Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense

ZHAO Yang; LIU Shuang; WANG Zhibiao; WU Junyu; CHEN Daipeng; ZHENG Li

doi:10.15886/j.cnki.rdswxb.20240019

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Volume 16 Issue 1

Mar. 2025

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Article Navigation > Journal of Tropical Biology > 2025 > 16(1): 87-97

ZHAO Yang, LIU Shuang, WANG Zhibiao, WU Junyu, CHEN Daipeng, ZHENG Li. Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense[J]. Journal of Tropical Biology, 2025, 16(1): 87-97. doi: 10.15886/j.cnki.rdswxb.20240019

Citation:

ZHAO Yang, LIU Shuang, WANG Zhibiao, WU Junyu, CHEN Daipeng, ZHENG Li. Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense[J]. Journal of Tropical Biology, 2025, 16(1): 87-97. doi: 10.15886/j.cnki.rdswxb.20240019

Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense

doi: 10.15886/j.cnki.rdswxb.20240019

1. Nanfan College/Sanya Nanfan Institute, Hainan University, Sanya, Hainan 572025, China;
2. School of Tropical Agriculture and Forestry, Hainan University, Danzhou, Hainan 571737, China

Received Date: 2024-02-01
Rev Recd Date: 2024-03-08
Publish Date: 2025-03-15

Abstract

Fusarium wilt of banana is one of the major diseases infecting banana. Effectors produced by Fusarium oxysporum f. sp. Cubense（Foc） play an important role during its infection of banana. Previously, a candidate effector FoSSP80 in Foc was screened. Bioinformatics analysis revealed that the FoSSP80 contained a signal peptide without transmembrane structural domains. Furthermore, the FoSSP80 was confirmed to have a secretory function by using the yeast secretion system. Transient expression of FoSSP80 in Nicotiana benthamiana led to inhibition of programmed cell death（PCD） induced by BAX. Moreover, FoSSP80 inhibited the accumulation of reactive oxygen species（ROS） and the callose deposition. The knockout mutant ΔFoSSP80 did not show significant differences in colony morphology, growth rate, and conidial production and pathogenicity compared with the wild-type and complement strains. These results suggested that FoSSP80 is a typical secretory protein and can inhibit plant defense responses.
- banana,
- Fusarium wilt,
- effector,
- plant immunity

References

[1]	李华平,李云锋,聂燕芳.香蕉枯萎病的发生及防控研究现状[J]. 华南农业大学学报, 2019, 40(5):128-136.
[2]	GHAG S B, SHEKHAWAT U K S, GANAPATHI T R.Fusarium wilt of banana:biology, epidemiology and management[J]. International Journal of Pest Management,2015, 61(3):250-263.
[3]	PLOETZ R C. Management of Fusarium wilt of banana:a review with special reference to tropical race 4[J]. Crop Protection, 2015, 73:7-15.
[4]	ATKINSON N J, URWIN P E. The interaction of plant biotic and abiotic stresses:from genes to the field[J]. Journal of Experimental Botany, 2012, 63(10):3523-3543.
[5]	JONES J D G, DANGL J L. The plant immune system[J]. Nature, 2006, 444(7117):323-329.
[6]	BOLLER T, HE S Y. Innate immunity in plants:an arms race between pattern recognition receptors in plants and effectors in microbial pathogens[J]. Science, 2009, 324(5928):742-744.
[7]	HOUTERMAN P M, SPEIJER D, DEKKER H L, et al.The mixed xylem sap proteome of Fusarium oxysporuminfected tomato plants[J]. Molecular Plant Pathology,2007, 8(2):215-221.
[8]	SCHMIDT S M, HOUTERMAN P M, SCHREIVER I, et al. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum[J]. BMC Genomics, 2013, 14:119.
[9]	REP M, VAN DER DOES H C, MEIJER M, et al. A small,cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato[J]. Molecular Microbiology,2004, 53(5):1373-1383.
[10]	HOUTERMAN P M, MA L, VAN OOIJEN G, et al. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly[J]. The Plant Journal:for Cell and Molecular Biology, 2009, 58(6):970-978.
[11]	MA L, HOUTERMAN P M, GAWEHNS F, et al. The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato[J]. The New Phytologist, 2015,208(2):507-518.
[12]	GAWEHNS F, HOUTERMAN P M, ICHOU F A, et al.The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death[J]. Molecular Plant-Microbe Interactions:MPMI, 2014,27(4):336-348.
[13]	HOU X, AN B, WANG Q, et al. SGE1 is involved in conidiation and pathogenicity of Fusarium oxysporum f.sp. cubense[J]. Canadian Journal of Microbiology, 2018,64(5):349-357.
[14]	AN B, HOU X, GUO Y, et al. The effector SIX8 is required for virulence of Fusarium oxysporum f. sp.cubense tropical race 4 to Cavendish banana[J]. Fungal Biology, 2019, 123(5):423-430.
[15]	GUO L, WANG J, LIANG C, et al. Fosp9, a novel secreted protein, is essential for the full virulence of Fusarium oxysporum f. sp. cubense on banana(Musa spp.) [J]. Applied and Environmental Microbiology,2022, 88(6):e0060421.
[16]	WANG Y, ZHANG X, WANG T, et al. The small secreted protein FoSsp1 elicits plant defenses and negatively regulates pathogenesis in Fusarium oxysporum f.sp. cubense(Foc4) [J]. Frontiers in Plant Science, 2022,13:873451.
[17]	WANG T, XU Y, ZHAO Y, et al. Systemic screening of Fusarium oxysporum candidate effectors reveals FoSSP17 that suppresses plant immunity and contributes to virulence[J]. Phytopathology Research, 2023, 5(1):42.
[18]	TAMURA K, STECHER G, KUMAR S. MEGA11:molecular evolutionary genetics analysis version 11[J]. Molecular Biology and Evolution, 2021, 38(7):3022-3027.
[19]	王田,符俐盈,赵阳,等.香蕉枯萎病菌候选效应蛋白FoSSP20的鉴定和功能初探[J]. 热带生物学报, 2024,15(1):85-93.
[20]	GU B, KALE S D, WANG Q, et al. Rust secreted protein Ps87 is conserved in diverse fungal pathogens and contains a RXLR-like motif sufficient for translocation into plant cells[J]. PLoS One, 2011, 6(11):e27217.
[21]	WEI Y, LIU W, HU W, et al. The chaperone MeHSP90recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava[J]. The New Phytologist, 2020, 226(2):476-491.
[22]	DONG J, CHEN W. The role of autophagy in chloroplast degradation and chlorophagy in immune defenses during Pst DC3000(AvrRps4) infection[J]. PLoS One, 2013,8(8):e73091.
[23]	GOSWAMI R S. Targeted gene replacement in fungi using a split-marker approach[J]. Methods in Molecular Biology, 2012, 835:255-269.
[24]	YUN Y, LIU Z, ZHANG J, et al. The MAPKK FgMkk1 of Fusarium graminearum regulates vegetative differentiation, multiple stress response, and virulence via the cell wall integrity and high-osmolarity glycerol signaling pathways[J]. Environmental Microbiology, 2014, 16(7):2023-2037.
[25]	CHEN D, WANG Y, ZHOU X, et al. The Sch9 kinase regulates conidium size, stress responses, and pathogenesis in Fusarium graminearum[J]. PLoS One, 2014, 9(8):e105811.
[26]	ZHANG L, CENCI A, ROUARD M, et al. Transcriptomic analysis of resistant and susceptible banana corms in response to infection by Fusarium oxysporum f. sp.cubense tropical race 4[J]. Scientific Reports, 2019,9(1):8199.
[27]	LEE M C S, MILLER E A, GOLDBERG J, et al. Bidirectional protein transport between the ER and Golgi[J]. Annual Review of Cell and Developmental Biology, 2004,20:87-123.
[28]	LACOMME C, SANTA CRUZ S. Bax-induced cell death in tobacco is similar to the hypersensitive response[J]. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(14):7956-7961.
[29]	ABRAMOVITCH R B, KIM Y J, CHEN S, et al. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death[J]. The EMBO Journal, 2003, 22(1):60-69.
[30]	LI X, JIN C, YUAN H, et al. The barley powdery mildew effectors CSEP0139 and CSEP0182 suppress cell death and promote B. graminis fungal virulence in plants[J]. Phytopathology Research, 2021, 3(1):7.
[31]	LING T, VANDELLE E, BELLIN D, et al. Nitric oxide produced during the hypersensitive response modulates the plant signaling network and inhibits the pathogen's virulence machinery[J]. Nitric Oxide, 2012, 27:S9.

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通讯作者: 陈斌, bchen63@163.com

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沈阳化工大学材料科学与工程学院沈阳 110142

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Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense

1. Nanfan College/Sanya Nanfan Institute, Hainan University, Sanya, Hainan 572025, China;

2. School of Tropical Agriculture and Forestry, Hainan University, Danzhou, Hainan 571737, China

Received Date: 2024-02-01

Rev Recd Date: 2024-03-08

Publish Date: 2025-03-15

Key words:

Abstract: Fusarium wilt of banana is one of the major diseases infecting banana. Effectors produced by Fusarium oxysporum f. sp. Cubense（Foc） play an important role during its infection of banana. Previously, a candidate effector FoSSP80 in Foc was screened. Bioinformatics analysis revealed that the FoSSP80 contained a signal peptide without transmembrane structural domains. Furthermore, the FoSSP80 was confirmed to have a secretory function by using the yeast secretion system. Transient expression of FoSSP80 in Nicotiana benthamiana led to inhibition of programmed cell death（PCD） induced by BAX. Moreover, FoSSP80 inhibited the accumulation of reactive oxygen species（ROS） and the callose deposition. The knockout mutant ΔFoSSP80 did not show significant differences in colony morphology, growth rate, and conidial production and pathogenicity compared with the wild-type and complement strains. These results suggested that FoSSP80 is a typical secretory protein and can inhibit plant defense responses.

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Reference (31)

[1]	李华平,李云锋,聂燕芳.香蕉枯萎病的发生及防控研究现状[J]. 华南农业大学学报, 2019, 40(5):128-136.
[2]	GHAG S B, SHEKHAWAT U K S, GANAPATHI T R.Fusarium wilt of banana:biology, epidemiology and management[J]. International Journal of Pest Management,2015, 61(3):250-263.
[3]	PLOETZ R C. Management of Fusarium wilt of banana:a review with special reference to tropical race 4[J]. Crop Protection, 2015, 73:7-15.
[4]	ATKINSON N J, URWIN P E. The interaction of plant biotic and abiotic stresses:from genes to the field[J]. Journal of Experimental Botany, 2012, 63(10):3523-3543.
[5]	JONES J D G, DANGL J L. The plant immune system[J]. Nature, 2006, 444(7117):323-329.
[6]	BOLLER T, HE S Y. Innate immunity in plants:an arms race between pattern recognition receptors in plants and effectors in microbial pathogens[J]. Science, 2009, 324(5928):742-744.
[7]	HOUTERMAN P M, SPEIJER D, DEKKER H L, et al.The mixed xylem sap proteome of Fusarium oxysporuminfected tomato plants[J]. Molecular Plant Pathology,2007, 8(2):215-221.
[8]	SCHMIDT S M, HOUTERMAN P M, SCHREIVER I, et al. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum[J]. BMC Genomics, 2013, 14:119.
[9]	REP M, VAN DER DOES H C, MEIJER M, et al. A small,cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato[J]. Molecular Microbiology,2004, 53(5):1373-1383.
[10]	HOUTERMAN P M, MA L, VAN OOIJEN G, et al. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly[J]. The Plant Journal:for Cell and Molecular Biology, 2009, 58(6):970-978.
[11]	MA L, HOUTERMAN P M, GAWEHNS F, et al. The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato[J]. The New Phytologist, 2015,208(2):507-518.
[12]	GAWEHNS F, HOUTERMAN P M, ICHOU F A, et al.The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death[J]. Molecular Plant-Microbe Interactions:MPMI, 2014,27(4):336-348.
[13]	HOU X, AN B, WANG Q, et al. SGE1 is involved in conidiation and pathogenicity of Fusarium oxysporum f.sp. cubense[J]. Canadian Journal of Microbiology, 2018,64(5):349-357.
[14]	AN B, HOU X, GUO Y, et al. The effector SIX8 is required for virulence of Fusarium oxysporum f. sp.cubense tropical race 4 to Cavendish banana[J]. Fungal Biology, 2019, 123(5):423-430.
[15]	GUO L, WANG J, LIANG C, et al. Fosp9, a novel secreted protein, is essential for the full virulence of Fusarium oxysporum f. sp. cubense on banana(Musa spp.) [J]. Applied and Environmental Microbiology,2022, 88(6):e0060421.
[16]	WANG Y, ZHANG X, WANG T, et al. The small secreted protein FoSsp1 elicits plant defenses and negatively regulates pathogenesis in Fusarium oxysporum f.sp. cubense(Foc4) [J]. Frontiers in Plant Science, 2022,13:873451.
[17]	WANG T, XU Y, ZHAO Y, et al. Systemic screening of Fusarium oxysporum candidate effectors reveals FoSSP17 that suppresses plant immunity and contributes to virulence[J]. Phytopathology Research, 2023, 5(1):42.
[18]	TAMURA K, STECHER G, KUMAR S. MEGA11:molecular evolutionary genetics analysis version 11[J]. Molecular Biology and Evolution, 2021, 38(7):3022-3027.
[19]	王田,符俐盈,赵阳,等.香蕉枯萎病菌候选效应蛋白FoSSP20的鉴定和功能初探[J]. 热带生物学报, 2024,15(1):85-93.
[20]	GU B, KALE S D, WANG Q, et al. Rust secreted protein Ps87 is conserved in diverse fungal pathogens and contains a RXLR-like motif sufficient for translocation into plant cells[J]. PLoS One, 2011, 6(11):e27217.
[21]	WEI Y, LIU W, HU W, et al. The chaperone MeHSP90recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava[J]. The New Phytologist, 2020, 226(2):476-491.
[22]	DONG J, CHEN W. The role of autophagy in chloroplast degradation and chlorophagy in immune defenses during Pst DC3000(AvrRps4) infection[J]. PLoS One, 2013,8(8):e73091.
[23]	GOSWAMI R S. Targeted gene replacement in fungi using a split-marker approach[J]. Methods in Molecular Biology, 2012, 835:255-269.
[24]	YUN Y, LIU Z, ZHANG J, et al. The MAPKK FgMkk1 of Fusarium graminearum regulates vegetative differentiation, multiple stress response, and virulence via the cell wall integrity and high-osmolarity glycerol signaling pathways[J]. Environmental Microbiology, 2014, 16(7):2023-2037.
[25]	CHEN D, WANG Y, ZHOU X, et al. The Sch9 kinase regulates conidium size, stress responses, and pathogenesis in Fusarium graminearum[J]. PLoS One, 2014, 9(8):e105811.
[26]	ZHANG L, CENCI A, ROUARD M, et al. Transcriptomic analysis of resistant and susceptible banana corms in response to infection by Fusarium oxysporum f. sp.cubense tropical race 4[J]. Scientific Reports, 2019,9(1):8199.
[27]	LEE M C S, MILLER E A, GOLDBERG J, et al. Bidirectional protein transport between the ER and Golgi[J]. Annual Review of Cell and Developmental Biology, 2004,20:87-123.
[28]	LACOMME C, SANTA CRUZ S. Bax-induced cell death in tobacco is similar to the hypersensitive response[J]. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(14):7956-7961.
[29]	ABRAMOVITCH R B, KIM Y J, CHEN S, et al. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death[J]. The EMBO Journal, 2003, 22(1):60-69.
[30]	LI X, JIN C, YUAN H, et al. The barley powdery mildew effectors CSEP0139 and CSEP0182 suppress cell death and promote B. graminis fungal virulence in plants[J]. Phytopathology Research, 2021, 3(1):7.
[31]	LING T, VANDELLE E, BELLIN D, et al. Nitric oxide produced during the hypersensitive response modulates the plant signaling network and inhibits the pathogen's virulence machinery[J]. Nitric Oxide, 2012, 27:S9.

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Functional characterization of candidate effector FoSSP80 in Fusarium oxysporum f. sp. cubense

doi: 10.15886/j.cnki.rdswxb.20240019

Abstract

References

Proportional views

通讯作者: 陈斌, bchen63@163.com

Proportional views

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