Pathogenicity and comparative genomic analysis of Mycobacterium avium subsp. paratuberculosis strains isolated from China: novel insights into virulence differentiation

doi:10.1016/j.jia.2025.06.002

Advanced Online Publication | Current Issue | Archive | Adv Search

Pathogenicity and comparative genomic analysis of Mycobacterium avium subsp. paratuberculosis strains isolated from China: novel insights into virulence differentiation

Guanghui Dang¹^*, Ping Lu¹^*, Zhuming Cai¹, Yingying Cui¹, Xinxin Zang¹, Fagang Zhong², Xin Huang²^#, Huajun Zheng³^#, Siguo Liu¹^#

¹State Key Laboratory for Animal Disease Control and Prevention, Division of Bacterial Diseases, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin 150069, China

²State Key Laboratory of Genetic Improvement and Healthy Breeding of Sheep, Xinjiang Academy of Agricultural and Reclamation Sciences, Shihezi 832000, China

³Shanghai-MOST Key Laboratory of Health and Disease Genomics/NHC Key Lab of Reproduction Regulation, Shanghai Institute for Biomedical and Pharmaceutical Technologies, Shanghai 200237, China

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

副结核病（Paratuberculosis，pTB）是由副结核分枝杆菌（Mycobacterium avium subsp. paratuberculosis, MAP）引发的反刍动物（如牛、羊）慢性消耗性疫病，以顽固性腹泻、进行性消瘦及肠黏膜结节性增生为主要临床特征。该病原体在全球中呈现持续性传播态势，严重危害牛羊畜牧业的可持续发展。并且MAP与人类克罗恩病（Crohn’s disease）存在某种潜在的联系，加之其在乳制品供应链中的存活扩散特性，已构成重大公共卫生威胁。2005年，Li L等研究者首次完成了从美国奶牛群分离的MAP K-10菌株的全基因组解析工作，成功绘制了该病原体的完整基因图谱。在此基础上，全球科研团队陆续破译了不同宿主来源MAP分离株的全基因组序列，这些高质量基因组数据的积累为深入探究MAP毒力表型变异机制提供了分子层面的理论依据。值得注意的是，尽管我国多个省份均有MAP感染的流行病学报道，但迄今为止尚未见针对本土流行菌株开展系统性全基因组测序研究的报道。本研究从中国的内蒙、辽宁、黑龙江和新疆四省的牛羊中分离获得6株MAP分离株，分别命名为NM10，LN219，HLJ37，HLJ160，XJ41和XJ121。通过对六株MAP分离菌株的全基因组测序和泛基因组分析，结果显示：六株MAP分离菌株间具有高度的基因组亲缘性，然而，LN219和NM10菌株在其特有基因组中分别携带两个和三个超毒力因子（不与MHC分子结合的毒力因子），而其余四株分离菌株各仅含有一个超毒力因子；AlphaFold预测表明，相较于其他四株MAP分离菌株及MAP K-10参考菌株，LN219和NM10分离菌株的anti-anti-σ因子中发现有九个氨基酸缺失，导致其anti-anti-σ因子与anti-σ因子复合体的结合亲和力降低。以上因子可能部分解释了中国流行MAP菌株间的毒力差异。此外，MAP表型分析与体内小鼠感染实验证实，LN219和NM10分离菌株的致病性（体重、脏器菌落定殖和脏器病理损伤）和毒力均显著高于其他四株MAP分离菌株。因此，通过进一步研究鉴定出MAP中与关键疾病表型相关的基因，能够针对这些基因开展靶向功能实验，从而为pTB的有效防控提供理论技术支撑。

Abstract

Mycobacterium avium subsp. paratuberculosis (MAP) causes paratuberculosis (pTB) in ruminants and may be linked to Crohn's disease in humans. Despite extensive MAP genomic data from various animals worldwide, there is a significant lack of such data and understanding of MAP pathogenicity in China. This study used whole-genome sequencing (WGS) and pathogenicity analysis in mice to examine virulence differences among six MAP field strains (designated NM10, LN219, HLJ37, HLJ160, XJ41, and XJ121) isolated from cattle and sheep in various regions of China affected by pTB. The WGS and pan-genome analysis revealed close genomic relatedness among the six MAP strains. However, strains LN219 and NM10 exhibited two and three hypervirulence factors, respectively, while the other four isolated strains each contained only one hypervirulence factor within their specific genomes. Moreover, AlphaFold predictions indicated that the nine amino acid deletions identified in the anti-anti-σ factor of strains LN219 and NM10 led to the lowest binding affinity in the anti-anti-σ factor_anti-σ factor complexes, relative to the other four Chinese strains and the K-10 strain. In addition, bacterial phenotype analyses and in vivo animal experiments have shown that the pathogenicity and virulence of the LN219 and NM10 strains were significantly elevated compared to the other four isolated strains. These factors may partially account for the differences in virulence observed among MAP strains circulating in China. Furthermore, identifying the genes in this bacterium that are associated with critical disease phenotypes can enable targeted functional experiments on these genes, thereby improving control strategies for pTB.

Keywords: Mycobacterium avium subsp. paratuberculosis whole-genome sequencing anti-anti-σ factor virulence pathogenicity

Online: 02 June 2025

Fund: This study was supported by the National Key Research and Development Program of China (2023YFD1801302, 2021YFD1800403), the National Natural Science Foundation of China (32273005), and the Central Public-interest Scientific Institution Basal Research Fund (1610302024002).

About author: #Correspondence Xin Huang, E-mail: ahx512@163.com; Huajun Zheng, E-mail: zhenghj@chgc.sh.cn; Siguo Liu, E-mail: liusiguo@caas.cn *These authors contributed equally

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Guanghui Dang, Ping Lu, Zhuming Cai, Yingying Cui, Xinxin Zang, Fagang Zhong, Xin Huang#, Huajun Zheng, Siguo Liu. 2025. Pathogenicity and comparative genomic analysis of Mycobacterium avium subsp. paratuberculosis strains isolated from China: novel insights into virulence differentiation. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.06.002

Amin A S, Hsu C Y, Darwish S F, Ghosh P, Abdel-Fatah E M, Behour T S, Talaat A M. 2015. Ecology and genomic features of infection with Mycobacterium avium subspecies paratuberculosis in Egypt. Microbiology (Reading), 161, 807-818.

Barkema H W, Orsel K, Nielsen S S, Koets A P, Rutten V, Bannantine J P, Keefe G P, Kelton D F, Wells S J, Whittington R J, Mackintosh C G, Manning E J, Weber M F, Heuer C, Forde T L, Ritter C, Roche S, Corbett C S, Wolf R, Griebel P J, et al. 2018. Knowledge gaps that hamper prevention and control of Mycobacterium avium subspecies paratuberculosis infection. Transboundary and emerging diseases, 65, 125-148.

Beard P M, Daniels M J, Henderson D, Pirie A, Rudge K, Buxton D, Rhind S, Greig A, Hutchings M R, Mckendrick I, Stevenson K, Sharp J M. 2001. Paratuberculosis infection of nonruminant wildlife in Scotland. Journal of clinical microbiology, 39, 1517-1521.

Beaucher J, Rodrigue S, Jacques P E, Smith I, Brzezinski R, Gaudreau L. 2002. Novel Mycobacterium tuberculosis anti-sigma factor antagonists control sigmaF activity by distinct mechanisms. Molecular Microbiology, 45, 1527-1540.

Capella-Gutierrez S, Silla-Martinez J M, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972-1973.

Chan P P, Lin B Y, Mak A J, Lowe T M. 2021. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic acids research, 49, 9077-9096.

Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Molecular plant, 13, 1194-1202.

Chen Y, Hou L, Khalid A K, Robertson I D, Zhao Y, Chen X, Guo A. 2024. Individual- and Herd-Level Milk ELISA Test Status and Incidence for Paratuberculosis in Hubei Province, China. Veterinary sciences, 11,

Clarke C J. 1997. The pathology and pathogenesis of paratuberculosis in ruminants and other species. Journal of comparative pathology, 116, 217-261.

Collins D M, De Zoete M, Cavaignac S M. 2002. Mycobacterium avium subsp. paratuberculosis strains from cattle and sheep can be distinguished by a PCR test based on a novel DNA sequence difference. Journal of clinical microbiology, 40, 4760-4762.

Coutsias E A, Seok C, Dill K A. 2004. Using quaternions to calculate RMSD. Journal of computational chemistry, 25, 1849-1857.

Danecek P, Bonfield J K, Liddle J, Marshall J, Ohan V, Pollard M O, Whitwham A, Keane T, Mccarthy S A, Davies R M, Li H. 2021. Twelve years of SAMtools and BCFtools. Gigascience, 10, giab008.

Darling A C, Mau B, Blattner F R, Perna N T. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome research, 14, 1394-1403.

Delcher A L, Bratke K A, Powers E C, Salzberg S L. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics, 23, 673-679.

Fostier C R, Monlezun L, Ousalem F, Singh S, Hunt J F, Boel G. 2021. ABC-F translation factors: from antibiotic resistance to immune response. FEBS letters, 595, 675-706.

Gardy J L, Laird M R, Chen F, Rey S, Walsh C J, Ester M, Brinkman F S. 2005. PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics, 21, 617-623.

Ghosh P, Hsu C, Alyamani E J, Shehata M M, Al-Dubaib M A, Al-Naeem A, Hashad M, Mahmoud O M, Alharbi K B, Al-Busadah K, Al-Swailem A M, Talaat A M. 2012. Genome-wide analysis of the emerging infection with Mycobacterium avium subspecies paratuberculosis in the Arabian camels (Camelus dromedarius). PLoS One, 7, e31947.

Glickman M S, Cox J S, Jacobs W R, Jr. 2000. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Molecular Cell, 5, 717-727.

Hassan N M, Alhossary A A, Mu Y, Kwoh C K. 2017. Protein-Ligand Blind Docking Using QuickVina-W With Inter-Process Spatio-Temporal Integration. Scientific reports, 7, 15451.

Hedin W, Froberg G, Fredman K, Chryssanthou E, Selmeryd I, Gillman A, Orsini L, Runold M, Jonsson B, Schon T, Davies Forsman L. 2023. A Rough Colony Morphology of Mycobacterium abscessus Is Associated With Cavitary Pulmonary Disease and Poor Clinical Outcome. The Journal of infectious diseases, 227, 820-827.

Kalyaanamoorthy S, Minh B Q, Wong T K F, Von Haeseler A, Jermiin L S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature methods, 14, 587-589.

Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution, 30, 772-780.

Kishita Y, Sugiura A, Onuki T, Ebihara T, Matsuhashi T, Shimura M, Fushimi T, Ichino N, Nagatakidani Y, Nishihata H, Nitta K R, Yatsuka Y, Imai-Okazaki A, Wu Y, Osaka H, Ohtake A, Murayama K, Okazaki Y. 2023. Strategic validation of variants of uncertain significance in ECHS1 genetic testing. Journal of medical genetics, 60, 1006-1015.

Kuriata A, Gierut A M, Oleniecki T, Ciemny M P, Kolinski A, Kurcinski M, Kmiecik S. 2018. CABS-flex 2.0: a web server for fast simulations of flexibility of protein structures. Nucleic acids research, 46, W338-W343.

Lagesen K, Hallin P, Rodland E A, Staerfeldt H H, Rognes T, Ussery D W. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic acids research, 35, 3100-3108.

Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature methods, 9, 357-359.

Li L, Bannantine J P, Zhang Q, Amonsin A, May B J, Alt D, Banerji N, Kanjilal S, Kapur V. 2005. The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proceedings of the National Academy of Sciences of the United States of America, 102, 12344-12349.

Lu N, Niu Y L, Song Y, Zhang D D, Jiang J, Wei J, Geng H L, Cao H. 2023. Prevalence of paratuberculosis in cattle in China: A systematic review and meta-analysis. Preventive veterinary medicine, 220, 106043.

Ma J G, Tian A L, Zheng W B, Zou Y, Zhang Y T, Yang Z Q. 2019. First report of bovine viral diarrhea virus and Mycobacterium avium subspecies paratuberculosis infection in Tibetan sheep (Ovis aries) in Tibetan Plateau, China. Tropical animal health and production, 51, 719-722.

Makinoshima H, Glickman M S. 2005. Regulation of Mycobacterium tuberculosis cell envelope composition and virulence by intramembrane proteolysis. Nature, 436, 406-409.

Matsumoto S, Furugen M, Yukitake H, Yamada T. 2000. The gene encoding mycobacterial DNA-binding protein I (MDPI) transformed rapidly growing bacteria to slowly growing bacteria. FEMS microbiology letters, 182, 297-301.

Mohammed T, Mamo G, Zewude A, Sirak A, Gumi B, Ameni G. 2023. Prevalence of paratuberculosis in cattle based on gross and microscopic lesions in Ethiopia. BMC veterinary research, 19, 203.

Nguyen L T, Schmidt H A, Von Haeseler A, Minh B Q. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular biology and evolution, 32, 268-274.

Ott S L, Wells S J, Wagner B A. 1999. Herd-level economic losses associated with Johne's disease on US dairy operations. Preventive veterinary medicine, 40, 179-192.

Ottardi M, Lechner I, Wang J, Schmitt S, Schneeberger M, Schmid R M, Stephan R, Meylan M. 2024. Seroprevalence of Mycobacterium avium subsp. paratuberculosis in Swiss dairy herds and risk factors for a positive herd status and within-herd prevalence. Frontiers in veterinary science, 11, 1409694.

Ousalem F, Singh S, Chesneau O, Hunt J F, Boel G. 2019. ABC-F proteins in mRNA translation and antibiotic resistance. Research in microbiology, 170, 435-447.

Pettersen E F, Goddard T D, Huang C C, Couch G S, Greenblatt D M, Meng E C, Ferrin T E. 2004. UCSF Chimera--a visualization system for exploratory research and analysis. Journal of computational chemistry, 25, 1605-1612.

Pettersen E F, Goddard T D, Huang C C, Meng E C, Couch G S, Croll T I, Morris J H, Ferrin T E. 2021. UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein science, 30, 70-82.

Rasmussen P, Barkema H W, Mason S, Beaulieu E, Hall D C. 2021. Economic losses due to Johne's disease (paratuberculosis) in dairy cattle. Journal of dairy science, 104, 3123-3143.

Richards V P, Nigsch A, Pavinski Bitar P, Sun Q, Stuber T, Ceres K, Smith R L, Robbe Austerman S, Schukken Y, Grohn Y T, Stanhope M J. 2021. Evolutionary genomic and bacteria GWAS analysis of Mycobacterium avium subsp. paratuberculosis and dairy cattle Johne's disease phenotypes. Applied and environmental microbiology, 87,

Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic acids research, 42, W320-324.

Serraino A, Bonilauri P, Giacometti F, Ricchi M, Cammi G, Piva S, Zambrini V, Canever A, Arrigoni N. 2017. Short communication: Investigation into Mycobacterium avium ssp. paratuberculosis in pasteurized milk in Italy. Journal of dairy science, 100, 118-123.

Shao M, Cui N, Tang Y, Chen F, Cui Y, Dang G, Liu S. 2023. A candidate subunit vaccine induces protective immunity against Mycobacterium avium subspecies paratuberculosis in mice. NPJ Vaccines, 8, 72.

Shin S J, Lee B S, Koh W J, Manning E J, Anklam K, Sreevatsan S, Lambrecht R S, Collins M T. 2010. Efficient differentiation of Mycobacterium avium complex species and subspecies by use of five-target multiplex PCR. Journal of clinical microbiology, 48, 4057-4062.

Sinha D, Chakraborty T, Sinha D, Poddar A, Chattopadhyaya R, Sau S. 2021. Understanding the structure, stability, and anti-sigma factor-binding thermodynamics of an anti-anti-sigma factor from Staphylococcus aureus. Journal of Biomolecular Structure & Dynamics, 39, 6539-6552.

Skolnick J, Gao M, Zhou H, Singh S. 2021. AlphaFold 2: Why It Works and Its Implications for Understanding the Relationships of Protein Sequence, Structure, and Function. Journal of chemical information and modeling, 61, 4827-4831.

Song W, Sun H X, Zhang C, Cheng L, Peng Y, Deng Z, Wang D, Wang Y, Hu M, Liu W, Yang H, Shen Y, Li J, You L, Xiao M. 2019. Prophage Hunter: an integrative hunting tool for active prophages. Nucleic acids research, 47, W74-W80.

Stabel J R. 1997. An improved method for cultivation of Mycobacterium paratuberculosis from bovine fecal samples and comparison to three other methods. Journal of veterinary diagnostic investigation, 9, 375-380.

Sun W W, Lv W F, Cong W, Meng Q F, Wang C F, Shan X F, Qian A D. 2015. Mycobacterium avium Subspecies paratuberculosis and Bovine Leukemia Virus Seroprevalence and Associated Risk Factors in Commercial Dairy and Beef Cattle in Northern and Northeastern China. BioMed research international, 2015, 315173.

Wade M, Li Y C, Wahl G M. 2013. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nature reviews Cancer, 13, 83-96.

Wang H, Yang Z, Swingle B, Kvitko B H. 2021. AlgU, a Conserved Sigma Factor Regulating Abiotic Stress Tolerance and Promoting Virulence in Pseudomonas syringae. Molecular plant-microbe interactions, 34, 326-336.

Wayne L G, Sohaskey C D. 2001. Nonreplicating persistence of mycobacterium tuberculosis. Annual review of microbiology, 55, 139-163.

Wynne J W, Bull T J, Seemann T, Bulach D M, Wagner J, Kirkwood C D, Michalski W P. 2011. Exploring the zoonotic potential of Mycobacterium avium subspecies paratuberculosis through comparative genomics. PLoS One, 6, e22171.

Yue R, Liu C, Barrow P, Liu F, Cui Y, Yang L, Zhao D, Zhou X. 2016. The isolation and molecular characterization of Mycobacterium avium subsp. paratuberculosis in Shandong province, China. Gut pathogens, 8, 9.

Zare Y, Shook G E, Collins M T, Kirkpatrick B W. 2014. Genome-wide association analysis and genomic prediction of Mycobacterium avium subspecies paratuberculosis infection in US Jersey cattle. PLoS One, 9, e88380.

Zhang D, Gao F, Jakovlic I, Zou H, Zhang J, Li W X, Wang G T. 2020. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular ecology resources, 20, 348-355.

Zhao L, Wang Y, Wang J L, Zhao W H, Cheng H X, Ma Y M, Chai H L, Zhang Z S, Wang L F, Miao Z Q, Ding Y L, Sulijid J, Dang G H, Liu S Y, Wang F L, Liu S G, Liu Y H. 2021. Serological investigation and genotyping of Mycobacterium avium subsp. paratuberculosis in sheep and goats in Inner Mongolia, China. PLoS One, 16, e0256628.

Zhao Y, Wu J, Yang J, Sun S, Xiao J, Yu J. 2012. PGAP: pan-genomes analysis pipeline. Bioinformatics, 28, 416-418.

Zhu X, Lu Q, Li Y, Long Q, Zhang X, Long X, Cao D. 2023. Contraction and expansion dynamics: deciphering genomic underpinnings of growth rate and pathogenicity in Mycobacterium. Frontiers in microbiology, 14, 1292897.

[1]	YUAN Li-fang, JIANG Hang, LIU Qi-bao, JIANG Xi-long, WEI Yan-feng, YIN Xiang-tian, LI Ting-gang. Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis[J]. >Journal of Integrative Agriculture, 2025, 24(7): 0-.
[2]	Shulin Zhang, Yu Wang, Jinmei Hu, Xinyue Cui, Xiaoru Kang, Wei Zhao, Yuemin Pan. The N-mannosyltransferase MoAlg9 plays important roles in the development and pathogenicity of Magnaporthe oryzae[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2266-2284.
[3]	Zhizhou Xu, Guichun Wu, Bo Wang, Baodian Guo, Cong Sheng, Yangyang Zhao, Bao Tang, Yancun Zhao, Fengquan Liu. Sigma factor 70 RpoD contributes to virulence by regulating cell motility, oxidative stress tolerance, and manipulating the expression of hrpG and hrpX in Xanthomonas oryzae pv. oryzae[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1844-1859.
[4]	Wenrui Fan, Yuntong Chen, Mengmeng Yu, Yongzhen Liu, Yulong Gao. Advances on ALV-J in China over the past two decades[J]. >Journal of Integrative Agriculture, 2025, 24(2): 429-440.
[5]	Wenqin Fang, Yonghe Hong, Tengsheng Zhou, Yangdou Wei, Lili Lin, Zonghua Wang, Xiaohan Zhu. Uncoupling of nutrient metabolism and cellular redox by cytosolic routing of the mitochondrial G-3-P dehydrogenase Gpd2 causes loss of conidiation and pathogenicity in Pyricularia oryzae[J]. >Journal of Integrative Agriculture, 2025, 24(2): 638-654.
[6]	Gaosong Liu, Xuelian Lü, Qiufeng Tian, Wanjiang Zhang, Fei Yi, Yueling Zhang, Shenye Yu. *Deletion of Salmonella* pathogenicity islands SPI-1, 2 and 3 induces substantial morphological and metabolic alternation and protective immune potential**[J]. >Journal of Integrative Agriculture, 2025, 24(1): 272-289.
[7]	Haiyang Li, Yuan Zhang, Cancan Qin, Zhifang Wang, Lingjun Hao, Panpan Zhang, Yongqiang Yuan, Chaopu Ding, Mengxuan Wang, Feifei Zan, Jiaxing Meng, Xunyu Zhuang, Zheran Liu, Limin Wang, Haifeng Zhou, Linlin Chen, Min Wang, Xiaoping Xing, Hongxia Yuan, Honglian Li, Shengli Ding. Identification and characterization of FpRco1 in regulating vegetative growth and pathogenicity based on T-DNA insertion in Fusarium pseudograminearum[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3055-3065.
[8]	Libin Liang, Yaning Bai, Wenyan Huang, Pengfei Ren, Xing Li, Dou Wang, Yuhan Yang, Zhen Gao, Jiao Tang, Xingchen Wu, Shimin Gao, Yanna Guo, Mingming Hu, Zhiwei Wang, Zhongbing Wang, Haili Ma, Junping Li. Genetic and biological properties of H9N2 avian influenza viruses isolated in central China from 2020 to 2022[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2778-2791.
[9]	Xiaojie Xu, Shaoyan Jiang, Chunju Liu, Xujie Sun, Qing Zhu, Xiuzhai Chen, Pengchao Jiang, Fenglong Wang, Yanping Tian, Xiangdong Li. Development of a stable attenuated double-mutant of tobacco mosaic virus for cross-protection[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2318-2331.
[10]	Yuhan Yang, Dou Wang, Yaning Bai, Wenyan Huang, Shimin Gao, Xingchen Wu, Ying Wang, Jianle Ren, Jinxin He, Lin Jin, Mingming Hu, Zhiwei Wang, Zhongbing Wang, Haili Ma, Junping Li, Libin Liang. Genetic and pathogenic characterization of new infectious bronchitis virus strains in the GVI-1 and GI-19 lineages isolated in central China[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2407-2420.
[11]	Yue Jiang, Rong Wang, Lili Du, Xueyu Wang, Xi Zhang, Pengfei Qi, Qianfei Wu, Baoyi Peng, Zonghua Wang, Mo Wang, Ya Li. The DNA damage repair complex MoMMS21–MoSMC5 is required for infection-related development and pathogenicity of Magnaporthe oryzae [J]. >Journal of Integrative Agriculture, 2024, 23(6): 1956-1966.
[12]	Linlin Chen, Yixuan Shan, Zaifang Dong, Yake Zhang, Mengya Peng, Hongxia Yuan, Yan Shi, Honglian Li, Xiaoping Xing. A potential hyphal fusion protein complex with an important role in development and virulence interacts with autophagy-related proteins in Fusarium pseudograminearum[J]. >Journal of Integrative Agriculture, 2024, 23(12): 4093-4106.
[13]	Yina Xu, Hailing Li, Haoyu Leng, Chaofan Su, Siqi Tang, Yongtao Wang, Shiwei Zhang, Yali Feng, Yanan Wu, Daxin Wang, Ying Zhang. Genetic and biological properties of H10Nx influenza viruses in China[J]. >Journal of Integrative Agriculture, 2024, 23(11): 3860-3869.
[14]	Chengdong Yang, Manfei Luo, Xue Zhang, Linlin Ye, Ge Yu, Yi Lü, Yi Chen, Taixu Chen, Xuejian Wang, Wanzhen Feng, Qinghe Chen. Autophagy-related protein PlAtg3 participates in vegetative growth, sporangial cleavage, autophagy and pathogenicity of Peronophythora litchii[J]. >Journal of Integrative Agriculture, 2024, 23(11): 3788-3800.
[15]	Dong Deng, Wenqi Wu, Canxing Duan, Suli Sun, Zhendong Zhu. *A novel pathogen Fusarium* cuneirostrum causing common bean (Phaseolus vulgaris) root rot in China** [J]. >Journal of Integrative Agriculture, 2024, 23(1): 166-176.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors