Preliminary study on the function of Gymnosporangium yamadae effector GyHGSRE1

GAO Xinmei, SHAO Chenxi, LIANG Yingmei, LAO Wenhao

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2025, Vol. 49 ›› Issue (5) : 209-216.

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JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2025, Vol. 49 ›› Issue (5) : 209-216. DOI: 10.12302/j.issn.1000-2006.202312029

Preliminary study on the function of Gymnosporangium yamadae effector GyHGSRE1

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Abstract

【Objective】The study determined the core biological function of the effector protein GyHGSRE1 secreted by the Gymnosporangium yamadae haustoria. This work provides foundational data for elucidating the molecular mechanisms of G. yamadae effector protein.【Method】The haustorial transcriptome of G. yamadae prioritized GyHGSRE1 as a highly expressed effector (FPKM = 117.92). MEME (http://meme-suite.org/) predicted its two-dimensional structure, while Tencent AI (https://drug.ai.tencent.com) generated the three-dimensional model. Real-time PCR quantified GyHGSRE1 expression level during fungal infection. Yeast secretion assays validated the signal peptide’s secretory capacity. Transient expression via Agrobacterium tumefaciens assessed GyHGSRE1 function in Nicotiana benthamiana and apple (Malus domestica) leaves.【Result】GyHGSRE1 contains an N-terminal serine-rich signal peptide. qRT-PCR demonstrated peak expression during haustorium maturation and spore development (pycniosporophores/aeciospores). The protein was localized to plant cell cytoplasm and nuclei, triggering cell death and immune responses in leaf cells of N. benthamiana. Full-length GyHGSRE1 induced cell death in apple leaves, but deletion of the signal peptide attenuated this activity.【Conclusion】The glycine-serine-rich atypical effector GyHGSRE1 exhibits dual localization and cell necrosis-inducing effects across plant species, implying broad-spectrum elicitor potential. Its expression correlates with critical infection stages (host colonization and sporulation). The signal peptide may mediate functional specificity, likely influencing host-pathogen recognition.

Key words

Gymnosporangium yamadae / atypical effector protein / elicitor / signal peptide / plant immunity

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GAO Xinmei , SHAO Chenxi , LIANG Yingmei , et al. Preliminary study on the function of Gymnosporangium yamadae effector GyHGSRE1[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY. 2025, 49(5): 209-216 https://doi.org/10.12302/j.issn.1000-2006.202312029

References

[1]
JONES J D, DANGL J L. The plant immune system[J]. Nature, 2006, 444(7117): 323-329. DOI: 10.1038/nature05286.
[2]
YUAN M H, NGOU B P M, DING P T, et al. PTI-ETI crosstalk: an integrative view of plant immunity[J]. Current Opinion in Plant Biology, 2021, 62: 102030. DOI: 10.1016/j.pbi.2021.102030.
[3]
GARNICA D P, NEMRI A, UPADHYAYA N M, et al. The ins and outs of rust haustoria[J]. PLoS Pathogens, 2014, 10(9): e1004329. DOI: 10.1371/journal.ppat.1004329.
[4]
SAUNDERS D G, WIN J, CANO L M, et al. Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi[J]. PLoS One, 2012, 7(1): e29847. DOI: 10.1371/journal.pone.0029847.
[5]
XU Q, TANG C L, WANG L K, et al. Haustoria-arsenals during the interaction between wheat and Puccinia striiformis f. sp. tritici[J]. Molecular Plant Pathology, 2020, 21(1): 83-94. DOI: 10.1111/mpp.12882.
[6]
CATANZARITI A M, DODDS P N, LAWRENCE G J, et al. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors[J]. Plant Cell, 2006, 18(1): 243-256. DOI: 10.1105/tpc.105.035980.
[7]
刘霞, 陶思齐, 翁涵, 等. 山田胶锈菌和亚洲胶锈菌吸器提取体系建立[J]. 菌物学报, 2019, 38(9): 1430-1439.
LIU X, TAO S Q, WENG H, et al. Construction of haustorial isolation systems of Gymnosporangium yamadae and G. asiaticum[J]. Mycosystema, 2019, 38(9): 1430-1439. DOI: 10.13346/j.mycosystema.190049.
[8]
翁涵, 刘霞, 陶思齐, 等. 山田胶锈菌和亚洲胶锈菌吸器的比较转录组分析[J]. 生物工程学报, 2022, 38(10): 3825-3843.
WENG H, LIU X, TAO S Q, et al. Comparative transcriptomic analysis of the haustoria of Gymnosporangium yamadae and G. asiaticum[J]. Chinese Journal of Biotechnology, 2022, 38(10): 3825-3843. DOI: 10.13345/j.cjb.220379.
[9]
TAO S Q, CAO B, TIAN C M, et al. Comparative transcriptome analysis and identification of candidate effectors in two related rust species (Gymnosporangium yamadae and Gymnosporangium asiaticum)[J]. BMC Genomics, 2017, 18(1): 651. DOI: 10.1186/s12864-017-4059-x.
[10]
TAO S Q, CAO B, MORIN E, et al. Comparative transcriptomics of Gymnosporangium spp. teliospores reveals a conserved genetic program at this specific stage of the rust fungal life cycle[J]. BMC Genomics, 2019, 20(1): 723. DOI: 10.1186/s12864-019-6099-x.
[11]
TAO S Q, AUER L, MORIN E, et al. Transcriptome analysis of apple leaves infected by the rust fungus Gymnosporangium yamadae at two sporulation stages[J]. Molecular Plant-Microbe Interactions, 2020, 33(3): 444-461. DOI: 10.1094/MPMI-07-19-0208-R.
[12]
SHAO C X, LAO W H, LIANG Y M. Reference genes selection of Gymnosporangium yamadae during the interaction with apple leaves[J]. Journal of Fungi, 2022, 8(8): 830. DOI: 10.3390/jof8080830.
[13]
GIETZ R D, SCHIESTL R H, WILLEMS A R, et al. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure[J]. Yeast, 1995, 11(4): 355-360. DOI: 10.1002/yea.320110408.
[14]
赵薇, 许彤骏, 王喻元, 等. 溶藻细菌的筛选及群体感应信号对其活力的调节作用[J]. 生物加工过程, 2023, 21(4):461-470.
ZHAO W, XU T J, WANG Y Y, et al. Screening the algicidal bacteria from phycosphere environment and evaluate their algicidal activity under quorum sensing regulation[J]. Chinese Journal of Bioprocess Engineering, 2023, 21(4):461-470. DOI:10.3969/j.issn.1672-3678.2023.04.010.
[15]
QI T, GUO J, LIU P, et al. Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat[J]. Molecular Plant, 2019, 12(12): 1624-1638. DOI: 10.1016/j.molp.2019.09.010.
[16]
LIU C, WANG Y Q, WANG Y F, et al. Glycine-serine-rich effector PstGSRE4 in Puccinia striiformis f. sp. tritici inhibits the activity of copper zinc superoxide dismutase to modulate immunity in wheat[J]. PLoS Pathogens, 2022, 18(7): e1010702. DOI: 10.1371/journal.ppat.1010702.
[17]
DUPLESSIS S, LORRAIN C, PETRE B, et al. Host adaptation and virulence in heteroecious rust fungi[J]. Annual Review of Phytopathology, 2021, 59: 403-422. DOI: 10.1146/annurev-phyto-020620-121149.
[18]
OWJI H, NEZAFAT N, NEGAHDARIPOUR M, et al. A comprehensive review of signal peptides: structure, roles, and applications[J]. European Journal of Cell Biology, 2018, 97(6): 422-441. DOI: 10.1016/j.ejcb.2018.06.003.
[19]
XU Q, HU S, JIN M X, et al. The N-terminus of a Fusarium graminearum-secreted protein enhances broad-spectrum disease resistance in plants[J]. Molecular Plant Pathology, 2022, 23(12): 1751-1764. DOI: 10.1111/mpp.13262.
[20]
LORRAIN C, PETRE B, DUPLESSIS S. Show me the way: rust effector targets in heterologous plant systems[J]. Current Opinion Microbiology, 2018, 46: 19-25. DOI: 10.1016/j.mib.2018.01.016.
[21]
MA L, LUKASIK E, GAWEHNS F, et al. The use of agroinfiltration for transient expression of plant resistance and fungal effector proteins in Nicotiana benthamiana leaves[J]. Methods in Molecular Biology, 2012, 835: 61-74. DOI: 10.1007/978-1-61779-501-5_4.
[22]
MA Z G, LIU J J, ZAMANY A, et al. Transient gene expression in western white pine using agroinfiltration[J]. Journal of Forestry Research, 2020, 31(5): 1823-1832. DOI: 10.1007/s11676-019-00938-5.
[23]
ZHANG Q L, XU C R, WEI H Y, et al. Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple[J]. Horticulture Research, 2021, 8(1): 219. DOI: 10.1038/s41438-021-00654-4.
[24]
MA Z G, LIU J J, ZAMANY A. Identification and functional characterization of an effector secreted by Cronartium ribicola[J]. Phytopathology, 2019, 109(6): 942-951. DOI: 10.1094/PHYTO-11-18-0427-R.
[25]
AZMI N S A, SINGKARAVANIT-OGAWA S, IKEDA K, et al. Inappropriate expression of an NLP effector in Colletotrichum orbiculare impairs infection on Cucurbitaceae cultivars via plant recognition of the C-terminal region[J]. Molecular Plant-Microbe Interactions, 2018, 31(1): 101-111. DOI: 10.1094/MPMI-04-17-0085-FI.
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