Genomic blueprints of soybean (Glycine max) pathogen resistance: revealing the key genes for sustainable agriculture
Aiman Hina
A * , Muhammad Khuram Razzaq B C * , Asim Abbasi D , Muhamad Basit Shehzad E , Muhammad Arshad D , Tayyaba Sanaullah F , Kamran Arshad C , Ghulam Raza G , Hayssam M. Ali H , Faisal Hayat I , Naeem Akhtar J and Nader R. Abdelsalam K
A
B
C
D
E
F
G
H
I
J
K
Abstract
Soybean (Glycine max) is an important oilseed, protein and biodiesel crop. It faces significant threats from bacterial, fungal and viral pathogens, which cause economic losses and jeopardises global food security. In this article, we explore the relationship between soybeans and these pathogens, focusing on the molecular responses that are crucial for soybeans defence mechanisms. Molecular responses involve small RNAs and specific genes, including resistance (R) genes that are pivotal in triggering immune responses. Functional genomics, which makes use of cutting-edge technologies, such as CRISPR Cas9 gene editing, allows us to identify genes that provide insights into the defence mechanisms of soybeans with the focus on using genomics to understand the mechanisms involved in host pathogen interactions and ultimately improve the resilience of soybeans. Genes like GmKR3 and GmVQ58 have demonstrated resistance against soybean mosaic virus and common cutworm, respectively. Genetic studies have identified quantitative trait loci (QTLs) including those linked with soybean cyst nematode, root-knot nematode and Phytophthora root and stem rot resistance. Additionally, resistance against Asian soybean rust and soybean cyst nematode involves specific genes and their variations in terms of different copy numbers. To address the challenges posed by evolving pathogens and meet the demands of a growing population, accelerated soybean breeding efforts leveraging functional genomics are imperative. Targeted breeding strategies based on a deeper understanding of soybean gene function and regulation will enhance disease resistance, ensuring sustainable agriculture and global food security. Collaborative research and continued technological advancements are crucial for securing a resilient and productive agricultural future.
Keywords: CRISPR Cas9, food security, pathogen resistance genes, plant defence, R genes, soybean cyst nematode, soybean genomics, small RNA.
References
Abd-Elgawad MMM (2022) Understanding molecular plant–nematode interactions to develop alternative approaches for nematode control. Plants 11, 2141.
| Crossref | Google Scholar | PubMed |
Akbar S, Wei Y, Zhang M-Q (2022) RNA interference: promising approach to combat plant viruses. International Journal of Molecular Sciences 23, 5312.
| Crossref | Google Scholar | PubMed |
Alizadeh M, Vasebi Y, Chauhan M, Rani A (2021) Biopriming: a prospective techniques for crop improvement. Innovations 66, 1035-1058.
| Google Scholar |
Allen TW, Bradley CA, Sisson AJ, Byamukama E, Chilvers MI, Coker CM, Collins AA, Damicone JP, Dorrance AE, Dufault NS, et al. (2017) Soybean yield loss estimates due to diseases in the United States and Ontario, Canada, from 2010 to 2014. Plant Health Progress 18, 19-27.
| Crossref | Google Scholar |
Ansari M, Ahmed S, Khan MT, Hamad NA, Ali HM, Abbasi A, Mubeen I, Intisar A, Hasan ME, Jasim IK (2023) Evaluation of in vitro and in vivo antifungal activity of green synthesized silver nanoparticles against early blight in tomato. Horticulturae 9, 369.
| Crossref | Google Scholar |
Arjoune Y, Sugunaraj N, Peri S, Nair SV, Skurdal A, Ranganathan P, Johnson B (2022) Soybean cyst nematode detection and management: a review. Plant Methods 18, 110.
| Crossref | Google Scholar |
Ashfield T, Redditt T, Russell A, Kessens R, Rodibaugh N, Galloway L, Kang Q, Podicheti R, Innes RW (2014) Evolutionary relationship of disease resistance genes in soybean and Arabidopsis specific for the Pseudomonas syringae effectors AvrB and AvrRpm1. Plant Physiology 166, 235-251.
| Crossref | Google Scholar | PubMed |
Aung K, Jiang Y, He SY (2018) The role of water in plant–microbe interactions. The Plant Journal 93, 771-780.
| Crossref | Google Scholar | PubMed |
Babu M, Gagarinova AG, Brandle JE, Wang A (2008) Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. Journal of General Virology 89, 1069-1080.
| Crossref | Google Scholar | PubMed |
Barilli E, Rubiales D, Gjetting T, Lyngkjaer MF (2014) Differential gene transcript accumulation in peas in response to powdery mildew (Erysiphe pisi) attack. Euphytica 198, 13-28.
| Crossref | Google Scholar |
Bayless AM, Zapotocny RW, Grunwald DJ, Amundson KK, Diers BW, Bent AF (2018) An atypical N-ethylmaleimide sensitive factor enables the viability of nematode-resistant Rhg1 soybeans. Proceedings of the National Academy of Sciences 115, E4512-E4521.
| Crossref | Google Scholar |
Beattie GA (2011) Water relations in the interaction of foliar bacterial pathogens with plants. Annual Review of Phytopathology 49, 533-555.
| Crossref | Google Scholar | PubMed |
Bebber DP, Gurr SJ (2015) Crop-destroying fungal and oomycete pathogens challenge food security. Fungal Genetics and Biology 74, 62-64.
| Crossref | Google Scholar | PubMed |
Beneventi MA, da Silva OB, de Sá MEL, Firmino AAP, de Amorim RMS, Albuquerque ÉVS, da Silva MCM, da Silva JP, Campos MdA, Lopes MJC, Togawa RC, Pappas GJ, Grossi–de–Sa MF (2013) Transcription profile of soybean-root-knot nematode interaction reveals a key role of phythormones in the resistance reaction. BMC Genomics 14, 322.
| Crossref | Google Scholar |
Benjamin G, Pandharikar G, Frendo P (2022) Salicylic acid in plant symbioses: beyond plant pathogen interactions. Biology 11, 861.
| Crossref | Google Scholar | PubMed |
Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Science 20, 254-255.
| Crossref | Google Scholar |
Buss GR, Ma G, Chen P, Tolin SA (1997) Registration of V94-5152 soybean germplasm resistant to soybean mosaic potyvirus. Crop Science 37, 1987-1988.
| Crossref | Google Scholar |
Buzzell RI, Tu JC (1989) Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic virus. Journal of Heredity 80, 400-401.
| Crossref | Google Scholar |
Cervantes-Martinez I, Chen P, Orazaly M, Klepadlo M (2015) Identification of a new allele at the Rsv3 locus for resistance to Soybean mosaic virus in PI 61944 soybean accession. Crop Science 55, 999-1005.
| Crossref | Google Scholar |
Chang H-X, Lipka AE, Domier LL, Hartman GL (2016) Characterization of disease resistance loci in the USDA soybean germplasm collection using genome-wide association studies. Phytopathology 106, 1139-1151.
| Crossref | Google Scholar | PubMed |
Che Z, Zhang S, Pu Y, Yang Y, Liu H, Yang H, Wang L, Zhang Y, Liu B, Zhang H, et al. (2023) A novel soybean malectin-like receptor kinase-encoding gene, GmMLRK1, provides resistance to soybean mosaic virus. Journal of Experimental Botany 74, 2692-2706.
| Crossref | Google Scholar | PubMed |
Chen P, Buss GR, Roane CW, Tolin SA (1991) Allelism among genes for resistance to soybean mosaic virus in strain-differential soybean cultivars. Crop Science 31, 305-309.
| Crossref | Google Scholar |
Chen P, Buss GR, Tolin SA (1993) Resistance to soybean mosaic virus conferred by two independent dominant genes in PI 486355. Journal of Heredity 84, 25-28.
| Crossref | Google Scholar |
Chen P, Ma G, Buss GR, Gunduz I, Roane CW, Tolin SA (2001) Inheritance and allelism tests of Raiden soybean for resistance to soybean mosaic virus. Journal of Heredity 92, 51-55.
| Crossref | Google Scholar | PubMed |
Chen P, Buss GR, Tolin SA, Gunduz I, Cicek M (2002) A valuable gene in Suweon 97 soybean for resistance to soybean mosaic virus. Crop Science 42, 333-337.
| Crossref | Google Scholar |
Chen H, Arsovski AA, Yu K, Wang A (2016) Genome-wide investigation using sRNA-seq, degradome-seq and transcriptome-seq reveals regulatory networks of microRNAs and their target genes in soybean during soybean mosaic virus infection. PLoS ONE 11, e0150582.
| Crossref | Google Scholar | PubMed |
Cheng YW, Chan KL (1968) The breeding of rust resistance soybean ‘Tainung 3’. Journal of Taiwan Agricultural Research 17, 30-34.
| Google Scholar |
Cheng Y, Ma Q, Ren H, Xia Q, Song E, Tan Z, Li S, Zhang G, Nian H (2017) Fine mapping of a Phytophthora-resistance gene RpsWY in soybean (Glycine max L.) by high-throughput genome-wide sequencing. Theoretical and Applied Genetics 130, 1041-1051.
| Crossref | Google Scholar | PubMed |
Chowda-Reddy RV, Sun H, Chen H, Poysa V, Ling H, Gijzen M, Wang A (2011a) Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. Molecular Plant-Microbe Interactions 24, 37-43.
| Crossref | Google Scholar | PubMed |
Chowda-Reddy RV, Sun H, Hill JH, Poysa V, Wang A (2011b) Simultaneous mutations in multi-viral proteins are required for Soybean mosaic virus to gain virulence on soybean genotypes carrying different R genes. PLoS ONE 6, e28342.
| Crossref | Google Scholar | PubMed |
Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, et al. (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338, 1206-1209.
| Crossref | Google Scholar | PubMed |
Cook DE, Bayless AM, Wang K, Guo X, Song Q, Jiang J, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiology 165, 630-647.
| Crossref | Google Scholar | PubMed |
Cooper B, Campbell KB, Feng J, Garrett WM, Frederick R (2011) Nuclear proteomic changes linked to soybean rust resistance. Molecular BioSystems 7, 773-783.
| Crossref | Google Scholar | PubMed |
Dana H, Chalbatani GM, Mahmoodzadeh H, Karimloo R, Rezaiean O, Moradzadeh A, Mehmandoost N, Moazzen F, Mazraeh A, Marmari V, et al. (2017) Molecular mechanisms and biological functions of siRNA. International Journal of Biomedical Science 13, 48-57.
| Crossref | Google Scholar | PubMed |
de Wit PJGM (2016) Cladosporium fulvum effectors: weapons in the arms race with tomato. Annual Review of Phytopathology 54, 1-23.
| Crossref | Google Scholar | PubMed |
Dixon RA, Achnine L, Kota P, Liu C-J, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defence – a genomics perspective. Molecular Plant Pathology 3, 371-390.
| Crossref | Google Scholar | PubMed |
Dong L, Cheng Y, Wu J, Cheng Q, Li W, Fan S, Jiang L, Xu Z, Kong F, Zhang D, Xu P, Zhang S (2015) Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean. Journal of Experimental Botany 66, 2635-2647.
| Crossref | Google Scholar | PubMed |
Dong J, Zielinski RE, Hudson ME (2020) t-SNAREs bind the Rhg1 α-SNAP and mediate soybean cyst nematode resistance. The Plant Journal 104, 318-331.
| Crossref | Google Scholar | PubMed |
Dorrance AE, McClure SA, St. Martin SK (2003) Effect of partial resistance on Phytophthora stem rot incidence and yield of soybean in Ohio. Plant Disease 87, 308-312.
| Crossref | Google Scholar | PubMed |
Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences 109, E2183-E2191.
| Crossref | Google Scholar |
Du H, Fang C, Li Y, Kong F, Liu B (2023) Understandings and future challenges in soybean functional genomics and molecular breeding. Journal of Integrative Plant Biology 65, 468-495.
| Crossref | Google Scholar | PubMed |
Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V (2021) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Frontiers in Plant Science 11, 552969.
| Crossref | Google Scholar | PubMed |
Durrant WE, Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185-209.
| Crossref | Google Scholar | PubMed |
Dutta TK, Banakar P, Rao U (2015) The status of RNAi-based transgenic research in plant nematology. Frontiers in Microbiology 5, 760.
| Crossref | Google Scholar | PubMed |
Ellendorff U, Fradin EF, de Jonge R, Thomma BPHJ (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. Journal of Experimental Botany 60, 591-602.
| Crossref | Google Scholar | PubMed |
Farhatullah A, Stayton MM, Groose RW, Khan MJ (2011) Genetic analysis of race-specificity of Pseudomonas syringae pv. glycinea. Pakistan Journal of Botany 43, 7-13.
| Google Scholar |
Feng L, Sun J, Jiang Y, Duan X (2022) Role of reactive oxygen species against pathogens in relation to postharvest disease of papaya fruit. Horticulturae 8, 205.
| Crossref | Google Scholar |
Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275-296.
| Crossref | Google Scholar |
Forghani F, Hajihassani A (2020) Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Frontiers in Plant Science 11, 1125.
| Crossref | Google Scholar | PubMed |
Freeman BC, Beattie GA (2009) Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 22, 857-867.
| Crossref | Google Scholar | PubMed |
Garcia A, Calvo ÉS, de Souza Kiihl RA, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theoretical and Applied Genetics 117, 545-553.
| Crossref | Google Scholar | PubMed |
Geng X, Jin L, Shimada M, Kim MG, Mackey D (2014) The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta 240, 1149-1165.
| Crossref | Google Scholar | PubMed |
Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, Dangl JL, Grant SR (2008) The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Molecular Plant-Microbe Interactions 21, 361-370.
| Crossref | Google Scholar | PubMed |
Gouveia BC, Calil IP, Machado JPB, Santos AA, Fontes EPB (2017) Immune receptors and co-receptors in antiviral innate immunity in plants. Frontiers in Microbiology 7, 2139.
| Crossref | Google Scholar | PubMed |
Grennan AK (2006) Plant response to bacterial pathogens. Overlap between innate and gene-for-gene defense response. Plant Physiology 142, 809-811.
| Crossref | Google Scholar | PubMed |
Gudesblat GE, Torres PS, Vojno AA (2009a) Stomata and pathogens: warfare at the gates. Plant Signaling & Behavior 4, 1114-1116.
| Crossref | Google Scholar | PubMed |
Gudesblat GE, Torres PS, Vojnov AA (2009b) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiology 149, 1017-1027.
| Crossref | Google Scholar | PubMed |
Guimarães RL, Stotz HU (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiology 136, 3703-3711.
| Crossref | Google Scholar | PubMed |
Gunduz I, Buss GR, Ma G, Chen P, Tolin SA (2001) Genetic analysis of resistance to Soybean mosaic virus in OX670 and Harosoy soybean. Crop Science 41, 1785-1791.
| Crossref | Google Scholar |
Gunduz I, Buss GR, Chen P, Tolin SA (2002) Characterization of SMV resistance genes in Tousan 140 and Hourei soybean. Crop Science 42, 90-95.
| Crossref | Google Scholar | PubMed |
Gunduz I, Buss GR, Chen P, Tolin SA (2004) Genetic and phenotypic analysis of Soybean mosaic virus resistance in PI 88788 soybean. Phytopathology 94, 687-692.
| Crossref | Google Scholar | PubMed |
Guo X, Chronis D, De La Torre CM, Smeda J, Wang X, Mitchum MG (2015) Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors. Plant Biotechnology Journal 13, 801-810.
| Crossref | Google Scholar | PubMed |
Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Science 26, 1135-1136.
| Crossref | Google Scholar |
Hartwig EE, Bromfield KR (1983) Relationships among three genes conferring specific resistance to rust in soybeans. Crop Science 23, 237-239.
| Crossref | Google Scholar |
Hidayat O, Somaatmadja S (1979) Screening of soybean breeding lines for resistance to soybean rust (Phakopsora pachyrhizi Sydow). Soybean Rust Newsletter 2, 9-22.
| Google Scholar |
Hina A, Cao Y, Song S, Li S, Sharmin RA, Elattar MA, Bhat JA, Zhao T (2020) High-resolution mapping in two RIL populations refines major “QTL Hotspot” regions for seed size and shape in soybean (Glycine max L.). International Journal of Molecular Sciences 21, 1040.
| Crossref | Google Scholar | PubMed |
Huang J, Yang M, Lu L, Zhang X (2016) Diverse functions of small RNAs in different plant–pathogen communications. Frontiers in Microbiology 7, 1552.
| Crossref | Google Scholar | PubMed |
Hwang T-Y, Moon J-K, Yu S, Yang K, Mohankumar S, Yu YH, Lee YH, Kim HS, Kim HM, Maroof MAS, Jeong S-C (2006) Application of comparative genomics in developing molecular markers tightly linked to the virus resistance gene Rsv4 in soybean. Genome 49, 380-388.
| Crossref | Google Scholar | PubMed |
Ibrahim HMM, Alkharouf NW, Meyer SLF, Aly MAM, Gamal El-Din AEKY, Hussein EHA, Matthews BF (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Experimental Parasitology 127, 90-99.
| Crossref | Google Scholar | PubMed |
Islam W, Islam Su, Qasim M, Wang L (2017) Host-Pathogen interactions modulated by small RNAs. RNA Biology 14, 891-904.
| Crossref | Google Scholar | PubMed |
Jahan MA, Harris B, Lowery M, Infante AM, Percifield RJ, Kovinich N (2020) Glyceollin transcription factor GmMYB29A2 regulates soybean resistance to Phytophthora sojae. Plant Physiology 183, 530-546.
| Crossref | Google Scholar | PubMed |
Jiang J, Zhu H, Li N, Batley J, Wang Y (2022) The miR393-target module regulates plant development and responses to biotic and abiotic stresses. International Journal of Molecular Sciences 23, 9477.
| Crossref | Google Scholar | PubMed |
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323-329.
| Crossref | Google Scholar | PubMed |
Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946-961.
| Crossref | Google Scholar | PubMed |
Joshi I, Kohli D, Pal A, Chaudhury A, Sirohi A, Jain PK (2022) Host delivered-RNAi of effector genes for imparting resistance against root-knot and cyst nematodes in plants. Physiological and Molecular Plant Pathology 118, 101802.
| Crossref | Google Scholar |
Jwa N-S, Hwang BK (2017) Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Frontiers in Plant Science 8, 1687.
| Crossref | Google Scholar | PubMed |
Kandoth PK, Heinz R, Yeckel G, Gross NW, Juvale PS, Hill J, Whitham SA, Baum TJ, Mitchum MG (2013) A virus-induced gene silencing method to study soybean cyst nematode parasitism in Glycine max. BMC Research Notes 6, 255.
| Crossref | Google Scholar |
Kang YJ, Kim KH, Shim S, Yoon MY, Sun S, Kim MY, Van K, Lee S-H (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biology 12, 139.
| Crossref | Google Scholar |
Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Jr., Zhu J-K, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proceedings of the National Academy of Sciences 103, 18002-18007.
| Crossref | Google Scholar |
Keen NT, Buzzell RI (1991) New disease resistance genes in soybean against Pseudomonas syringae pv glycinea: evidence that one of them interacts with a bacterial elicitor. Theoretical and Applied Genetics 81, 133-138.
| Crossref | Google Scholar | PubMed |
Kiihl RAS, Hartwig EE (1979) Inheritance of reaction to soybean mosaic virus in soybeans. Crop Science 19, 372-375.
| Crossref | Google Scholar |
Kim DH, Kim KH, Van K, Kim MY, Lee S-H (2010) Fine mapping of a resistance gene to bacterial leaf pustule in soybean. Theoretical and Applied Genetics 120, 1443-1450.
| Crossref | Google Scholar | PubMed |
Kim KH, Park J-H, Kim MY, Heu S, Lee S-H (2011) Genetic mapping of novel symptom in response to soybean bacterial leaf pustule in PI 96188. Journal of Crop Science and Biotechnology 14, 119-123.
| Crossref | Google Scholar |
Klepadlo M, Chen P, Wu C (2016) Genetic analysis of resistance to Soybean mosaic virus in PI 438307 soybean accession. Crop Science 56, 3016-3023.
| Crossref | Google Scholar |
Klepadlo M, Chen P, Shi A, Mason RE, Korth KL, Srivastava V, Wu C (2017a) Two tightly linked genes for soybean mosaic virus resistance in soybean. Crop Science 57, 1844-1853.
| Crossref | Google Scholar |
Klepadlo M, Chen P, Shi A, Mason RE, Korth KL, Srivastava V (2017b) Single nucleotide polymorphism markers for rapid detection of the Rsv4 locus for soybean mosaic virus resistance in diverse germplasm. Molecular Breeding 37, 10.
| Crossref | Google Scholar |
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annual Review of Phytopathology 47, 39-62.
| Crossref | Google Scholar | PubMed |
Lee TG, Diers BW, Hudson ME (2016) An efficient method for measuring copy number variation applied to improvement of nematode resistance in soybean. The Plant Journal 88, 143-153.
| Crossref | Google Scholar | PubMed |
Leibman-Markus M, Schneider A, Gupta R, Marash I, Rav-David D, Carmeli-Weissberg M, Elad Y, Bar M (2023) Immunity priming uncouples the growth–defense trade-off in tomato. Development 150, dev201158.
| Crossref | Google Scholar |
Li D, Chen P, Alloatti J, Shi A, Chen YF (2010) Identification of new alleles for resistance to Soybean mosaic virus in soybean. Crop Science 50, 649-655.
| Crossref | Google Scholar |
Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance gene in PI 567102B. Theoretical and Applied Genetics 125, 133-142.
| Crossref | Google Scholar | PubMed |
Li B, Lu D, Shan L (2014) Ubiquitination of pattern recognition receptors in plant innate immunity. Molecular Plant Pathology 15, 737-746.
| Crossref | Google Scholar | PubMed |
Li S, Castillo-González C, Yu B, Zhang X (2017) The functions of plant small RNAs in development and in stress responses. The Plant Journal 90, 654-670.
| Crossref | Google Scholar | PubMed |
Li X, Qin R, Du Q, Cai L, Hu D, Du H, Yang H, Wang J, Huang F, Wang H, Yu D (2020) Knockdown of GmVQ58 encoding a VQ motif-containing protein enhances soybean resistance to the common cutworm (Spodoptera litura Fabricius). Journal of Experimental Botany 71, 3198-3210.
| Crossref | Google Scholar | PubMed |
Liao L, Chen P, Buss GR, Yang Q, Tolin SA (2002) Inheritance and allelism of resistance to soybean mosaic virus in Zao18 soybean from China. Journal of Heredity 93, 447-452.
| Crossref | Google Scholar | PubMed |
Liao L, Chen P, Rajcan I, Buss GR, Tolin SA (2011) Genetic analysis of “8101” soybean containing three genes for resistance to soybean mosaic virus. Crop Science 51, 503-511.
| Crossref | Google Scholar |
Lin J, Mazarei M, Zhao N, Hatcher CN, Wuddineh WA, Rudis M, Tschaplinski TJ, Pantalone VR, Arelli PR, Hewezi T, Chen F, Stewart CN, Jr (2016) Transgenic soybean overexpressing GmSAMT1 exhibits resistance to multiple-HG types of soybean cyst nematode Heterodera glycines. Plant Biotechnology Journal 14, 2100-2109.
| Crossref | Google Scholar | PubMed |
Liston A, Masters SL (2017) Homeostasis-altering molecular processes as mechanisms of inflammasome activation. Nature Reviews Immunology 17, 208-214.
| Crossref | Google Scholar | PubMed |
Liu C-W, Murray JD (2016) The role of flavonoids in nodulation host-range specificity: an update. Plants 5, 33.
| Crossref | Google Scholar | PubMed |
Liu J-Z, Horstman HD, Braun E, Graham MA, Zhang C, Navarre D, Qiu W-L, Lee Y, Nettleton D, Hill JH, Whitham SA (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiology 157, 1363-1378.
| Crossref | Google Scholar | PubMed |
Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale PS, et al. (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492, 256-260.
| Crossref | Google Scholar | PubMed |
Liu J-Z, Braun E, Qiu W-L, Shi Y-F, Marcelino-Guimarães FC, Navarre D, Hill JH, Whitham SA (2014) Positive and negative roles for soybean MPK6 in regulating defense responses. Molecular Plant-Microbe Interactions 27, 824-834.
| Crossref | Google Scholar | PubMed |
Liu Z, Shi L, Yang S, Lin Y, Weng Y, Li X, Hussain A, Noman A, He S (2017) Functional and promoter analysis of ChiIV3, a chitinase of pepper plant, in response to Phytophthora capsici infection. International Journal of Molecular Sciences 18, 1661.
| Crossref | Google Scholar | PubMed |
Liu S, Liu Z, Hou X, Li X (2023) Genetic mapping and functional genomics of soybean seed protein. Molecular Breeding 43, 29.
| Crossref | Google Scholar | PubMed |
Lozano-Durán R, Bourdais G, He SY, Robatzek S (2014) The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytologist 202, 259-269.
| Crossref | Google Scholar | PubMed |
Ma G, Chen P, Buss GR, Tolin SA (1995) Genetic characteristics of two genes for resistance to soybean mosaic virus in PI486355 soybean. Theoretical and Applied Genetics 91, 907-914.
| Crossref | Google Scholar | PubMed |
Ma G, Chen P, Buss GR, Tolin SA (2002) Complementary action of two independent dominant genes in Columbia soybean for resistance to soybean mosaic virus. Journal of Heredity 93, 179-184.
| Crossref | Google Scholar | PubMed |
Ma G, Chen P, Buss GR, Tolin SA (2003) Genetic study of a lethal necrosis to soybean mosaic virus in PI 507389 soybean. Journal of Heredity 94, 205-211.
| Crossref | Google Scholar | PubMed |
Machado ACZ (2014) Current nematode threats to Brazilian agriculture. Current Agricultural Science and Technology 20, 26-55.
| Google Scholar |
Martinez G, Köhler C (2017) Role of small RNAs in epigenetic reprogramming during plant sexual reproduction. Current Opinion in Plant Biology 36, 22-28.
| Crossref | Google Scholar | PubMed |
McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiology 159, 1295-1308.
| Crossref | Google Scholar | PubMed |
McLachlan DH, Kopischke M, Robatzek S (2014) Gate control: guard cell regulation by microbial stress. New Phytologist 203, 1049-1063.
| Crossref | Google Scholar | PubMed |
McLean RJ, Byth DE (1980) Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. Australian Journal of Agricultural Research 31, 951-956.
| Crossref | Google Scholar |
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969-980.
| Crossref | Google Scholar | PubMed |
Meyer JDF, Silva DCG, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA, Graham MA (2009) Identification and analyses of candidate genes for Rpp4-mediated resistance to Asian soybean rust in soybean. Plant Physiology 150, 295-307.
| Crossref | Google Scholar | PubMed |
Mitchum MG (2016) Soybean resistance to the soybean cyst nematode Heterodera glycines: an update. Phytopathology 106, 1444-1450.
| Crossref | Google Scholar | PubMed |
Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Science 47, 829-834.
| Crossref | Google Scholar |
Morales AMAP, O’Rourke JA, Van De Mortel M, Scheider KT, Bancroft TJ, Borém A, Nelson RT, Nettleton D, Baum TJ, Shoemaker RC, et al. (2013) Transcriptome analyses and virus induced gene silencing identify genes in the Rpp4-mediated Asian soybean rust resistance pathway. Functional Plant Biology 40, 1029-1047.
| Crossref | Google Scholar | PubMed |
Mubarik MS, Wang X, Khan SH, Ahmad A, Khan Z, Amjid MW, Razzaq MK, Ali Z, Azhar MT (2021) Engineering broad-spectrum resistance to cotton leaf curl disease by CRISPR-Cas9 based multiplex editing in plants. GM Crops & Food 12, 647-658.
| Crossref | Google Scholar | PubMed |
Narvel J, Jakkula L, Phillips D, Wang T, Lee S-H, Boerma H (2001) Molecular mapping of Rxp conditioning reaction to bacterial pustule in soybean. Journal of Heredity 92, 267-270.
| Crossref | Google Scholar | PubMed |
Natarajan S, Tavakolan M, Alkharouf NW, Matthews BF (2014) SCNProDB: a database for the identification of soybean cyst nematode proteins. Bioinformation 10, 387-389.
| Crossref | Google Scholar | PubMed |
Newman M-A, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers in Plant Science 4, 139.
| Crossref | Google Scholar | PubMed |
Nicaise V (2014) Crop immunity against viruses: outcomes and future challenges. Frontiers in Plant Science 5, 660.
| Crossref | Google Scholar | PubMed |
Niu J, Guo N, Sun J, Li L, Cao Y, Li S, Huang J, Zhao J, Zhao T, Xing H (2017) Fine mapping of a resistance gene RpsHN that controls Phytophthora sojae using recombinant inbred lines and secondary populations. Frontiers in Plant Science 8, 538.
| Google Scholar | PubMed |
Noman A, Fahad S, Aqeel M, Ali U, Amanullah , Anwar S, Baloch SK, Zainab M (2017) miRNAs: major modulators for crop growth and development under abiotic stresses. Biotechnology Letters 39, 685-700.
| Crossref | Google Scholar | PubMed |
Noon JB, Hewezi T, Baum TJ (2019) Homeostasis in the soybean miRNA396–GRF network is essential for productive soybean cyst nematode infections. Journal of Experimental Botany 70, 1653-1668.
| Crossref | Google Scholar | PubMed |
Ochola S, Huang J, Ali H, Shu H, Shen D, Qiu M, Wang L, Li X, Chen H, Kange A, Qutob D, Dong S (2020) Editing of an effector gene promoter sequence impacts plant-Phytophthora interaction. Journal of Integrative Plant Biology 62, 378-392.
| Crossref | Google Scholar | PubMed |
Ogle HJ, Byth DE, McLean R (1979) Effect of rust (Phakopsora pachyrhizi) on soybean yield and quality in south-eastern Queensland. Australian Journal of Agricultural Research 30, 883-893.
| Crossref | Google Scholar |
Park C-J, Caddell DF, Ronald PC (2012) Protein phosphorylation in plant immunity: insights into the regulation of pattern recognition receptor-mediated signaling. Frontiers in Plant Science 3, 177.
| Crossref | Google Scholar | PubMed |
Patil VS, Wuike RV, Thakare CS, Chirame BB (1997) Viability of uredospores of Phakopsora pachyrhizi Syd. at different storage conditions. Journal of Maharashtra Agricultural Universities 22, 260-261.
| Google Scholar |
Patil G, Mian R, Vuong T, Pantalone V, Song Q, Chen P, Shannon GJ, Carter TC, Nguyen HT (2017) Molecular mapping and genomics of soybean seed protein: a review and perspective for the future. Theoretical and Applied Genetics 130, 1975-1991.
| Crossref | Google Scholar | PubMed |
Pedley KF, Pandey AK, Ruck A, Lincoln LM, Whitham SA, Graham MA (2019) Rpp1 encodes a ULP1-NBS-LRR protein that controls immunity to Phakopsora pachyrhizi in soybean. Molecular Plant-Microbe Interactions 32, 120-133.
| Crossref | Google Scholar | PubMed |
Peláez P, Sanchez F (2013) Small RNAs in plant defense responses during viral and bacterial interactions: similarities and differences. Frontiers in Plant Science 4, 343.
| Crossref | Google Scholar | PubMed |
Petitot A-S, Kyndt T, Haidar R, Dereeper A, Collin M, de Almeida Engler J, Gheysen G, Fernandez D (2017) Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots. Annals of Botany 119, 885-899.
| Crossref | Google Scholar | PubMed |
Rambani A, Pantalone V, Yang S, Rice JH, Song Q, Mazarei M, Arelli PR, Meksem K, Stewart CN, Hewezi T (2020) Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. New Phytologist 227, 168-184.
| Crossref | Google Scholar | PubMed |
Rani R, Raza G, Ashfaq H, Rizwan M, Razzaq MK, Waheed MQ, Shimelis H, Babar AD, Arif M (2023a) Genome-wide association study of soybean (Glycine max [L.] Merr.) germplasm for dissecting the quantitative trait nucleotides and candidate genes underlying yield-related traits. Frontiers in Plant Science 14, 1229495.
| Crossref | Google Scholar |
Rani R, Raza G, Tung MH, Rizwan M, Ashfaq H, Shimelis H, Razzaq MK, Arif M (2023b) Genetic diversity and population structure analysis in cultivated soybean (Glycine max [L.] Merr.) using SSR and EST-SSR markers. PLoS ONE 18, e0286099.
| Crossref | Google Scholar | PubMed |
Razzaq MK, Aleem M, Mansoor S, Khan MA, Rauf S, Iqbal S, Siddique KHM (2021) Omics and CRISPR-Cas9 approaches for molecular insight, functional gene analysis, and stress tolerance development in crops. International Journal of Molecular Sciences 22, 1292.
| Crossref | Google Scholar | PubMed |
Razzaq MK, Akhter M, Ahmad RM, Cheema KL, Hina A, Karikari B, Raza G, Xing G, Gai J, Khurshid M (2022) CRISPR-Cas9 based stress tolerance: new hope for abiotic stress tolerance in chickpea (Cicer arietinum). Molecular Biology Reports 49, 8977-8985.
| Crossref | Google Scholar | PubMed |
Razzaq MK, Hina A, Abbasi A, Karikari B, Ashraf HJ, Mohiuddin M, Maqsood S, Maqsood A, Haq IU, Xing G, Raza G, Bhat JA (2023a) Molecular and genetic insights into secondary metabolic regulation underlying insect-pest resistance in legumes. Functional & Integrative Genomics 23, 217.
| Crossref | Google Scholar | PubMed |
Razzaq MK, Rani R, Xing G, Xu Y, Raza G, Aleem M, Iqbal S, Arif M, Mukhtar Z, Nguyen HT, et al. (2023b) Genome-wide identification and analysis of the Hsp40/J-protein family reveals its role in soybean (Glycine max) growth and development. Genes 14, 1254.
| Crossref | Google Scholar | PubMed |
Rosso M-N, Dubrana MP, Cimbolini N, Jaubert S, Abad P (2005) Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Molecular Plant-Microbe Interactions 18, 615-620.
| Crossref | Google Scholar | PubMed |
Roth MG, Webster RW, Mueller DS, Chilvers MI, Faske TR, Mathew FM, Bradley CA, Damicone JP, Kabbage M, Smith DL (2020) Integrated management of important soybean pathogens of the United States in changing climate. Journal of Integrated Pest Management 11, 17.
| Crossref | Google Scholar |
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends in Plant Science 15, 247-258.
| Crossref | Google Scholar | PubMed |
Saghai Maroof MA, Jeong SC, Gunduz I, Tucker DM, Buss GR, Tolin SA (2008) Pyramiding of soybean mosaic virus resistance genes by marker-assisted selection. Crop Science 48, 517-526.
| Crossref | Google Scholar |
Samac DA, Peñuela S, Schnurr JA, Hunt EN, Foster-Hartnett D, Vandenbosch KA, Gantt JS (2011) Expression of coordinately regulated defence response genes and analysis of their role in disease resistance in Medicago truncatula. Molecular Plant Pathology 12, 786-798.
| Crossref | Google Scholar | PubMed |
Santoni G, Cardinali C, Morelli MB, Santoni M, Nabissi M, Amantini C (2015) Danger- and pathogen-associated molecular patterns recognition by pattern-recognition receptors and ion channels of the transient receptor potential family triggers the inflammasome activation in immune cells and sensory neurons. Journal of Neuroinflammation 12, 21.
| Crossref | Google Scholar | PubMed |
Saur IML, Panstruga R, Schulze-Lefert P (2021) NOD-like receptor-mediated plant immunity: from structure to cell death. Nature Reviews Immunology 21, 305-318.
| Crossref | Google Scholar | PubMed |
Schmitthenner AF (2000) Phytophthora rot of soybean. Plant Health Progress 1, 13.
| Crossref | Google Scholar |
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183.
| Crossref | Google Scholar | PubMed |
Schuebel F, Rocker A, Edelmann D, Schessner J, Brieke C, Meinhart A (2016) 3′-NADP and 3′-NAADP, two metabolites formed by the bacterial type III effector AvrRxo1. Journal of Biological Chemistry 291, 22868-22880.
| Crossref | Google Scholar | PubMed |
Selote D, Shine MB, Robin GP, Kachroo A (2014) Soybean NDR 1-like proteins bind pathogen effectors and regulate resistance signaling. New Phytologist 202, 485-498.
| Crossref | Google Scholar | PubMed |
Senthil-Kumar M, Mysore KS (2011) New dimensions for VIGS in plant functional genomics. Trends in Plant Science 16, 656-665.
| Crossref | Google Scholar | PubMed |
Seo M, Kang S-T, Moon J-K, Lee S-K, Kim Y-H, Jeong K-H, Yun H-T (2009) Identification of quantitative trait loci associated with resistance to bacterial pustule (Xanthomonas axonopodis pv. glycines) in Soybean. Korean Journal of Breeding Science 41, 456-462.
| Google Scholar |
Shakiba E, Chen P, Shi A, Li D, Dong D, Brye K (2012) Two novel alleles at the Rsv 3 locus for resistance to Soybean mosaic virus in PI 399091 and PI 61947 soybeans. Crop Science 52, 2587-2594.
| Crossref | Google Scholar |
Shakiba E, Chen P, Shi A, Li D, Dong D, Brye K (2013) Inheritance and allelic relationships of resistance genes for Soybean mosaic virus in ‘Corsica’ and ‘Beeson’ soybean. Crop Science 53, 1455-1463.
| Crossref | Google Scholar |
Sharmin RA, Karikari B, Chang F, Al Amin GM, Bhuiyan MR, Hina A, Lv W, Chunting Z, Begum N, Zhao T (2021) Genome-wide association study uncovers major genetic loci associated with seed flooding tolerance in soybean. BMC Plant Biology 21, 497.
| Crossref | Google Scholar |
Shi A, Chen P, Li DX, Zheng C, Hou A, Zhang B (2008) Genetic confirmation of 2 independent genes for resistance to soybean mosaic virus in J05 soybean using SSR markers. Journal of Heredity 99, 598-603.
| Crossref | Google Scholar | PubMed |
Silva DCG, Yamanaka N, Brogin RL, Arias CAA, Nepomuceno AL, Di Mauro AO, Pereira SS, Nogueira LM, Passianotto ALL, Abdelnoor RV (2008) Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theoretical and Applied Genetics 117, 57-63.
| Crossref | Google Scholar | PubMed |
Singh BB (1977) Breeding for resistance to soybean rust in India. Soybean Rust Newsletter 1, 13-16.
| Google Scholar |
Souza TP, Dias RO, Silva-Filho MC (2017) Defense-related proteins involved in sugarcane responses to biotic stress. Genetics and Molecular Biology 40, 360-372.
| Crossref | Google Scholar | PubMed |
Staskawicz BJ, Dahlbeck D, Keen NT (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proceedings of the National Academy of Sciences 81, 6024-6028.
| Crossref | Google Scholar |
Sugimoto T, Kato M, Yoshida S, Matsumoto I, Kobayashi T, Kaga A, Hajika M, Yamamoto R, Watanabe K, Aino M, et al. (2012) Pathogenic diversity of Phytophthora sojae and breeding strategies to develop Phytophthora-resistant soybeans. Breeding Science 61, 511-522.
| Crossref | Google Scholar | PubMed |
Sun Q, Sun Y, Walker MA, Labavitch JM (2013) Vascular occlusions in grapevines with Pierce’s disease make disease symptom development worse. Plant Physiology 161, 1529-1541.
| Crossref | Google Scholar | PubMed |
Trdá L, Boutrot F, Claverie J, Brulé D, Dorey S, Poinssot B (2015) Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Frontiers in Plant Science 6, 219.
| Crossref | Google Scholar | PubMed |
Tucker ML, Xue P, Yang R (2010) 1-Aminocyclopropane-1-carboxylic acid (ACC) concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode (Heterodera glycines)-infected roots. Journal of Experimental Botany 61, 463-472.
| Crossref | Google Scholar | PubMed |
Underwood W (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Frontiers in Plant Science 3, 85.
| Crossref | Google Scholar | PubMed |
Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions 15, 747-752.
| Crossref | Google Scholar | PubMed |
van de Mortel M, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida ÁMR, Baum TJ, Whitham SA (2007) Distinct biphasic mRNA changes in response to Asian soybean rust infection. Molecular Plant-Microbe Interactions 20, 887-899.
| Crossref | Google Scholar | PubMed |
Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55, 85-97.
| Crossref | Google Scholar |
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135-162.
| Crossref | Google Scholar | PubMed |
Wang M, Sun Y, Sun G, Liu X, Zhai L, Shen Q, Guo S (2015) Water balance altered in cucumber plants infected with Fusarium oxysporum f. sp. cucumerinum. Scientific Reports 5, 7722.
| Crossref | Google Scholar | PubMed |
Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118-123.
| Crossref | Google Scholar | PubMed |
Whitham SA, Qi M, Innes RW, Ma W, Lopes-Caitar V, Hewezi T (2016) Molecular soybean-pathogen interactions. Annual Review of Phytopathology 54, 443-468.
| Crossref | Google Scholar | PubMed |
Withers J, Dong X (2017) Post-translational regulation of plant immunity. Current Opinion in Plant Biology 38, 124-132.
| Crossref | Google Scholar | PubMed |
Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. Journal of Nematology 38, 173-180.
| Google Scholar | PubMed |
Wrather JA, Anderson TR, Arsyad DM, Tan Y, Ploper LD, Porta-Puglia A, Ram HH, Yorinori JT (2001a) Soybean disease loss estimates for the top ten soybean-producing counries in 1998. Canadian Journal of Plant Pathology 23, 115-121.
| Crossref | Google Scholar |
Wrather JA, Stienstra WC, Koenning SR (2001b) Soybean disease loss estimates for the United States from 1996 to 1998. Canadian Journal of Plant Pathology 23, 122-131.
| Crossref | Google Scholar |
Xin X-F, Nomura K, Aung K, Velásquez AC, Yao J, Boutrot F, Chang JH, Zipfel C, He SY (2016) Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539, 524-529.
| Crossref | Google Scholar | PubMed |
Xu X, Zeng L, Tao Y, Vuong T, Wan J, Boerma R, Noe J, Li Z, Finnerty S, Pathan SM, Shannon JG, Nguyen HT (2013) Pinpointing genes underlying the quantitative trait loci for root-knot nematode resistance in palaeopolyploid soybean by whole genome resequencing. Proceedings of the National Academy of Sciences 110, 13469-13474.
| Crossref | Google Scholar |
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.
| Crossref | Google Scholar | PubMed |
Yadeta KA, Thomma BPHJ (2013) The xylem as battleground for plant hosts and vascular wilt pathogens. Frontiers in Plant Science 4, 97.
| Crossref | Google Scholar | PubMed |
Yang X, Li Y, Wang A (2021) Research advances in potyviruses: from the laboratory bench to the field. Annual Review of Phytopathology 59, 1-29.
| Crossref | Google Scholar | PubMed |
Yang Z, Zhi P, Chang C (2022) Priming seeds for the future: plant immune memory and application in crop protection. Frontiers in Plant Science 13, 961840.
| Crossref | Google Scholar | PubMed |
Zaynab M, Kanwal S, Hussain I, Qasim M, Noman A, Iqbal U, Ali GM, Bahadar K, Jamil A, Sughra K (2017) Rice chitinase gene expression in genetically engineered potato confers resistance against Fusarium solani and Rhizictonia solani. PSM Microbiology 2, 63-73.
| Crossref | Google Scholar |
Zhang C, Yang C, Whitham SA, Hill JH (2009) Development and use of an efficient DNA-based viral gene silencing vector for soybean. Molecular Plant-Microbe Interactions 22, 123-131.
| Crossref | Google Scholar | PubMed |
Zhang C, Bradshaw JD, Whitham SA, Hill JH (2010) The development of an efficient multipurpose bean pod mottle virus viral vector set for foreign gene expression and RNA silencing. Plant Physiology 153, 52-65.
| Crossref | Google Scholar | PubMed |
Zhang X, Li H, Zhang J, Zhang C, Gong P, Ziaf K, Xiao F, Ye Z (2011) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Research 20, 569-581.
| Crossref | Google Scholar | PubMed |
Zhang C, Ding Z, Wu K, Yang L, Li Y, Yang Z, Shi S, Liu X, Zhao S, Yang Z, et al. (2016) Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice. Molecular Plant 9, 1302-1314.
| Crossref | Google Scholar | PubMed |
Zheng C, Chen P, Gergerich R (2005) Characterization of resistance to Soybean mosaic virus in diverse soybean germplasm. Crop Science 45, 2503-2509.
| Crossref | Google Scholar |
Zheng C, Chen P, Gergerich R (2006) Genetic analysis of resistance to soybean mosaic virus in J05 soybean. Journal of Heredity 97, 429-437.
| Crossref | Google Scholar | PubMed |
Zhong C, Sun S, Li Y, Duan C, Zhu Z (2018a) Next-generation sequencing to identify candidate genes and develop diagnostic markers for a novel Phytophthora resistance gene, RpsHC18, in soybean. Theoretical and Applied Genetics 131, 525-538.
| Crossref | Google Scholar | PubMed |
Zhong C, Sun S, Yao L, Ding J, Duan C, Zhu Z (2018b) Fine mapping and identification of a novel Phytophthora root rot resistance locus RpsZS18 on chromosome 2 in soybean. Frontiers in Plant Science 9, 44.
| Crossref | Google Scholar | PubMed |
Zhong C, Li Y, Sun S, Duan C, Zhu Z (2019) Genetic mapping and molecular characterization of a broad-spectrum Phytophthora sojae resistance gene in Chinese soybean. International Journal of Molecular Sciences 20, 1809.
| Crossref | Google Scholar | PubMed |
Zubaidah S, Mujtahida I, Kuswantoro H (2023) Response of morphological, anatomical, and agronomic characteristics of soybean genotypes to Cowpea Mild Mottle Virus. Biodiversitas Journal of Biological Diversity 24, 4017-4026.
| Crossref | Google Scholar |
Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4, 2578-2597.
| Crossref | Google Scholar | PubMed |
