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Establishment of a system for screening and identification of novel bactericide targets in the plant pathogenic bacterium xanthomonas oryzae pv. oryzae using Tn-seq and SPR

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Journal of Integrative Agriculture 2024年第5期23卷 1580-1592页

作者： Chaoyue Pang Ling Jin Haoyu Zang Damalk Saint-Claire SKoklannou Jiazhi Sun Jiawei Yang Yongxing Wang Liang Xu Chunyan Gu Yang Sun Xing Chen Yu Chen School of Plant Protection Anhui Agricultural UniversityHefei 230036China Institute of Plant Protection and Agro-Products Safety Anhui Academy of Agricultural SciencesHefei 230031China Anhui Province Laboratory for Green Pesticide Development and Application School of Plant ProtectionAnhui Agricultural UniversityHefei230036China Hefei Research Center State Key Laboratory for Biology of Plant Diseases and Insect PestsHefei 230036China Key Laboratory of Integrated Crop Pest Management of Anhui Province School of Plant ProtectionAnhui Agricultural University Hefei230036China Shandong Vicome Greenland Chemical Co. Ltd.Jinan 250204China

xanthomonas spp. cause severe bacterial diseases. However, effective strategies for prevention and management of these diseases are scarce. Thus, it is necessary to improve the efficiency of control of diseases caused by xanthomonas. In this study, xanthomonas oryzae pv. oryzae(Xoo), which causes rice bacterial leaf blight, has been studied as a representative. A transposon insertion library of Xoo, comprising approximately 200,000 individual insertion mutants, was generated. Transposon sequencing data indicated that the mariner C9 transposase mapped at 35.7–36.4% of all potential insertion sites, revealing 491 essential genes required for the growth of Xoo in rich media. The results show that, compared to the functions of essential genes of other bacteria, the functions of some essential genes of Xoo are unknown, 25 genes might be dangerous for the xanthomonas group, and 3 are specific to xanthomonas. High-priority candidates for developing broad-spectrum, xanthomonas-specific, and environment-friendly bactericides were identified in this study. In addition, this study revealed the possible targets of dioctyldiethylenetriamine using surface plasmon resonance(SPR) in combination with high performance liquid chromatography–mass spectrometry(HPLC–MS). The study also provided references for the research of some certain bactericides with unknown anti-bacterial mode of action. In conclusion, this study urged a better understanding of xanthomonas,provided meaningful data for the management of bacterial leaf blight, and disclosed selected targets of a novel bactericide.

关键词： rice bacterial leaf blight xanthomonas essential genes Tn-seq dioctyldiethylenetriamine

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The xanthomonas typeⅢeffector Xop AP prevents stomatal closure by interfering with vacuolar acidification

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Journal of Integrative Plant Biology 2022年第10期64卷 1994-2008页

作者： Longyu Liu Ying Li Zhengyin Xu Huan Chen Jingyi Zhang Brittany Manion Fengquan Liu Lifang Zou Zheng Qing Fu Gongyou Chen State Key Laboratory of Microbial Metabolism/Shanghai Collaborative Innovation Center of Agri‐Seeds School of Agriculture and BiologyShanghai Jiao Tong UniversityShanghai 200240China Department of Biological Sciences University of South CarolinaColumbia 29208USA Institute of Plant Protection Jiangsu Academy of Agricultural SciencesNanjing 210014China

Plant stomata close rapidly in response to a rise in the plant hormone abscisic acid(ABA)or salicylic acid(SA)and after recognition of pathogenassociated molecular patterns(PAMPs).Stomatal closure is the result of vacuolar convolution,ion efflux,and changes in turgor pressure in guard cells.Phytopathogenic bacteria secrete typeⅢeffectors(T3Es)that interfere with plant defense mechanisms,causing severe plant disease symptoms.Here,we show that the virulence and infection of xanthomonas oryzae pv.oryzicola(Xoc),which is the causal agent of rice bacterial leaf streak disease,drastically increased in transgenic rice(Oryza sativa L.)plants overexpressing the Xoc T3E gene Xop AP,which encodes a protein annotated as a lipase.We discovered that Xop AP binds to phosphatidylinositol 3,5-bisphosphate(Ptd Ins(3,5)P_(2)),a memb rane phospholipid that functions in p H control in lysosomes,membrane dynamics,and protein trafficking.Xop AP inhibited the acidification of vacuoles by competing with vacuolar H^(+)-pyrophosphatase(V-PPase)for binding to Ptd Ins(3,5)P_(2),leading to stomatal opening.Transgenic rice overexpressing Xop AP also showed inhibition of stomatal closure when challenged by Xoc infection and treatment with the PAMP flg22.Moreover,Xop AP suppressed flg22-induced gene expression,reactive oxygen species burst and callose deposition in host plants,demonstrating that Xop AP subverts PAMP-triggered immunity during Xoc infection.Taken together,these findings demonstrate that Xop AP overcomes stomatal immunity in plants by binding to lipids.

关键词： Ptd Ins(3 5)P2 stomatal closure typeⅢeffector vacuole acidification xanthomonas Xop AP

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The genetic arms race between plant and xanthomonas:lessons learned from TALE biology

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Science China(Life Sciences) 2021年第1期64卷 51-65页

作者： Jiao Xue Zhanhua Lu Wei Liu Shiguang Wang Dongbai Lu Xiaofei Wang Xiuying He Rice Research Institute Guangdong Academy of Agricultural SciencesGuangdong Provincial Key Laboratory of New Technology in Rice BreedingGuangzhou510640China

The pathogenic bacterial genus xanthomonas infects a wide variety of host plants and causes devastating diseases in many crops.Transcription activator-like effectors(TALEs)are important virulence factors secreted by xanthomonas with the ability to directly bind to the promoters of target genes in plant hosts and activate their expression,which often facilitates the proliferation of pathogens.Understanding how plants cope with TALEs will provide mechanistic insights into crop breeding for xanthomonas defense.Over the past 30 years,numerous studies have revealed the modes of action of TALEs in plant cells and plant defense strategies to overcome TALE attack.Based on these findings,new technologies were adopted for disease management to optimize crop production.In this article,we will review the most recent advances in the evolutionary arms race between plant resistance and TALEs from xanthomonas,with a specific focus on TALE applications in the development of novel breeding strategies for durable and broad-spectrum resistance.

关键词： transcription activator-like effectors xanthomonas susceptibility genes resistance genes TALE application

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Designer TAL Effectors Induce Disease Susceptibility and Resistance to xanthomonas oryzae pv. Oryzae in Rice

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Molecular Plant 2013年第3期6卷 781-789页

作者： Ting Li Sheng Huang Junhui Zhou Bing Yang Department of Genetics Development and Cell Biology Iowa State University Ames IA 50011 USA Present address: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources College of Life Science and Technology Guangxi University Nanning Guangxi 530005 China

TAL （transcription activator-like） effectors from xanthomonas bacteria activate the cognate host genes, leading to disease susceptibility or resistance dependent on the genetic context of host target genes. The modular nature and DNA recognition code of TAL effectors enable custom-engineering of designer TAL effectors （dTALE） for gene activation. However, the feasibility of dTALEs as transcription activators for gene functional analysis has not been demonstrated. Here, we report the use of dTALEs, as expressed and delivered by the pathogenic xanthomonas oryzae pv. oryzae （Xoo）, in revealing the new function of two previously identified disease-related genes and the potential of one developmental gene for disease susceptibility in rice/Xoo interactions. The dTALE gene dTALE-xa27, designed to target the susceptible allele of the resistance gene Xa27, elicited a resistant reaction in the otherwise susceptible rice cultivar IR24. Four dTALE genes were made to induce the four annotated Xa27 homologous genes in rice cultivar Nipponbare, but none of the four induced Xa27-1ike genes conferred resistance to the dTALE-containing Xoo strains. A dTALE gene was also generated to activate the recessive resistance gene xa13, an allele of the disease-susceptibility gene Os8N3 （also named Xa13 or OsSWEETll, a member of sucrose efflux transporter SWEET gene family）. The induction of xa13 by the dTALE rendered the resistant rice IRBB13 （xa13/xa13） susceptible to Xoo. Finally, OsSWEET12, an as-yet uncharacterized SWEET gene with no corresponding naturally occurring TAL effector identified, conferred susceptibility to the Xoo strains expressing the corresponding dTALE genes. Our results demonstrate that dTALEs can be delivered through the bacterial secretion system to activate genes of interest for functional analysis in plants.

关键词： TA/effector rice xanthomonas Xa27 disease susceptibility disease resistance designer TAL effector.

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Citron C-05 inhibits both the penetration and colonization of xanthomonas citri subsp.citri to achieve resistance to citrus canker disease

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Horticulture Research 2020年第1期7卷 1981-1992页

作者： Hongyan Fu Mingming Zhao Jing Xu Limei Tan Jian Han Dazhi Li Meijun Wang Shunyuan Xiao Xianfeng Ma Ziniu Deng College of Horticulture Hunan Agricultural University410128 ChangshaHunanChina National Center for Citrus Improvement 410128 ChangshaHunanChina Hunan Horticultural Research Institute 410125 ChangshaHunanChina Institute for Bioscience and Biotechnology Research&Department of Plant Sciences and Landscape Architecture University of Maryland College ParkRockvilleMD 20850USA

Citrus canker,caused by xanthomonas citri subsp.citri(Xcc),is a serious bacterial disease that affects citrus production worldwide.Citron C-05(Citrus medica)is the only germplasm in the Citrus genus that has been identified to exhibit strong resistance to Xcc.However,it has not been determined when,where,and how Xcc is restricted in the tissues of Citron C-05 during the infection process.In the present study,we investigated the spatiotemporal growth dynamics of an eGFP-labeled virulent Xcc(eGFP-Xcc)strain in Citron C-05 along with five susceptible biotypes(i.e.,lemon,pummelo,sour orange,sweet orange,and ponkan mandarin)upon inoculation via the spraying or leaf infiltration of a bacterial suspension.The results from extensive confocal laser scanning microscopy analyses showed that while Xcc grew rapidly in plants of all five susceptible genotypes,Xcc was severely restricted in the epidermal and mesophyll cell layers of the leaves of Citron C-05 in the early stage of infection.Not surprisingly,resistance against Xcc in Citron C-05 was found to be associated with the production of reactive oxygen species and hypersensitive response-like cell death,as well as greater upregulation of several defense-related genes,including a pathogenesis-related gene(PR1)and a glutathione S-transferase gene(GST1),compared with sweet orange as a susceptible control.Taken together,our results not only provide further valuable details of the spatiotemporal dynamics of the host entry,propagation,and spread of Xcc in both resistant and susceptible citrus plants but also suggest that resistance to Xcc in Citron C-05 may be attributed to the activation of multiple defense mechanisms.

关键词： citrus xanthomonas resistance

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Diversity and interaction of common bacterial blight disease-causing bacteria(xanthomonas spp.) with Phaseolus vulgaris L.

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The Crop Journal 2019年第1期7卷 1-7页

作者： Joab K.Tugume Geoffrey Tusiime Allan Male Sekamate Robin Buruchara Clare Mugisha Mukankusi Makerere University Department of Agricultural Production International Centre for Tropical Agriculture (CIAT)/Pan African Bean Research Alliance (PABRA)

Common bacterial blight(CBB) is associated with common bean(Phaseolus vulgaris L.), an important grain legume for human consumption worldwide. The disease, caused by xanthomonas spp. is spread mainly through seed. This paper focuses on the diversity of X.axonopodis pv. phaseoli and X. fuscans subsp. fuscans and interactions between related bacteria and the bean host. Review has suggested that the diversity and taxonomic studies of these pathogens are not exhaustive, especially in areas where detailed molecular analysis has not been conducted and previous characterizations were based on phenotypic features and PCR-based techniques. Also, no study has confirmed differential pathogenicity on bean genotypes based on compatible versus incompatible reactions. However, isolates react differently to wild and domesticated bean sources of resistance in common bean genetic backgrounds. A systematic approach will be required to investigate global changes in gene expression among different sources of resistance in a common bean background.The bacterial isolates that cause CBB should be functionally characterized using genotypes containing major quantitative trait loci(QTL) for CBB resistance. These studies will increase understanding of resistance and how it is manipulated by pathogens.

关键词： xanthomonas axonopodis Interaction Gene expression Diversity

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Action modes of transcription activator-like effectors(TALEs) of xanthomonas in plants

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Journal of Integrative Agriculture 2017年第12期16卷 2736-2745页

作者： XU Zheng-yin ZOU Li-fang MA Wen-xiu CAI Lu-lu YANG Yang-yang CHEN Gong-you School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism Shanghai Jiao Tong University Shanghai200240 P.R.China

Plant-pathogenic xanthomonas infects a wide variety of host plants and causes many devastating diseases on crops. Transcription activator-like effectors（TALEs） are delivered by a type III secretion system（T3 SS） of xanthomonas into plant nuclei to directly bind specific DNA sequences（TAL effector-binding elements, EBEs） on either strand of host target genes with an unique modular DNA-binding domain and to bidirectionally drive host gene transcription. The target genes in plants consist of host susceptibility（S） genes promoting disease（ETS） and resistance（R） genes triggering defense（ETI）. Here we generally summarized the discovery of TALEs in xanthomonas species, their functions in bacterial pathogenicity in plants and their target genes in different host plants, and then focused on the newly revealed modes of protein action in triggering or suppressing plant defense.

关键词： xanthomonas TALE iTALE ETS ETI suppressor

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An improved protein expression system for T3SS genes regulation analysis in xanthomonas oryzae pv. oryzae

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Journal of Integrative Agriculture 2019年第6期18卷 1189-1198页

作者： XU Jin-bo ZHANG Cui-ping WUNIERBIEKE Mei-li YANG Xiao-fei LI Yi-lang CHEN Xiao-bin CHEN Gong-you ZOU Li-fang Department of Environment and Resource School of Agriculture and BiologyShanghai Jiao Tong University

xanthomonas oryzea pv.oryzae(Xoo)is the causal agent of bacterial blight of rice,which is a significant threat to many of rice-growing regions.The type Ⅲ secretion system(T3SS)is an essential virulence factor in Xoo.Expression of the T3SS is often induced in the host environment or in hrp-inducing medium but is repressed in nutrient-rich medium.The elucidation of molecular mechanism underlying induction of T3SS genes expression is a very important step to lift the veil on global virulence regulation network in Xoo.Thus,an efficient and reliable genetic tool system is required for detection of the T3SS proteins.In this study,we constructed a protein expression vector pH3-flag based on the backbone of pHM1,a most widely used vector in Xoo strains,especially a model strain PXO99A.This vector contains a synthesized MCS-FLAG cassette that consists of a multiple cloning site(MCS),containing a modified pUC18 polylinker,and Flag as a C-terminal tag.The cassette is flanked by transcriptional terminators to eliminate interference of external transcription enabling detection of accurate protein expression.We evaluated the potential of this expression vector as T3SS proteins detection system and demonstrated it is applicable in the study of T3SS genes expression regulation in Xoo.This improved expression system could be very effectively used as a molecular tool in understanding some virulence genes expression and regulation in Xoo and other xanthomonas spp.

关键词： xanthomonas oryzae pv.oryzae broad-host range vector expression vector T3SS genes

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Evolution of xanthomonas Gene Content:Gene Gain/Loss History and Species Divergence

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Journal of Integrative Agriculture 2012年第6期11卷 954-961页

作者： JIN Gu-lei ZHANG Guo-qing XIE Guan-lin ZHU Jun LOU Miao-miao ZHOU Xue-ping ZHANGXiao-wei SUN Guo-chang LI Bin ZHU Bo State Key Laboratory of Rice Biology and Key Laboratory of Molecular Biology of Crop Pathogens and Insects Ministry of Agriculture/ Institute of Biotechnology Zhejiang University Hangzhou 310029 P.R.China Institute of Bioinformatics Zhejiang University Hangzhou 310029 P.R.China Crop Management Station Jiaxing 314051 P.R.China State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control/Institute of Plant Protection and Microbiology Zhejiang Academy of Agricultural Sciences Hangzhou 310021 P.R.China

Horizontal gene transfer （HGT） plays key roles in the evolution of pathogenetic bacteria, especially in pathogenetic associated genes. In this study, the evolutionary dynamics of xanthomonas at species level were determined by the comparative analysis of the complete genomes of 15 xanthomonas strains. A concatenated multiprotein phyletic pattern and a dataset with xanthomonas clusters of orthologous genes were constructed. Mathematical extrapolation estimates that the core genome will reach a minimum of about 1 547 genes while the pan-genome will increase up to 22 624 genes when sequencing 1 000 genomes. The HGT extent in this genus was assessed by using a Markov-based probabilistic method. The reconstructed gene gain/loss history, which contained several features consistent with biological observations, showed that nearly 60% of the xanthomonas genes were acquired by HGT. A large fraction of variability was in the clade ancestor nodes and ＂leaves of the tree＂. Coexpression analysis suggested that the pathogenic and metabolic variation between xanthomonas oryzae pv. oryzicola and xanthomonas oryzae pv. oryzae might due to recently-transferred genes. Our results strongly supported that the gene gain/loss may play an important role in divergence and pathogenicity variation of xanthomonas species.

关键词： xanthomonas core and pan-genome gene gain/loss horizontal gene transfer

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HrcQ is necessary for xanthomonas oryzae pv. oryzae HR-induction in non-host tobacco and pathogenicity in host rice

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The Crop Journal 2013年第2期1卷 143-150页

作者： Xiaoping Zhang Chunlian Wang Chongke Zheng Jinying Che Yanqiang Li Kaijun Zhao National Key Facility for Crop Gene Resources and Genetic Improvement (NFCRI) Key Laboratory of Crop Genetics and BreedingMinistry of Agriculture/Institute of Crop ScienceChinese Academy of Agriculture Sciences

Bacterial blight, caused by xanthomonas oryzae pv. oryzae(Xoo), is one of the most destructive diseases of rice(Oryza sativa L.) worldwide. The type III secretion system(T3SS) of Xoo, encoded by the hrp(hypersensitive response and pathogenicity) genes, plays critical roles in conferring pathogenicity in host rice and triggering a hypersensitive response(HR) in non-host plants. To investigate the major genes conferring the pathogenicity and avirulence of Xoo, we previously constructed a random Tn5-insertion mutant library of Xoo strain PXO99A. We report here the isolation and characterization of a Tn5-insertion mutant PXM69. Tn5-insertion mutants were screened on indica rice JG30, which is highly susceptible to PXO99A, by leaf-cutting inoculation.Four mutants with reduced virulence were obtained after two rounds of screening. Among them, the mutant PXM69 had completely lost virulence to the rice host and ability to elicit HR in non-host tobacco. Southern blotting analysis showed a single copy of a Tn5-insertion in the genome of PXM69. PCR walking and sequencing analysis revealed that the Tn5 transposon was inserted at nucleotide position 70,192–70,201 in the genome of PXO99A, disrupting the type III hrc(hrp-conserved) gene hrcQ, the first gene in the D operon of the hrp cluster in Xoo. To confirm the relationship between the Tn5-insertion and the avirulence phenotype of PXM69, we used the marker exchange mutagenesis to create a PXO99Amutant, ΔhrcQ::KAN, in which the hrcQ was disrupted by a kanamycin-encoding gene cassette at the same site as that of the Tn5-insertion. ΔhrcQ::KAN showed the same phenotype as mutant PXM69. Reintroduction of the wild-type hrcQ gene partially complemented the pathogenic function of PXM69. RT-PCR and cellulase secretion assays showed that the Tn5-disruption of hrcQ did not affect transcription of downstream genes in the D operon and function of the type II secretion system. Our results provide new insights into the pathogenic functions of clustered hrp genes in Xoo.

关键词： xanthomonas oryzae pv.oryzae Tn5-insertion mutant Type III secretion system Pathogenicity

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