山羊草激酶融合蛋白赋予小麦白粉病抗性-动脉网

A kinase fusion protein from Aegilops longissima confers resistance to wheat powdery mildew

Nature 等信源发布 2024-08-02 15:08

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AbstractMany disease resistance genes have been introgressed into wheat from its wild relatives. However, reduced recombination within the introgressed segments hinders the cloning of the introgressed genes. Here, we have cloned the powdery mildew resistance gene Pm13, which is introgressed into wheat from Aegilops longissima, using a method that combines physical mapping with radiation-induced chromosomal aberrations and transcriptome sequencing analysis of ethyl methanesulfonate (EMS)-induced loss-of-function mutants.

摘要许多抗病基因已从其野生近缘种渗入小麦中。然而，渗入片段内重组的减少阻碍了渗入基因的克隆。在这里，我们使用物理作图与辐射诱导的染色体畸变和甲基磺酸乙酯（EMS）诱导的功能丧失突变体的转录组测序分析相结合的方法，克隆了白粉病抗性基因Pm13，该基因从长山羊草渗入小麦。

Pm13 encodes a kinase fusion protein, designated MLKL-K, with an N-terminal domain of mixed lineage kinase domain-like protein (MLKL_NTD domain) and a C-terminal serine/threonine kinase domain bridged by a brace. The resistance function of Pm13 is validated through transient and stable transgenic complementation assays.

Pm13编码一种激酶融合蛋白，命名为MLKL-K，具有混合谱系激酶结构域样蛋白（MLKL\u NTD结构域）的N端结构域和由支架桥接的C端丝氨酸/苏氨酸激酶结构域。通过瞬时和稳定的转基因互补试验验证了Pm13的抗性功能。

Transient over-expression analyses in Nicotiana benthamiana leaves and wheat protoplasts reveal that the fragment Brace-Kinase122-476 of MLKL-K is capable of inducing cell death, which is dependent on a functional kinase domain and the three α-helices in the brace region close to the N-terminus of the kinase domain..

本塞姆氏烟草叶片和小麦原生质体中的瞬时过表达分析表明，MLKL-K的片段Brace-Kinase122-476能够诱导细胞死亡，这取决于功能性激酶结构域和靠近激酶结构域N端的Brace区域中的三个α-螺旋。。

IntroductionCommon wheat (Triticum aestivum L., 2n = 6x = 42, AABBDD) is a widely grown cereal crop consumed by ~30% of the global population. Wheat production is constantly challenged by various fungal diseases, including rusts, Fusarium head blight, and powdery mildew1. Wheat powdery mildew, a foliar disease, is caused by the obligate biotrophic pathogen Blumeria graminis f.

引言普通小麦（Triticum aestivum L.，2n=6x=42，AABBDD）是一种广泛种植的谷物作物，约占全球人口的30%。小麦生产不断受到各种真菌疾病的挑战，包括锈病，镰刀菌赤霉病和白粉病1。。

sp. tritici (Bgt) and is prevalent across most winter and spring wheat growing areas in the world, leading to significant yield losses2,3,4. Bgt is highly dynamic and co-evolves with wheat crops, which results in rapidly shifts in the virulence patterns of pathogen and ineffectiveness of powdery mildew resistance (Pm) genes used in wheat production5,6.

小麦疫霉菌（Bgt）在世界上大多数冬小麦和春小麦种植区普遍存在，导致显着的产量损失2,3,4。Bgt是高度动态的，与小麦作物共同进化，导致病原体的毒力模式迅速转变，小麦生产中使用的白粉病抗性（Pm）基因无效5,6。

Hence, exploiting and utilizing more effective Pm genes from common wheat and its cultivated or wild relatives are important to control powdery mildew disease7.Aegilops longissima Schweinf. and Muschl. (2n = 2x = 14, SlSl) is a wild species in the Sitopsis section (S genome). It is highly related to the progenitor of the B genome of common wheat8,9.

因此，从普通小麦及其栽培或野生近缘种中开发和利用更有效的Pm基因对于控制白粉病具有重要意义。和马斯克尔。（2n 2x 14，SlSl）是Sitopsis部分（S基因组）的野生物种。它与普通小麦B基因组的祖先高度相关8,9。

This diploid species is resistant to various diseases, such as rusts10, eyespot11, and powdery mildew12. The transfer of powdery mildew resistance from Ae. longissima into common wheat was initiated in the 1980s, leading to the creation of a series of wheat-Ae. longissima chromosome translocation lines12,13,14,15.Pm13 was mapped to the distal part of the short arm of chromosome 3S1, which was transferred from Ae.

这种二倍体物种对各种疾病具有抗性，例如锈病10，眼斑病11和白粉病12。从20世纪80年代开始，将抗白粉病性从长茎赤霉转移到普通小麦中，导致产生了一系列小麦长茎赤霉染色体易位系12,13,14,15.Pm13被定位到染色体3S1短臂的远端，该短臂是从Ae转移而来的。

longissima into wheat chromosome 3BS12. This gene has not been widely used in agriculture despite its highly effective resistance to powdery mildew, which is possibly due to the linkage drag of Pm13 introgression. Efforts have been made to reduce the Ae. longissima chromosomal fragments by promo.

长柄进入小麦染色体3BS12。尽管该基因对白粉病具有高效抗性，但尚未在农业中广泛使用，这可能是由于Pm13基因渗入的连锁阻力所致。已经努力通过promo减少Ae。longissima染色体片段。

Pm13 from Ae. longissima confers resistance to 108 Bgt isolatesNon-denaturing fluorescence in situ hybridization (ND-FISH) was performed to characterize the chromosomal composition of wheat-Ae. longissima line No.3778, which has a pedigree of R1A/Bainong3217*5 that carries the powdery mildew resistance gene Pm13.

。

Stronger signals of the FAM-labeled probe Oligo-pSc119.2 (green) were observed in the terminal regions of the short arm of chromosome 3B (3BS) compared to Chinese Spring (CS). The Tamra-labeled probe Oligo-pTa535 stained red on the rest part of chromosome 3B, which was similar to CS (Fig. 1a). This indicates that wheat line No.

与中国春季（CS）相比，在3B染色体短臂（3BS）的末端区域观察到FAM标记的探针Oligo-pSc119.2（绿色）的更强信号。Tamra标记的探针Oligo-pTa535在3B染色体的其余部分染成红色，与CS相似（图1a）。这表明小麦品系No。

3778 carries a pair of translocated chromosomes 3SlS-3BS.3BL, where the alien segment 3SlS is introgressed onto a distal location of the wheat chromosome arm 3BS. This result is consistent with the previous cytogenetic and molecular evidence13.Fig. 1: Physical mapping of the highly effective Pm13.a Non-denaturing fluorescence in situ hybridization (ND-FISH) patterns of Chinese Spring (left) and line No.

3778携带一对易位染色体3SlS-3BS.3BL，其中外来片段3SlS渗入小麦染色体臂3BS的远端位置。这一结果与之前的细胞遗传学和分子证据一致13。图1：高效Pm13的物理作图。中国春（左）和品系号的非变性荧光原位杂交（ND-FISH）模式。

3778 (right). Chromosomes of Chinese Spring and No. 3778 were stained with 4’,6-diamidino-2-phenylindole (DAPI) (blue), Oligo-pSc119.2 (green), and Oligo-pTa535 (red). Orange arrows indicate the translocated chromosomes 3SlS-3BS.3BL. The experiment was independently repeated three times with consistent results.

3778（右）。用4'，6-二脒基-2-苯基吲哚（DAPI）（蓝色），Oligo-pSc119.2（绿色）和Oligo-pTa535（红色）染色中国春和3778号的染色体。橙色箭头表示易位的染色体3SlS-3BS.3BL。实验独立重复三次，结果一致。

Scale bar = 10 μm. b Representative images showing phenotypic effects of Pm13 against 8 out of 108 tested Bgt isolates. Line No. 3778 carrying Pm13, YM18 carrying Pm21, and Chancellor (CC) without any Pm gene were inoculated with the indicated isolates. Leaves are shown sequentially from left to right.

比例尺=10微米。b代表性图像显示Pm13对108个测试的Bgt分离株中的8个的表型效应。用指定的分离株接种携带Pm13的3778号品系，携带Pm21的YM18和没有任何Pm基因的总理（CC）。叶子从左到右依次显示。

c Representative images showing powdery mildew symptoms on susceptible γ-ray irradiation-induced M3 mutants (IT4), the resistant pa.

c代表性图像显示易感γ射线照射诱导的M3突变体（IT4）（抗性pa）上的白粉病症状。

MLKL-K is sufficient for powdery mildew resistanceBiolistic bombardment-based single-cell transient over-expression of MLKL-K CDS in the epidermal cells of susceptible wheat cv. XM44 significantly reduced the haustorium index (36.8%) of Bgt isolate E09 infection compared to the empty vector as the negative control (67.5%), while over-expressing of the positive control Pm21 resulted in a haustorium index (33.7%) comparable to MLKL-K (Fig. 2d, Supplementary Data 8).

MLKL-K足以抵抗白粉病。与空载体相比，敏感小麦品种XM44的表皮细胞中MLKL-K CD的基于基因枪法的单细胞瞬时过表达显着降低了Bgt分离株E09感染的吸器指数（36.8%）作为阴性对照（67.5%），而阳性对照Pm21的过表达导致吸器指数（33.7%）与MLKL-K相当（图2d，补充数据8）。

Subsequently, the construct containing the MLKL-K CDS under the control of its native promoter (2637 bp) and native terminator (1932 bp) (Fig. 2c) was transformed into the susceptible wheat cv. Fielder via the Agrobacterium-mediated transformation. Seven independent MLKL-K-positive transgenic T0 plants, verified by the diagnostic marker XMLKL-K, showed an immune reaction when inoculated with isolate BgtYZ01, while non-transgenic Fielder plants were susceptible (Fig. 2e, Supplementary Fig. 6).

随后，通过农杆菌介导的转化，将在其天然启动子（2637bp）和天然终止子（1932bp）控制下含有MLKL-K CDS的构建体（图2c）转化到易感小麦品种Fielder中。通过诊断标记XMLKL-K验证的七个独立的MLKL-K阳性转基因T0植物在接种分离物BgtYZ01时显示出免疫反应，而非转基因Fielder植物是敏感的（图2e，补充图6）。

The derived seven T1 families displayed a resistance/susceptibility segregation when challenged by BgtYZ01. Molecular analysis using marker XMLKL-K revealed that the presence of the transgene was associated with the resistant phenotype, and the absence of transgene was associated with the susceptible phenotype (Fig. 2f).

当受到BgtYZ01的挑战时，衍生的七个T1家族表现出抗性/易感性分离。使用标记XMLKL-K进行的分子分析表明，转基因的存在与抗性表型有关，而转基因的缺失与易感表型有关（图2f）。

Furthermore, all marker-positive T1 plants from T1-line 1 and T1-line 2 were resistant to 20 tested Bgt isolates (Supplementary Fig. 7). The expression of MLKL-K in seven T1 plants was also confirmed by qPCR (Supplementary Fig. 8). Collectively, these results demonstrate that the candidate gene MLKL-K is sufficient for the resistance to wheat powdery mildew and is the causal gene of the Pm13 locus.Truncated MLKL-K is capable of inducing cell deathT1 transgenic plants expressing MLKL-K were grown until the.

此外，来自T1品系1和T1品系2的所有标记阳性T1植物对20个测试的Bgt分离株具有抗性（补充图7）。通过qPCR也证实了MLKL-K在七种T1植物中的表达（补充图8）。总的来说，这些结果表明候选基因MLKL-K足以抵抗小麦白粉病，并且是Pm13基因座的致病基因。截短的MLKL-K能够诱导细胞死亡表达MLKL-K的T1转基因植物生长直至。

Data availability

数据可用性

Data supporting the findings of this work are available within the paper and its Supplementary Information files. Datasets generated and analyzed during the current study are available from the corresponding author upon request. RNA-Seq data from the Bgt-infected leaves of the WT line No. 3778 and its mutants can be found in the European Nucleotide Archive (ENA) under the accession number PRJEB63085.

本文及其补充信息文件中提供了支持这项工作结果的数据。在当前研究期间生成和分析的数据集可应要求从通讯作者处获得。来自WT品系3778及其突变体的Bgt感染叶片的RNA-Seq数据可以在欧洲核苷酸档案（ENA）中找到，登录号为PRJEB63085。

The transcriptome assembly of the WT line No. 3778 was deposited in the ENA under the accession number HCEC01000000. The sequence of Pm13 from wheat line No. 3778 and its alleles from Ae. longissima accessions were deposited in the Genbank of NCBI under the accession numbers OR052510-[OR052527]. The transcriptome assembly of the WT line No.

WT品系3778的转录组组装体以登录号HCEC01000000保藏在ENA中。来自小麦品系3778的Pm13序列及其来自长柄Ae的等位基因以登录号OR052510-[OR052527]保藏在NCBI的Genbank中。WT行号的转录组组装。

3778, sequences of the transcript NODE_25350 and the CDS, and the genomic sequence of Pm13 are also available on the DRYAD database [https://doi.org/10.5061/dryad.qjq2bvqmz]. Source data are provided with this paper..

3778，转录本NODE\u 25350和CDS的序列，以及Pm13的基因组序列也可以在DRYAD数据库中找到[https://doi.org/10.5061/dryad.qjq2bvqmz]。本文提供了源数据。。

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Download referencesAcknowledgementsThis study was supported by grants from National Key R&D Program of China (2022YFF1001500/2022YFF1001503 to Q.S.), National Natural Science Foundation of China (32171990 to H.H., 32172001 to H.L. and 32372507 to S.G.), Natural Science Foundation of Jiangsu Province (BK20231321 to H.H.) and State Key Laboratory of Plant Cell and Chromosome Engineering (PCCE-KF-2021-05 to H.H.

下载参考文献致谢本研究得到了国家重点研发计划（2022YFF1001500/2022YFF1001503至Q.S.），国家自然科学基金（32171990至H.H.，32172001至H.L.和32372507至S.G.），江苏省自然科学基金（BK2031321至H.H.）和植物细胞与染色体工程国家重点实验室（PCCE-KF-2021-05至H.H.）的资助。

and PCCE-KF-2022-07 to S.Z.), King Abdullah University of Science and Technology (to S.G.K.) and Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (start-up funding to Y.W.). The authors thank Dr. Genying Li of Crop Research Institution, Shandong Academy of Agricultural Sciences, Jinan, China for providing the binary vector pLGY03.Author informationAuthor notesThese authors contributed equally: Huagang He, Zhaozhao Chen.Authors and AffiliationsSchool of Life Sciences, Jiangsu University, Zhenjiang, ChinaHuagang He, Zhaozhao Chen, Jiale Wang & Qianyuan ZhangState Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, ChinaRenchun Fan, Yanan Li, Yitong Zhao & Qian-Hua ShenInstitute of Biotechnology and Nuclear Technology Research, Sichuan Academy of Agricultural Sciences, Chengdu, ChinaJie ZhangSchool of Environment and Safety Engineering, Jiangsu University, Zhenjiang, ChinaShanying ZhuSchool of Life Sciences, Henan University, Kaifeng, ChinaAnli GaoInstitute of Plant Protection and Soil Science, Hubei Academy of Agricultural Sciences, Wuhan, ChinaShuangjun GongKey Laboratory of Plant Design, National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, I.

和S.Z.的PCCE-KF-2022-07），阿卜杜拉国王科技大学（S.G.K.）和中国科学院分子植物科学卓越中心（Y.W.的启动资金）。作者感谢山东省农业科学院作物研究所李根英博士提供的二元载体pLGY03。作者信息作者注意到这些作者做出了同样的贡献：何华刚，陈兆钊。作者及所属单位江苏大学生命科学学院，镇江，中国贺华刚，陈兆钊，王家乐，张千元，中国科学院种子设计创新研究院遗传与发育生物学研究所植物细胞与染色体工程国家重点实验室，北京，中国任春凡，李亚南，赵一彤，沈千华四川省农业科学院生物技术与核技术研究所，成都，江苏大学环境与安全工程学院，镇江，河南大学生命科学学院，开封，中国安利湖北省农业科学院植物保护与土壤科学研究所，武汉，中国双植物设计重点实验室，植物分子遗传学国家重点实验室，分子植物科学卓越中心，I。

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PubMed Google ScholarContributionsH.H., S.G.K., and Y.W. conceived and designed the research. H.H., Z.C., R.F., J.Z., S.Z., J.W., Q.Z., A.G., S.G., L.Z., Y.L. and Y.Z. performed experiments. H.H., Y.W., Z.C. and Q.S analyzed the data. H.H. and Y.W. wrote the manuscript with input from H.L.

PubMed谷歌学术贡献。H、，S.G.K.和Y.W.构思并设计了这项研究。H、 H.，Z.C.，R.F.，J.Z.，S.Z.，J.W.，Q.Z.，A.G.，S.G.，L.Z.，Y.L.和Y.Z.进行了实验。H、 H.，Y.W.，Z.C.和Q.S分析了数据。H、 H.和Y.W.在H.L.的输入下撰写了手稿。

and S.G.K. H.H. and Z.C. contributed equally to this work.Corresponding authorsCorrespondence to.

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Reprints and permissionsAbout this articleCite this articleHe, H., Chen, Z., Fan, R. et al. A kinase fusion protein from Aegilops longissima confers resistance to wheat powdery mildew.

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Nat Commun 15, 6512 (2024). https://doi.org/10.1038/s41467-024-50909-6Download citationReceived: 12 June 2023Accepted: 25 July 2024Published: 02 August 2024DOI: https://doi.org/10.1038/s41467-024-50909-6Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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