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Journal of Integrative Agriculture  2024, Vol. 23 Issue (9): 3045-3054    DOI: 10.1016/j.jia.2024.05.020
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Cytospora pyri promotes Erwinia amylovora virulence by providing metabolites and hyphae

Tong Shen1, 2, Mengdi Ye3, Yeping Xu1, 2, Bohan Ding1, 2, Hongtao Li1, 2, Li Zhang3, Jun Wang3, Yanli Tian1, 2, 4, Baishi Hu1, 2, 4, 5#, Youfu Zhao6

1 College of Plant Protection/Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Nanjing 210095, China

2 Key Laboratory of Plant Quarantine Pests Monitoring and Control, Ministry of Agriculture and Rural Affairs, Nanjing 210095, China

3 Plant Protection and Quarantine Station of Xinjiang Uygur Autonomous Region, Urumqi 830001, China

4 Xinjiang Key Laboratory of Agricultural Biosafety, Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences, Urumqi 830013, China

5 College of Agriculture, Xinjiang Agricultural University, Urumqi 830052, China

6 Plant Pathology Department, Washington State University, Prosser, WA 24106, USA

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摘要  
细菌-真菌互作广泛存在于自然界中。先前已有许多关于植物病原细菌与病原真菌互作的研究,但对梨树病原细菌与病原真菌的互作研究却鲜有报道。本团队在新疆库尔勒香梨园内发现梨腐烂病发生严重的梨园内常伴随梨火疫病的出现。然而这两种病原物在侵染梨树期间的关系尚不清楚。因此,本研究目的在于明确梨火疫病菌(Erwinia amylovora)与梨腐烂病菌(Cytospora pyri)之间是否存在互作以及探究其潜在的协同致病机制。本研究首先对采集到的梨树样品进行病原物检测,计算两种病原物的田间共存率;随后对E. amylovoraC. pyri进行了室内离体接种,观测病害的发生情况;最后通过对生长、物理互作、毒力因子产生及毒力因子编码基因表达的监测,解析E. amylovoraC. pyri互作的分子机制。结果表明,E. amylovoraC. pyri可在同一病斑中共存,且在离体梨树组织上同时接种两种病原菌可加重病害的发生。同时发现,C. pyri虽不影响E. amylovora的生长,却可以促进E. amylovora的扩散及毒力因子梨火疫毒素的产生。本研究结果表明,E. amylovoraC. pyri在侵染梨树期间存在协同致病作用,C. pyri可通过菌丝和代谢产物促进E. amylovora的扩散并提高致病力,从而加重病害的发生。本文是对梨树病原物E. amylovoraC. pyri互作研究的首次报道,开展梨树病原细菌与病原真菌的协同致病研究,对明确病原物的侵染机制,保证新疆梨产业平稳健康发展具有重要意义。


Abstract  
Bacterial–fungal interactions are widespread in nature.  We observed that pear orchards affected by Cytospora pyri (formerly Valsa pyri) were often accompanied with Erwinia amylovora.  However, the relationship of the two pathogens was unclear.  The objective of this study was to determine whether the synergistic effect exists between Eamylovora and Cpyri.  We first analyzed the coexistence frequencies of Eamylovora and Cpyri in pear trees.  Virulence of the two pathogens, growth, physical interactions, amylovoran production, and expression of genes for amylovoran biosynthesis were conducted.  Our results showed that Eamylovora and Cpyri could coexist on the same lesion and caused much more severe disease.  We also found that Eamylovora could physically attach to Cpyri and the expression of amylovoran biosynthesis genes were up-regulated with fungal metabolite treatment.  These results indicate that Eamylovora and Cpyri can cooperatively interact, which provides Cpyri with an opportunity to promote bacterial dispersal and production of virulence factor in Eamylovora.


Keywords:  pear fire blight       Erwinia amylovora       Valsa canker       amylovoran       synergy  
Received: 30 November 2023   Accepted: 17 April 2024
Fund: 
This work was supported by the Major Science and Technology Projects in Xinjiang, China (2023A02006).

About author:  Tong Shen, E-mail: 18331519385@163.com; #Correspondence Baishi Hu, Tel/Fax: +86-25-84395240, E-mail: hbs@njau.edu.cn

Cite this article: 

Tong Shen, Mengdi Ye, Yeping Xu, Bohan Ding, Hongtao Li, Li Zhang, Jun Wang, Yanli Tian, Baishi Hu, Youfu Zhao. 2024. Cytospora pyri promotes Erwinia amylovora virulence by providing metabolites and hyphae. Journal of Integrative Agriculture, 23(9): 3045-3054.

Bellemann P, Bereswill S, Berger S, Geider K. 1994. Visualization of capsule formation by Erwinia amylovora and assays to determine amylovoran synthesis. International Journal of Biological Macromolecules16, 290–296.

Bellemann P, Geider K. 1992. Localization of transposon insertions in pathogenicity mutants of Erwinia amylovora and their biochemical characterization. Journal of General Microbiology138, 931–940.

Bereswill S, Pahl A, Bellemann P, Zeller W, Geider K. 1992. Sensitive and species-specific detection of Erwinia amylovora by polymerase chain reaction analysis. Applied Environmental Microbiology58, 3522–3528.

Bernhard F, Poetter K, Geider K, Coplin D L. 1990. The rcsA gene from Erwinia amylovora: Identification, nucleotide sequence, and regulation of exopolysaccharide biosynthesis. Molecular Plant (Microbe Interactions), 3, 429–437.

Boer W, Folman L B, Summerbell R C, Boddy L. 2005. Living in a fungal world: Impact of fungi on soil bacterial niche development. FEMS Microbiology Reviews29, 795–811.

Bugert P, Geider K. 1995. Molecular analysis of the ams operon required for exopolysaccharide synthesis of Erwinia amylovoraMolecular Microbiology15, 917–933.

Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A. 2011. Bacterial-fungal interactions: Hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiology and Molecular Biology Reviews75, 583–609.

Geider K. 2000. Exopolysaccarides of Erwinia amylovora: Structure, biosynthesis, regulation, role in pathogenicity of amylovoran and levan. In: Vanneste J L, ed., Fire Blightthe Disease & Its Causative Agent Erwinia amylovora. Commonwealth Agricultural Bureaux International, Wallingford, UK. pp. 117–140.

Geier G , Geider K. 1993. Characterization and influence on virulence of the levansucrase gene from the fireblight pathogen Erwinia amylovoraPhysiological and Molecular Plant Pathology42, 387–404.

Hogan D A, Kolter R. 2002. Pseudomonas-Candida interactions: An ecological role for virulence factors. Science296, 2229–2232.

Hu B S, Xu Z G. 1999. Present distribution, dissemination and progress in detection of Erwinia amylovoraPlant Quarantine3, 7–11. (in Chinese)

Jock S, Donat V, López M M, Bazzi C, Geider K. 2002. Following spread of fire blight in Western, Central and Southern Europe by molecular differentiation of Erwinia amylovora strains with PFGE analysis. Environmental Microbiology4, 106–114.

Jung B, Park J, Kim N, Li T Y, Kim S, Bartley L E, Kim J, Kim I, Kang Y, Yun K, Choi Y, Lee H H, Ji S, Lee K S, Kim B Y, Shon J C, Kim W C, Liu K H, Yoon D, Kim S, et al. 2018. Cooperative interactions between seed-borne bacterial and air-borne fungal pathogens on rice. Nature Communications9, 31.

Koczan J M, Lenneman B R, McGrath M J, Sundin G W. 2011. Cell surface attachment structures contribute to biofilm formation and xylem colonization by Erwinia amylovoraApplied and Environmental Microbiology77, 7031–7039.

Koczan J M, McGrath M J, Zhao Y F, Sundin G W. 2009. Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: Implications in pathogenicity. Phytopathology99, 1237–1244.

Kohlmeier S, Smits T H, Ford R M, Keel C, Harms H, Wick L Y. 2005. Taking the fungal highway: Mobilization of pollutant-degrading bacteria by fungi. Environmental Science & Technology39, 4640–4646.

Liu J, Tian Y L, Zhao Y Q, Zeng R, Chen B H, Hu B S, Walcott R R. 2019. Ferric uptake regulator (FurA) is required for Acidovorax citrulli virulence on watermelon. Phytopathology109, 1997–2008.

Liu L. 2022. Study on relationship between fire blight and Valsa canker of Korla pear. MSc thesis, Xinjiang Agricultural University, China. (in Chinese)

Myung I S, Lee J Y, Yun M J, Lee Y H, Lee Y K, Park D H, Oh C S. 2016. Fire blight of apple, caused by Erwinia amylovora, a new disease in Korea. Plant Disease100, 1774.

Norelli J L, Holleran H T, Johnson W C, Robinson T L, Aldwinckle H S. 2003. Resistance of Geneva and other apple rootstocks to Erwinia amylovoraPlant Disease87, 26–32.

Oh C S, Beer S V. 2005. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiology Letters253, 185–192.

Ordax M, Marco-Noales E, López M M, Biosca E G. 2010. Exopolysaccharides favor the survival of Erwinia amylovora under copper stress through different strategies. Research Microbiology161, 549–555.

Rainey P B. 1991. Phenotypic variation of Pseudomonas putida and Ptolaasii affects attachment to Agaricus bisporus mycelium. Journal of General Microbiology137, 2769–2779.

Sjulin T M, Beer S V. 1978. Mechanism of wilt induction by amylovoran in cotoneaster shoots and its relation to wilting of shoots infected by Erwinia amylovoraPhytopathology68, 89–94.

Stopnisek N, Zühlke D, Carlier A, Barberán A, Fierer N, Becher D, Riedel K, Eberl L, Weisskopf L. 2016. Molecular mechanisms underlying the close association between soil Burkholderia and fungi. ISME Journal10, 253–264.

Sun X L, Xu Z H, Xie J Y, Hesselberg-Thomsen V, Tan T M, Zheng D Y, Strube M L, Dragoš A, Shen Q R, Zhang R F, Kovács Á T. 2021. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME Journal16, 774–787.

Tarkka M T, Sarniguet A, Frey-Klett P. 2009. Inter-kingdom encounters: Recent advances in molecular bacterium-fungus interactions. Current Genetics55, 233–243.

Vrancken K, Holtappels M, Schoofs H, Deckers T, Valcke R. 2013. Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: State of the art. Microbiology159, 823–832.

Wang D P, Korban S S, Pusey P L, Zhao Y F. 2012a. AmyR is a novel negative regulator of amylovoran production in Erwinia amylovoraPLoS ONE7, e45038.

Wang D P, Korban S S, Zhao Y F. 2009. The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovoraMolecular Plant Pathology10, 277–290.

Wang D P, Qi M S, Calla B, Korban S S, Clough S J, Cock P J A, Sundin G W, Toth I, Zhao Y F. 2012b. Genome-wide identification of genes regulated by the Rcs phosphorelay system in Erwinia amylovoraMolecular Plant (Microbe Interactions), 25, 6–17.

Wang J, Gao J C, Bayinkexike, Muyassar M, Zhang J H, Tian Y L, Hu B S. 2022. Blocking field spread of fire blight by electric heating automatic disinfection pruning scissors. Plant Quarantine36, 25–28. (in Chinese)

Wang X L, Kang Z S, Huang L L, Yang P. 2007. Pathogen identification of Valsa canker on pear tree: Evidences from rDNA-ITS sequences and cultural characteristics. Mycosystema26, 517–527. (in Chinese)

Wang Z. 2023. Pathogen population composition of fragrant pear Valsa Canker and transcriptome analysis of dominant species Cytospora pyri. Ph D thesis, Tarim University, China. (in Chinese)

Warmink J A, van Elsas J D. 2009. Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms. Applied and Environmental Microbiology75, 2820–2830.

Wen C Y, Xu M, Zhang J, Nie K, Zhang J. 2023. Seven ectomycorrhizal fungi: Determination of the growth curve characteristics. Chinese Agricultural Science Bulletin39, 35–41. (in Chinese)

Zhang F, Li Y Y. 2020. Present situation and countermeasures of pear industry in Korla. Northwest Horticulture11, 3–5. (in Chinese)

Zhang H. 2016. Conidium occurrence and canker sopt expansion of pear valsa canker and its mix-fungicides screening. MSc thesis, Anhui Agricultural University, China. (in Chinese)

Zhang M X, Zhai L F, Zhou Y X, Chen X R, Jia N N, Hong N, Wang G P. 2013. Laboratory determining methods of the pathogenicity of Valsa canker in pear. Journal of Fruit Science30, 317–322, 333. (in Chinese)

Zhao Y F, Qi M S. 2011. Comparative genomics of Erwinia amylovora and related Erwinia species-what do we learn? Genes-Basel2, 627–639.

Zhao Y F, Sundin G W, Wang D P. 2009a. Construction and analysis of pathogenicity island deletion mutants of Erwinia amylovoraCanadian Journal of Microbiology55, 457–464.

Zhao Y F, Wang D P, Nakka S, Sundin G W, Korban S S. 2009b. Systems level analysis of two-component signal transduction systems in Erwinia amylovora: Role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics10, 245.

Zwet T V D. 2006. Present worldwide distribution of fire blight and closely related diseases. Acta Horticulturae704, 35–36.

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