Abstract
Maize rough dwarf disease (MRDD), caused by maize rough dwarf virus (MRDV) or rice black-streaked dwarf virus (RBSDV), seriously threatens worldwide production of all major cereal crops, including maize, rice, wheat and barley. Here we report fine mapping and cloning of a previously reported major quantitative trait locus (QTL) (qMrdd2) for RBSDV resistance in maize. Subsequently, we show that qMrdd2 encodes a G2-like transcription factor named ZmGLK36 that promotes resistance to RBSDV by enhancing jasmonic acid (JA) biosynthesis and JA-mediated defence response. We identify a 26-bp indel located in the 5′ UTR of ZmGLK36 that contributes to differential expression and resistance to RBSDV in maize inbred lines. Moreover, we show that ZmDBF2, an AP2/EREBP family transcription factor, directly binds to the 26-bp indel and represses ZmGLK36 expression. We further demonstrate that ZmGLK36 plays a conserved role in conferring resistance to RBSDV in rice and wheat using transgenic or marker-assisted breeding approaches. Our results provide insights into the molecular mechanisms of RBSDV resistance and effective strategies to breed RBSDV-resistant cereal crops.
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Data availability
The datasets generated and/or analysed during the current study are provided with this paper. Any additional data are available from the corresponding author. No participant identifiable information will be disclosed. Source data are provided with this paper.
Code availability
The custom codes used in this study are deposited in GitHub (https://github.com/wangtao-go/fpkm/blob/main/calRPKM.pl).
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Acknowledgements
This work was supported by the National Key Research and Development Program of China (2022YFD1201802 and 2020YFE0202300), the National Natural Science Foundation of China (31771804), the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202109) and the Modern Agro-Industry Technology Research System of Maize (CARS-02-02).
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Z.X. performed most of the experiments. Z.X., Z.Z., H.W., J.W. and X. Li designed experiments and wrote the manuscript. Z.C., Q.D. and Y.T. designed the CRISPR target and constructed the plasmid library. W.L., Y.Z. and X. Lu analysed the data. F.W., R.C. and G.L. characterized the genotypes and phenotypes of the edited lines. K.W and W.S. carried out the transformation of transgenic wheat and in part, maize. S.T., M.L., D.Z., H.Y., C.M., Z.H., Z.W. and J.H. provided 226 temperate and 160 American inbred lines of maize. Y.C., Q.M. and X.K. performed the artificial inoculation of RBSDV and field management.
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Extended data
Extended Data Fig. 1 Phenotypic and cytological characteristics of maize rough dwarf disease.
a, Phenotype of Qi319 and Ye478 upon RBSDV infection. “-“ represents virus-free SBPH, and “+“ represents viruliferous SBPH. Scale bars, 35 cm. b, The relative expression of RBSDV coat protein (S10) mRNA. The values are denoted as means ± s.e.m. (n = 3 biologically independent samples). Five plants were taken as one biological replicate. c, d, The MRDD severity at the silking stage could be classified into five grades (0, 1, 2, 3, and 4) in view of the overall symptoms at the silking stage according to plant height and the characteristics of the lesions. Scale bars, 30 cm. e, The healthy plants (NIL-R) or severely diseased plants (NIL-S) of waxy enations on the axial surfaces of upper leaves under artificial inoculation of RBSDV. Scale bars, 1 cm. f, Number of internodes and length of internodes in plants with disease grades 0-4 at the silking stage. Data are means ± s.e.m. (n = 3 biologically independent samples). g, The left panels show the longitudinal sections of eighth internodes from the healthy NIL-R and diseased NIL-S plants. The right panels show transections of the eighth internode from the healthy NIL-R and diseased NIL-S plants. Scale bar, 10 μm. h, Cell length of the eighth internode between the healthy NIL-R and diseased NIL-S plants. Values are means ± SEM. (n = 30 biologically independent samples). Statistical significance was determined using two-sided Student’s t-test. Two independent experiments were performed with similar results in g and h.
Extended Data Fig. 2 The relative expression of candidate genes in the qMrdd2 region.
RT-qPCR assay validates the expression of candidate genes between the NIL-R and NIL-S plants under artificial inoculation of RBSDV at 12 dpi. The values are denoted as means ± s.e.m. (n = 3 independent biologically samples). Five plants were taken as one biological replicate (n = 5). Statistical significance was determined using two-sided Student’s t-test.
Extended Data Fig. 3 Identification of the ZmGLK36 knockout mutants and transgenic plants.
a, b, Sequencing analysis showing mutations in the CRISPR/Cas9-generated Zmglk36 knockout mutants. c, Validation of ZmGLK36 expression in the knockout plants using RT-qPCR. The values are denoted as means ± s.e.m. (n = 3 independent biologically samples). Five plants were taken as one biological replicate (n = 5). Statistical significance was determined using two-sided Student’s t-test.
Extended Data Fig. 4 Molecular characterization of ZmGLK36.
a, Phylogenetic analysis of ZmGLK36 and their orthologues from Arabidopsis, maize, rice and wheat. The phylogenetic tree was generated using the method of maximum likelihood with the MEGA7 software based on the full-length protein sequence. b, RT-qPCR assay showing the transcript abundance of ZmGLK36 in various tissues. Data are means ± s.e.m. (n = 3 independent biologically samples). Five plants were taken as one biological replicate (n = 5). c, The expression pattern of ZmGLK36 revealed by histochemical staining of the transgenic plants carrying a β-glucuronidase (GUS) reporter driven by the endogenous ZmGLK36 promoter. Scale bars, 2.5 cm. d, e, RNA in situ hybridization analysis of ZmGLK36 in leaf. Leaf blades of maize plants were cross-sectioned and hybridized with ZmGLK36-specific sense (d) or antisense (e) probes. Scale bars, 50 μm. f, Subcellular localization of the ZmGLK36-GFP and YFP-ZmGLK36 fusion proteins in maize protoplasts. Scale bars, 10 μm. The results are representative of three independent experiments. TF3 was used as a nuclear marker.
Extended Data Fig. 5 Sequence alignment analysis of ZmGLK36 in Qi319 and Ye478.
a, Structure and sequence comparison of the ZmGLK36 genomic region between Qi319 and Ye478. Black denotes exons. The red lines denote SNPs. b, Alignment of the cDNA sequences of ZmGLK36 in Qi319 and Ye478. c, Amino acid sequence alignment of ZmGLK36 between Qi319 and Ye478.
Extended Data Fig. 6 Phenotypic examination of the ZmGLK36 transgenic plants.
a, Validation of ZmGLK36 expression in the transgenic overexpression plants using RT-qPCR. The values are denoted as means ± s.e.m. (n = 3 independent biologically samples). b, d, The DSI values of the transgenic overexpression plants and Zong31. The plants were planted in Sanya and Beijing and used for artificial inoculation. Data are means ± s.e.m. from 3 biological replicates (n = 50 plants for each replicate). c, e, The relative expression of RBSDV- S10 mRNA in ZmGLK36 overexpression plants and Zong31 at anthesis. The plants were artificially inoculated at the V3 stage. The values are denoted as means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). Statistical significance was determined using two-sided Student’s t-test.
Extended Data Fig. 7 Phenotypic analysis based on marker Indel-26.
a, Sequence alignment analysis of 10 resistant inbred lines and 13 susceptible inbred lines from 226 temperate maize inbred lines based on the 26-bp Indel. b, Co-segregation analysis of the 26-bp Indel with RBSDV resistance using 20 RILs. Data are means ± s.e.m. from 3 biological replicates (n = 17 plants for each replicate). c, Haplotypes of ZmGLK36 among maize germplasm from the tropical maize inbred lines based on the Indel-26. Each point represents the average DSI of two replicates from a maize inbred line. (n = 17 plants for each replicate). Statistical significance was determined using two-sided Student’s t-test.
Extended Data Fig. 8 Predicted transcription factor binding sites in the 26-bp Indel in 5’UTR of ZmGLK36.
a, Diagram shows mutagenesis of the KO-26 knockout mutants. The sequence gap length is shown in parentheses. Red letters represent the 26-bp Indel. Green dashed lines indicate nucleotide deletion. b, Relative expression of ZmGLK36 under RBSDV inoculation (12 dpi). The values are denoted as means ± s.e.m. (n = 3 independent biological samples). Five plants were taken as one biological replicate. Qi319 was used as the positive control. c, DSI values of the KO-26 plants at the silking stage. The plants were inoculated with RBSDV at the V3 stage. Data are means ± s.e.m. from 3 biological replicates (n = 34 plants for each replicate). d, Relative expression of RBSDV coat protein (S10) in B73, KO-26 and Qi319 plants at the silking stage. The plants were inoculated with RBSDV at the V3 stage. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). e, Yeast one-hybrid (Y1H) assay shows that ZmbHLH74, but not ZmP1, binds to the 26-bp fragment. f, Transient transcriptional activity assay in maize protoplasts shows that ZmbHLH74, but not ZmP1, activates the LUC reporter gene expression. Values are means ± s.e.m (n = 5 repeats). g, h, Relative expression levels of ZmDBF2 and ZmbHLH74 in NIL-R and NIL-S after artificial inoculation with RBSDV. The values are denoted as means ± s.e.m. (n = 3 independent biologically samples). Each biological replicate has 5 plants. i, SDS–PAGE analysis of the purified MBP-ZmDBF2 recombinant protein. j, Western blot analysis of the purified MBP-ZmDBF2 recombinant protein by using the anti-MBP antibody. k, RT-qPCR assay showing the transcript abundance analysis of ZmDBF2 in various tissues. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). l, Diagram shows mutagenesis of the ZmDBF2 knockout mutants. m, ZmGLK36 transcript levels in the overexpression and KO lines of ZmDBF2. The values are denoted as means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). Statistical significance was determined using a two-sided t-test. The experiments in i, and j were independently performed two times with similar results.
Extended Data Fig. 9 Yeast two-hybrid assay of the interaction between ZmGLK36 and RBSDV proteins.
Yeast two-hybrid (Y2H) assay shows that there is no direct interaction between ZmGLK36 and RBSDV proteins (S1, S2, S3, S4, S5-1, S5-2, S6, S7-1, S7-2, S8, S9-1, S9-2 and S10).
Extended Data Fig. 10 ZmGLK36 entails the JA signaling pathway for resistance to RBSDV.
a, KEGG estimation of the RNA_seq data based on Zong31 and ZmGLK36 overexpressing plants under nonpathogenic stress conditions. b, KEGG estimation of the RNA_seq data based on NIL-R (inoculation of non-toxic SBPH) and NIL-R (inoculation of poisonous SBPH). c, d, RT-qPCR assay showing the transcript abundance analysis of ZmJMT and ZmLOX8 in Zong31, KO-1ZmGLK36, KO-2ZmGLK36, OE-1ZmGLK36-Qi319 and OE-1ZmGLK36-Ye478. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). e, f, Relative expression of ZmJMT and ZmLOX8 in NIL-S and NIL-R under artificial inoculation with RBSDV. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). g, Transient transcriptional activity assay in maize protoplasts shows that ZmGLK36 activates ZmLOX8 expression. Values are means ± s.e.m (n = 5 repeats). h, SDS–PAGE analysis of the purified His-ZmGLK36 recombinant protein. i, Western blot analysis of the purified His-ZmGLK36 recombinant protein by using the anti-His antibody. j, The left is sequencing peak diagram of premature termination of mutants. The right is relative expression of ZmJMT in wild type (B73) and Zmjmt mutants. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). k, DSI values of Qi319, Ye478, B73 and Zmjmt mutant plants at the salking stage. Data are means ± s.e.m. from 3 biological replicates (n = 34 plants for each replicate). l, Relative expression of RBSDV-S10 mRNA in B73 and Zmjmt mutant plants at the at the silking stage. The values are denoted as means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). m, Determination of JA content in Zong31, transgenic overexpression and knockout plants of ZmDBF2. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). n, RT-qPCR analysis of RBSDV-S10 mRNA accumulation in RBSDV-infected maize leaves pretreated with MeJA. Data are means ± s.e.m. from 3 biological replicates (n = 5 plants for each replicate). Statistical significance was determined using two-sided Student’s t-test. The experiments in h, and i were independently performed two times with similar results.
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Xu, Z., Zhou, Z., Cheng, Z. et al. A transcription factor ZmGLK36 confers broad resistance to maize rough dwarf disease in cereal crops. Nat. Plants 9, 1720–1733 (2023). https://doi.org/10.1038/s41477-023-01514-w
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DOI: https://doi.org/10.1038/s41477-023-01514-w
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