis P, Carr JP (2013) Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis. PLoS One 8, e66530
| Regulation of RNA-dependent RNA polymerase 1 and isochorismate synthase gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Ishibashi K, Saruta M, Shimizu T, Shu M, Anai T, Komatsu K, Yamada N, Katayose Y, Ishikawa M, Ishimoto M, Kaga A (2019) Soybean antiviral immunity conferred by dsRNase targets the viral replication complex. Nature Communications 10, 4033
| Soybean antiviral immunity conferred by dsRNase targets the viral replication complex.Crossref | GoogleScholarGoogle Scholar | 31562302PubMed |
Jeong SC, Kristipati S, Hayes AJ, Maughanb PJ, Noffsingerc SL, Gunduza I, Bussa GR, Saghai Maroof MA (2002) Genetic and sequence analysis of markers tightly linked to the Soybean mosaic virus resistance gene, Rsv3. Crop Science 42, 265–270.
Jones JD, Dangl JL (2006) The plant immune system Nature 444, 323–329.
Kazan K, Manners JM (2013) MYC2: the master in action. Molecular Plant 6, 686–703.
| MYC2: the master in action.Crossref | GoogleScholarGoogle Scholar | 23142764PubMed |
Klepadlo M, Chen P, Shi A, Maughanb PJ, Noffsingerc SL, Gunduza I, Bussa GR, Saghai Maroof MA (2017) Single nucleotide polymorphism markers for rapid detection of the Rsv4 locus for soybean mosaic virus resistance in diverse germplasm. Molecular Breeding 37, 10
| Single nucleotide polymorphism markers for rapid detection of the Rsv4 locus for soybean mosaic virus resistance in diverse germplasm.Crossref | GoogleScholarGoogle Scholar |
Li C, Karthikeyan A, Yuan Y, Yin J, Ren R, Yang Y, Zhi H (2017) Identification of candidate genes for resistance to Soybean mosaic virus strain SC3 by using fine mapping and transcriptome analyses. Crop and Pasture Science 68, 156–166.
| Identification of candidate genes for resistance to Soybean mosaic virus strain SC3 by using fine mapping and transcriptome analyses.Crossref | GoogleScholarGoogle Scholar |
Li K, Yang QH, Zhi HJ, Gai JY (2010) Identification and distribution of Soybean mosaic virus strains in southern China. Plant Disease 94, 351–357.
| Identification and distribution of Soybean mosaic virus strains in southern China.Crossref | GoogleScholarGoogle Scholar | 30754253PubMed |
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967.
| SOAP2: an improved ultrafast tool for short read alignment.Crossref | GoogleScholarGoogle Scholar | 19497933PubMed |
Lu Y, Truman W, Liu X, Bethke G, Zhou M, Myers CL, Katagiri F, Glazebrook J (2018) Different modes of negative regulation of plant immunity by calmodulin-related genes. Plant Physiology 176, 3046–3061.
| Different modes of negative regulation of plant immunity by calmodulin-related genes.Crossref | GoogleScholarGoogle Scholar | 29449432PubMed |
Luan H, Shine MB, Cui X, Chen X, Ma N, Kachroo P, Zhi H, Kachroo A (2016) The potyviral P3 protein targets eukaryotic elongation factor 1A to promote the unfolded protein response and viral pathogenesis. Plant Physiology 172, 221–234.
| The potyviral P3 protein targets eukaryotic elongation factor 1A to promote the unfolded protein response and viral pathogenesis.Crossref | GoogleScholarGoogle Scholar | 27356973PubMed |
Ma Y, Wang DG, Li HC, Zheng GJ, Yang YQ, Li HW, Zhi HJ (2011) Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus. Euphytica 181, 127–135.
| Fine mapping of the RSC14Q locus for resistance to soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar |
Nakano M (1982) Further study on strains of soybean mosaic virus in Kyushu. Proceedings of the Association for Plant Protection of Kyushu 28, 24–25.
| Further study on strains of soybean mosaic virus in Kyushu.Crossref | GoogleScholarGoogle Scholar |
Nakashima J, Laosinchai W, Cui X, Brown RM (2003) New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 10, 369–389.
| New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding.Crossref | GoogleScholarGoogle Scholar |
Oka K, Kobayashi M, Mitsuhara I, Seo S (2013) Jasmonic acid negatively regulates resistance to Tobacco mosaic virus in tobacco. Plant and Cell Physiology 54, 1999–2010.
| Jasmonic acid negatively regulates resistance to Tobacco mosaic virus in tobacco.Crossref | GoogleScholarGoogle Scholar | 24071744PubMed |
Pacheco R, Garcia Marcos A, Manzano A, De Lacoba MG, Camanes G, Garcia Agustin P, Diazruiz JR, Tenllado F (2012) Comparative analysis of transcriptomic and hormonal responses to compatible and incompatible plant–virus interactions that lead to cell death. Molecular Plant-Microbe Interactions 25, 709–723.
| Comparative analysis of transcriptomic and hormonal responses to compatible and incompatible plant–virus interactions that lead to cell death.Crossref | GoogleScholarGoogle Scholar | 22273391PubMed |
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489–521.
| Hormonal modulation of plant immunity.Crossref | GoogleScholarGoogle Scholar |
Ramos AC, Façanha AR, Feijó JA (2008) Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytologist 178, 177–188.
| Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 18208473PubMed |
Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE–SALICYLATE antagonism. Annual Review of Phytopathology 49, 317–343.
| Hormone crosstalk in plant disease and defense: more than just JASMONATE–SALICYLATE antagonism.Crossref | GoogleScholarGoogle Scholar | 21663438PubMed |
Rui R, Liu S, Karthikeyan A, Wang T, Niu H, Yin J, Yang Y, Wang L, Yang Q, Zhi H, Li K (2017) Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to Soybean mosaic virus. Theoretical and Applied Genetics 130, 2395–2410.
| Fine-mapping and identification of a novel locus Rsc15 underlying soybean resistance to Soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar | 28825113PubMed |
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht JE, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the paleopolyploid soybean. Nature 463, 178–183.
| Genome sequence of the paleopolyploid soybean.Crossref | GoogleScholarGoogle Scholar | 20075913PubMed |
Scholz SS, Vadassery J, Heyer M, Reichelt M, Bender KW, Snedden WA, Boland W, Mith€ofer A (2014) Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory. Molecular Plant 7, 1712–26.
| Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory.Crossref | GoogleScholarGoogle Scholar | 25267731PubMed |
Seo JK, Kwon SJ, Cho WK, Choi HS, Kim KH (2014) Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Scientific Report S4, 5905 https://doi.org/10.1038/srep05905
Sheard LB, Tan X, Mao H, Withers J, Bennissan G, Hinds TR, Kobayashi Y, Hsu F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400–405.
| Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor.Crossref | GoogleScholarGoogle Scholar | 20927106PubMed |
Shigenaga AM, Cristiana TA (2016) No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Seminars in Cell & Developmental Biology 56, 174–189.
| No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens.Crossref | GoogleScholarGoogle Scholar |
Takahashi K, Tanaka T, Iida W, Tsuda Y (1980) Studies on virus diseases and causal viruses of soybean in Japan. Bulletin of the Tohoku National Agricultural Experiment Station 62, 1–130.
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511–515.
| Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Crossref | GoogleScholarGoogle Scholar | 20436464PubMed |
Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithofer A (2012a) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiology 159, 1159–1175.
| CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22570470PubMed |
Vadassery J, Scholz SS, Mith€ofer A (2012b) Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived (Spodoptera littoralis) oral secretion. Plant Signaling & Behavior 7, 1277–1280.
| Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived (Spodoptera littoralis) oral secretion.Crossref | GoogleScholarGoogle Scholar |
Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The tify family previously known as ZIM. Trends in Plant Science 12, 239–244.
| The tify family previously known as ZIM.Crossref | GoogleScholarGoogle Scholar | 17499004PubMed |
Vos IA, Pieterse CMJ, Van Wees SCM (2013) Costs and benefits of hormone-regulated plant defences. Plant Pathology 62, 43–55.
| Costs and benefits of hormone-regulated plant defences.Crossref | GoogleScholarGoogle Scholar |
Wang D, Li K, Zhi H (2018) Progresses of resistance on soybean mosaic virus in soybean. Zhongguo Nong Ye Ke Xue 51, 3040–3059.
Wang D, Ma Y, Yang Y, Liu N, Li C, Song Y, Zhi H (2011) Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean. Theoretical and Applied Genetics 122, 555–565.
| Fine mapping and analyses of RSC8 resistance candidate genes to soybean mosaic virus in soybean.Crossref | GoogleScholarGoogle Scholar | 20981404PubMed |
Wang J, Shine MB, Gao QM, Navarre D, Jiang W, Liu C, Chen Q, Hu G, Kachroo A (2014) Enhanced disease susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiology 165, 1269–1284.
| Enhanced disease susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean.Crossref | GoogleScholarGoogle Scholar | 24872380PubMed |
Wang X, Gai J, Pu Z (2003) Classification and distribution of strain groups of soybean mosaic virus in middle and lower Huang-Huai and Changjiang valleys. Dadou Kexue 22, 102–107.
Xu B, Cheval C, Laohavisit A, Hocking B, Chiasson D, Olsson TSG, Shirasu K, Faulkner C, Gilliham M (2017) A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses. New Phytologist 215, 77–84.
| A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses.Crossref | GoogleScholarGoogle Scholar | 28513846PubMed |
Xu LW, Wu XZ, Jia ML, Li TJ, Wen F (2019) Research advances on MAPK cascade and their roles in plant disease resistance. Acta Laser Biology Sinica 6, 488–495.
Xun H, Yang X, He H, Wang M, Guo P, Wang Y, Pang J, Dong Y, Feng X, Wang S, Liu B (2019) Over-expression of GmKR3, a TIR–NBS–LRR type R gene, confers resistance to multiple viruses in soybean. Plant Molecular Biology 99, 95–111.
| Over-expression of GmKR3, a TIR–NBS–LRR type R gene, confers resistance to multiple viruses in soybean.Crossref | GoogleScholarGoogle Scholar | 30535849PubMed |
Yoshioka H, Adachi H, Nakano T, Miyagawa N, Asai S, Ishihama N, Yoshioka M (2016) Hierarchical regulation of NADPH oxidase by protein kinases in plant immunity. Physiological and Molecular Plant Pathology 95, 20–26.
| Hierarchical regulation of NADPH oxidase by protein kinases in plant immunity.Crossref | GoogleScholarGoogle Scholar |
Yu YG, Maroof MAS, Buss GR, Maughan PJ, Tolin SA (1994) RFLP and microsatellite mapping of a gene for soybean mosaic virus resistance. Phytopathology 84, 60–64.
| RFLP and microsatellite mapping of a gene for soybean mosaic virus resistance.Crossref | GoogleScholarGoogle Scholar |
Yuan Y, Yang Y, Shen Y, Yu K, Wang L, Ren R, Yin J, Zhi H (2020) Mapping and functional analysis of candidate genes involved in resistance to soybean (Glycine max) mosaic virus strain SC3. Plant Breeding 139, 618–625.
| Mapping and functional analysis of candidate genes involved in resistance to soybean (Glycine max) mosaic virus strain SC3.Crossref | GoogleScholarGoogle Scholar |
Zhang C, Grosics S, Whitham SA, Hill JH (2012) The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to Soybean mosaic virus. Molecular Plant–Microbe Interactions 25, 1307–1313.
| The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to Soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar | 22712511PubMed |
Zhao Q, Li H, Sun H, Li A, Liu S, Yu R, Cui X, Zhang D, Wuriyanghan H (2018) Salicylic acid and broad spectrum of NBS-LRR family genes are involved in SMV–soybean interactions. Plant Physiology and Biochemistry 123, 132–140.
| Salicylic acid and broad spectrum of NBS-LRR family genes are involved in SMV–soybean interactions.Crossref | GoogleScholarGoogle Scholar | 29232653PubMed |
Zheng GJ, Yang YQ, Ma Y, Ma Y, Yang X, Chen S, Ren R, Wang D, Yang Z, Jian H (2014) Fine mapping and candidate gene analysis of resistance gene RSC3Q to Soybean mosaic virus in Qihuang 1. Journal of Integrative Agriculture 13, 2608–2615.
| Fine mapping and candidate gene analysis of resistance gene RSC3Q to Soybean mosaic virus in Qihuang 1.Crossref | GoogleScholarGoogle Scholar |
Zheng HQ, Wu NY, Chow CN, Tseng KC, Chien CH, Hung YC, Li GZ, Chang WC (2017) EXPath tool: a system for comprehensively analyzing regulatory pathways and coexpression networks from high-throughput transcriptome data. DNA Research 24, 371–375.
| EXPath tool: a system for comprehensively analyzing regulatory pathways and coexpression networks from high-throughput transcriptome data.Crossref | GoogleScholarGoogle Scholar | 28338930PubMed |
Zhu X, Perez M, Aldon D, Galaud JP (2017) Respective contribution of CML8 and CML9, two arabidopsis calmodulin-like proteins, to plant stress responses. Plant Signaling & Behavior 12, e1322246
| Respective contribution of CML8 and CML9, two arabidopsis calmodulin-like proteins, to plant stress responses.Crossref | GoogleScholarGoogle Scholar |