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Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight

Abstract

Head or ear blight, mainly caused by Fusarium species, can devastate almost all staple cereal crops (particularly wheat), resulting in great economic loss and imposing health threats on both human beings and livestock1,2,3. However, achievement in breeding for highly resistant cultivars is still not satisfactory. Here, we isolated the major-effect wheat quantitative trait locus, Qfhs.njau-3B, which confers head blight resistance, and showed that it is the same as the previously designated Fhb1. Fhb1 results from a rare deletion involving the 3′ exon of the histidine-rich calcium-binding-protein gene on chromosome 3BS. Both wheat and Arabidopsis transformed with the Fhb1 sequence showed enhanced resistance to Fusarium graminearum spread. The translation products of this gene’s homologs among plants are well conserved and might be essential for plant growth and development. Fhb1 could be useful not only for curbing Fusarium head blight in grain crops but also for improving other plants vulnerable to Fusarium species.

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Fig. 1: Cloning of Qfhs.njau-3B
Fig. 2: His structure and expression and His subcellular localization.
Fig. 3: Transgenic validation of HisR conferring resistance to F. graminearum in wheat.

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Data availability

DNA sequence data that support the findings of this study have been deposited in GenBank (NCBI) under accession numbers KX022627.1KX022633.1, MK397611MK397761 and included in the Supplementary Information. RNA-Seq data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We thank S. Cai and H. Chen of the Jiangsu Academy of Agricultural Sciences, L. Li of the Chinese Academy of Agricultural Sciences, Y. Zhou, D. Liu and J. Wang of Sichuan Agricultural University, H. Wang and J. Tian of Shandong Agricultural University, B. Gill of Kansas State University, C. Chu of the Chinese Academy of Sciences, and many other colleagues, for providing materials for this study. We also thank L. Yan of Oklahoma State University for inspiring discussions and support, and all of the laboratory members not listed as authors for planting and phenotyping. This work was partially supported by grants from the Ministry of Science and Technology of China (2016YFD0101004, 2016YFD0101802, 2012ZX08009003, 2012CB125902, 2009ZX08009-049B, 2004CB117205 and 2002AA224161), innovation team program for Jiangsu universities (2014), ‘111’ project (B08025), Priority Academic Program Development of Jiangsu, Fundamental Research Funds for the Central Universities and Jiangsu collaborative innovation initiative for modern crop production. Special thanks to the National Natural Science Foundation of China for long-term funding support (30025030, 30430440, 30721140555, 31030054, 30671295 and 31501306).

Author information

Authors and Affiliations

Authors

Contributions

Z.M. designed the project. G.L., J.Z., H.J., Z.G., M.F., Y.L., P.Z., S.X., N.L., Y.Y., S.M., Z.K., L.J., X.A., G.J., W.L., W.C., R.Z., J.F., X.X., Y.L., Q.K., S.Z., Y.W., B.Q., S.C., Y.D., J.S., H.Y., X.W. and C.R. performed the experiments. G.L. and J.Z. analyzed the data. G.L. prepared the draft manuscript. H.J. performed investigations and experiment organization. Z.M. reviewed the manuscript.

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Correspondence to Zhengqiang Ma.

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Integrated supplementary information

Supplementary Figure 1 Haplotype analysis using a cultivar population of 151 accessions

. Hap, haplotype; WSB, Wangshuibai; ND2419, Nanda2419; MY, Mianyang99-323; CS, Chinese Spring. The resistance levels are represented by NDS and LDR. a, Haplotypes based on gene-specific markers within the 131.6 kb (Xmag7442-Xmag9452) interval surrounding Qfhs.njau-3B and the corresponding resistance performance. 1, WSB genotype; 0, 2, 3 and 4, other non-WSB genotype. The sample size (n) is shown in column ‘No. of lines’. The P values for two-tailed Student’s t-test for comparison of Hap2 to the others are shown. b, Five haplotypes based on the 3.8-kb His-3B sequence with the main nucleotide variations shown. There are 31 and 33 SNPs and one 3-bp indel in the coding DNA sequence regions of MY and CS haplotypes compared with PH691 haplotype. c, FHB resistance of the haplotypes in b. The sample size (n) for WSB-Hap, PH691-Hap, ND2419-Hap, MY-Hap and CS-Hap is 45, 32, 16, 43 and 15, respectively. The P values for two-tailed Student’s t-test for comparison of WSB-Hap to the others are shown. In a and c, box-and-whisker plots showing the medians (black line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots).

Supplementary Figure 2 PFT and HisR expression levels at flowering stage measured using RNA-seq data

. a, PFT expression in R-43 and PH691 spikes measured with FPKM. Values are represented as the means ± s.d. (n = 3 biologically independent samples). The spikelets at 0, 48 and 96 h after single-floret inoculation with F. graminearum were collected for RNA extraction. 125-bp paired reads were generated with Illumina Hiq2500. The total effective read per sample is at least 7.6 million. P values from two-tailed Student’s t-test of comparison between NIL and PH691 are shown. b, PFT expression in WSB and ND2419 spikes measured with FPKM. The spikelets at 0, 12 and 24 h after inoculation with F. graminearum were collected for RNA extraction. 150-bp paired reads were generated with an Illumina platform HiSeq X Ten System. This experiment has only one biological replicate. The total effective read per sample is at least 20 million for WSB and 22 million for ND2419. c, Expression of WSB HisR and ND2419 His-3B measured with FPKM using the same data as in b.

Supplementary Figure 3 Comparison of the polypeptides deduced from His homoeologs

. a, Three His homoeologs in PH691. b, HisR (from WSB His-3B) and HisS (from PH691 His-3B). In a, similarities are treated as identities.

Supplementary Figure 4 Expression of His homoeologs in PH691 measured with FPKM using the same data as in

Supplementary Figure 2a. Values are represented as the means ± s.d. (n = 3 biologically independent samples).

Supplementary Figure 5 Transgenic validation of HisR-conferring resistance to F. graminearum in wheat

. a, HisR expression levels relative to R-43 in eight T0 transgenic plants produced by transforming ND183 with HisR genomic DNA sequence. Values are represented as the means ± s.d. (n = 3 technical replicates). b, Representative disease symptoms at 20–25 days after inoculation (dai) of the negative control (ND183) and T0 transgenic plants #24, #28 and #52. In a and b, ND183 indicates transgene-negative plants generated in the transformation experiment. c, Scatter plot of areas under the disease progress curve (AUDPC) of transgenic plants and the transgene-negative control based on NDS at 4, 8, 12, 16 and 20 dai. The LDR data yielded a similar result and were not shown. The dashed horizontal lines represent the mean values of the transgenic T0 plants and transgene-negative control. Two-tailed Student’s t-test were performed to examine their statistical difference. Data from spikes of a common plant were indicated with the red bars superimposed on the x-axis and flanked with a vertical line. The numbers under the bars indicate the total spikes of each plant (n) and the number of unsuccessfully inoculated spikes (inside the parentheses).

Supplementary Figure 6 Evaluation of the F1 plants derived from crosses of PH691 with three T0 plants from ND183 transformation with HisR genomic sequence

. a, Representative disease symptom 20 dai of F1 plants derived from crosses of PH691 with T0 plants #38, #40 and #45. (+) and (−), with and without transgene. b, HisR expression level relative to R-43 in the F1 transgenic plants shown in a, (n = 2 biologically independent experiments each with three technical replicates). The transgene was expressed in all the lines although the relative expression values fluctuated. c, AUDPC of the transgene-negative F1 segregants and transgenic (+) F1 segregants from the T0 plants based on NDS and LDR at 4, 8, 12, 16 and 20 dai. The number of inoculated spikes (n) and the P values for two-tailed Dunnett’s test for comparison of the transgenic (+) F1 segregants in each F1 progenies to the transgene-negative F1 segregants are shown. d, NDS and LDR at 20 dai of the transgene-negative F1 segregants and transgenic (+) F1 segregants from the T0 plants. The number of inoculated spikes (n) and the P values for two-tailed Dunnett’s test for comparison of the transgenic (+) F1 segregants in each F1 progenies to the transgene-negative F1 segregants are shown. Similar to the results from F2 analysis in Supplementary Note, NDS and LDR after 16 dai showed moderate correlation with the transgene expression level (P = 0.05). In c and d, box-and-whisker plots showed the medians (orange line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots).

Supplementary Figure 7 Transformation of Yangmai158 with a ubiquitin promoter-driven HisR ORF

. a, Representative disease symptom 20 dai in the T1 progenies of three wheat transformants (#37, #38 and #39) and recipient cultivar Yangmai158 (Y158) inoculated with F. graminearum spores that include a strain carrying the GFP gene. The spike pictures in the bottom panel were merged from continuous photos taken under fluorescent light at 488-nm excitation wavelength using a fluorescence microscope (BX53, OLYMPUS, Japan). b, Expression of the transgenes in the wheat transformants. Experiments were repeated independently three times with similar results. M, DNA size standard in bp. c, Expression of HisR ORF in #37, #38 and #39 compared with expression in the WSB tissues without Fusarium infection (as described in Supplementary Fig. 2b). 150-bp paired reads were generated with an Illumina platform HiSeq X Ten System, (n = 2 biologically independent samples for transgenic plants). The total effective read per sample is at least 29 million. d, NDS of the T1 progenies from the three wheat transformants at 20 dai, with the box-and-whisker plots showing the medians (orange line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots). The number of inoculated spikes (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic segregants to the transgene-negative segregants are shown. In the progenies, the segregants with transgene showed significantly better resistance to FHB than the non-transgenic segregants.

Supplementary Figure 8 RNAi-mediated HisR silencing in NIL R-43

. a, Disease symptoms 15 dai of T0 transgenic plants #1 and #2 and the control R-43. Only one spike was used in inoculation. b, Semiquantitative RT-PCR of His-RNAi in the T0 transformants. M, DNA size standard in bp. The experiments were repeated independently three times with similar results. c, HisR expression levels in the two T0 transgenic plants relative to HisR in R-43 based on quantitative RT-PCR. Values are represented as the means ± s.d. (n = 3 technical replicates). In ac, R43 indicates transgene-negative plants from the transformation experiment. d, Representative disease symptoms 15 dai of the derived T1 transgenic plants expressing the transgenes together with the resistance control R-43 and susceptible control PH691. e, HisR expression levels in the T1 transgenic lines relative to R-43. Values are represented as the means ± s.d. The number of biologically independent samples (n) and the P values for two-tailed Student’s t-test for comparison of HisR expression in the transgenic lines to that in R-43 are shown. f, NDS of the T1 lines. The number of inoculated spikes (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic segregants to the transgene-negative segregants in each progenies are shown. g, Resistance phenotypes 15 dai of four transgenic T1 segregants without obvious HisR silencing. One to three spikes per plant were evaluated. h, Semiquantitative RT-PCR of the His-RNAi construct in the four plants mentioned in g. M, DNA size standard in bp. The experiments were repeated independently three times with similar results. i, HisR expression levels in the four plants mentioned in g relative to HisR expression in R-43, (n = 2 biologically independent experiments, each with three technical replicates). j, Disease symptoms 15 dai of two homozygous T2 transgenic families together with R-43. k, l, NDS (k) and LDR (l) of the two homozygous T2 transgenic families and R-43, with the box-and-whisker plots showing the medians (orange line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots). The number of inoculated spikes (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic plants to R-43 in each family are shown.

Supplementary Figure 9 RNAi-mediated His silencing in the susceptible line PH691

. a, Semiquantitative RT-PCR of His-RNAi in T0 transformants #7, #11 and #13. M, DNA size standard in bp. The experiments were repeated independently three times with similar results. b, His expression level in the three T0 transgenic plants relative to His expression in PH691 based on quantitative RT-PCR, detected with primers for all three His homoeologs. Values are represented as the means ± s.d. (n = 3 technical replicates). c, Disease symptoms 15 dai of the T0 transgenic plants and PH691. Only one spike was used in inoculation. In a-c, PH691 indicates transgene-negative plants from the transformation experiment. d, Disease symptoms 15 dai of PH691 together with the T2 transgenic plants derived from #7 and #11. e, f, NDS (e) and LDR (f) of the T2 transgenic and their transgene-negative siblings, with the box-and-whisker plots showing the medians (orange line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots). The number of inoculated spikes (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic plants to transgene-negative siblings in each family are shown.

Supplementary Figure 10 Rice His ortholog LOC_Os01g03060

. a, Phenotype of the rice His ortholog LOC_Os01g03060 mutant line 05Z11HB69. b, Structure of the mutated gene. c, Expression of the mutated gene. The rice plants were grown in pots with common cultivation practice. Photos in a were taken at the booting stage, showing the wild-type Zhonghua 11 (left pot) and the mutant line (right pot); the enlarged figure shows the necrosis in the upper section of newly grown leaves. The experiments were repeated independently twice with similar results. Black rectangle in b indicates the ORF region, and the triangle points to the T-DNA insertion point. TSS, transcription start site. The relative expression level of LOC_Os01g03060 in c was estimated for the four mutant plants (M1, M2, M10 and M12) relative to wild-type Zhonghua 11 (n = 2 biologically independent experiments, each with three technical replicates).

Supplementary Figure 11 Transformation of Arabidopsis thaliana with the CaMV35S promoter-driven His ORFs

. a, Disease symptoms 4 dai of four Arabidopsis transformants observed under the fluorescent light. RE8 and RE17, plants transformed with the CaMV35S::HisR-EGFP fusion construct; R5, plant transformed with the CaMV35S::HisR construct; S11, plants transformed with the CaMV35S::HisS construct. The photos were taken by fluorescence microscope (BX53, OLYMPUS, Japan) at the 488-nm excitation wavelength. b, HisR expression in RE8, RE17 and R5. c, HisS expression in S11. d, e, Lesion areas (d) and perimeters (e) on the detached rosette leaves at 4 dai from the Arabidopsis transformants and the control Col-0. The number of inoculated leaves (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic plant to Col-0 are shown. The box-and-whisker plots showed the medians (black line), upper and lower quartiles (box edges), 1.5 × interquartile range (whiskers), and outliers (dots). The number of inoculated spikes (n) and the P values for two-tailed Student’s t-test for comparison of the transgenic plants to transgene-negative siblings in each family are shown.

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Li, G., Zhou, J., Jia, H. et al. Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. Nat Genet 51, 1106–1112 (2019). https://doi.org/10.1038/s41588-019-0426-7

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