The antifungal responses of insects against an entomopathogenic fungi, Beauveria bassiana and their application potential in pest control

doi:10.3969/j.issn.1004-1524.20230374

Acta Agriculturae Zhejiangensis ›› 2024, Vol. 36 ›› Issue (4): 825-836.DOI: 10.3969/j.issn.1004-1524.20230374

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The antifungal responses of insects against an entomopathogenic fungi, Beauveria bassiana and their application potential in pest control

YANG Lei(), WANG Xiaofu, WEI Wei, CHEN Xiaoyun, PENG Cheng, XU Xiaoli, XU Junfeng()

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Traceability for Agricultural Genetically Modified Organisms, Ministry of Agriculture and Rural Affairs, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China

Received:2022-03-23 Online:2024-04-25 Published:2024-04-29
Contact: XU Junfeng

Abstract

Abstract:

Entomopathogenic fungi Beauveria bassiana can successfully infect and kill a wide range of insect hosts and therefore serve as effective bio-insecticide formulations. Accordingly, insects rely on a variety of strategies to defend against fungal infections, among which innate immunity is an essential component responsible for antifungal responses. The insect cuticle is the first barrier against fungal invasion. The cuticle and exocrine glands can secrete a variety of antifungal compounds to suppresses the virulence of B. bassiana. When the hyphae break through the cuticle and send infective spores to the hemocoel, cellular and humoral immunity work together to generate systemic immune responses. A variety of defense effectors are produced and functioned in cellular nodulation, encapsulation, melanization and apoptosis. Strong immune responses greatly affect the virulence of fungi, leading to the limitations of the application of these mycoinsecticide formulations. In this paper, we detailed immune genes, pathways and strategies against fungal infection. This study contributes to a better understanding of insect antifungal immunity mechanisms, as well as provides a solid basis for the effective improvement of entomopathogenic fungi virulence. This information offers us with new strategies for agricultural pest management.

Key words: entomopathogenic fungi, cuticle immunity, immune pathway, antifungal immune response, pest control

CLC Number:

S476

YANG Lei, WANG Xiaofu, WEI Wei, CHEN Xiaoyun, PENG Cheng, XU Xiaoli, XU Junfeng. The antifungal responses of insects against an entomopathogenic fungi, Beauveria bassiana and their application potential in pest control[J]. Acta Agriculturae Zhejiangensis, 2024, 36(4): 825-836.

Figures/Tables 4

References 83

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免疫类型 Immune response type	靶标RNA沉默对昆虫的影响 Effect of target RNA silencing on insect		基因 Gene	宿主昆虫 Host
识别分子 Recognition molecule	抗菌肽表达降低,对白僵菌的敏感性增加 Decreased the expression profiles of AMPs following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana		革兰氏阴性菌结合蛋白TmGNBP3 Gram-negative binding protein TmGNBP3	黄粉虫 Tenebrio molitor^[40]
	PPO活性降低,导致白僵菌毒力增加 Decreased the activities of immune-related phenoloxidase and increased the virulence of B. bassiana		革兰氏阴性菌结合蛋白ApGNBP1 Gram-negative binding protein ApGNBP1	豌豆蚜 Acyrthosiphon pisum^[39]
	抑制JAK/STAT信号通路,抑制黑化反应 Suppressed the JAK/STAT signaling pathway and the PO cascades		C型凝集素BmCTL5 C-type lectin BmCTL5	家蚕 Bombyx mori ^[43]
	PPO1活性下降,对真菌抗性降低 Decreased the expression levels of PPO1 and decreased the resistance to fungal challenge		C型凝集素CTL14 C-type lectin CTL14	棉铃虫 Helicoverpa armigera^[44]
丝氨酸蛋白酶 Serine proteases	Toll通路和黑化反应相关基因表达水平上调 Increased the expression profiles of genes belong to Toll pathway and melanization		丝氨酸蛋白酶CLSP2 Serine protease CLSP2	埃及伊蚊 Aedes aegypti^[47]
	抑制细菌和真菌感染产生的黑化反应 Inhibited melanization caused by bacterial and fungal infection		Clip结构域丝氨酸蛋白酶MP1 Clip domain serine protease MP1	黑腹果蝇 Drosophila melanogaster ^[72]
	主要抑制由真菌感染引起的黑化反应 Inhibited melanization caused by fungal infection		Clip结构域丝氨酸蛋白酶MP2 Clip domain serine protease MP2	黑腹果蝇 D. melanogaster ^[72]
	PO活性下降、菌丝黑化减少,真菌繁殖加快 Decreased PO activity, abolished completely melanin formation on hyphae and exhibited fungal proliferation		Clip结构域丝氨酸蛋白酶CLIPA8 Clip domain serine protease CLIPA8	冈比亚按蚊 Anopheles gambiae ^[20,73]
	共同干扰CLIPB9和CLIPA14基因抑制黑化反应,对真菌易感性增加 Co-silencing of CLIPB9 and CLIPA14 genes reduced melanization and increased susceptibility to the entomopathogenic fungus		Clip结构域丝氨酸蛋白酶CLIPB9和 CLIPA14 Clip domain serine protease CLIPB9 and CLIPA14	埃及伊蚊 A. aegypti ^[74]
调节因子 Regulatory factors	Serpin-27A表达降低,对白僵菌的敏感性增加 Decreased induction of Aedes Serpin-27A following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana		细胞因子Spz1C,受体蛋白Toll5A Cytokine Spatzle Spz1C, Toll receptor Toll5A	埃及伊蚊 A. aegypti ^[52]
		抗菌肽表达降低,对白僵菌的敏感性增加 Decreased the expression profiles of AMPs following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana	骨髓分化因子TmMyD88,肿瘤坏死因子受体相关因子4 Myeloid differentiation factor 8 TmMyD88, Tumour necrosis factor receptor-related factor 4		黄粉虫 T. molitor ^[40], 埃及伊蚊 A. aegypti ^[53]
		对白僵菌的敏感性增加 Increased susceptibility to the entomopathogenic fungus B. bassiana	NF-κB转录因子REL1 NF-κB transcription factor REL1		冈比亚按蚊 A. gambiae ^[50]
		影响serpin-27表达,抑制抗白僵菌免疫应答 Affected the expression profile of serpin-27 and suppressed the immune response against B. bassiana	NF-κB转录因子AaREL1-A和AaREL1-B NF-κB transcription factor AaREL1-A and AaREL1-B		埃及伊蚊 A. aegypti ^[51]
		死亡率增加 Increased the mortality of the host	NF-κB转录因子Sldorsal NF-κB transcription factor Sldorsal		斜纹夜蛾 Spodoptera litura ^[83]
		白僵菌感染蚊子的真菌增殖和存活时间降低 Reduced fungal proliferation and reduced survival times upon B. bassiana infection	NF-κB转录因子REL2 NF-κB transcription factor REL2		埃及伊蚊 A. aegypti ^[55]
		阻止REL1的核转录,对白僵菌的抗性增加 Increased resistance to B. bassiana by blocking the nuclear transcription of REL1	IMD通路的负调节子Caspar A negative regulator of the Imd pathway Caspar		埃及伊蚊 A. aegypti^[55⇓-57]
		白僵菌后感染家蚕存活时间下降 Decreased survival rate of silkworm	JAK/STAT调节因子,STAT调节的抗登革热限制因子DVRF1 Dome Transcription factor of JAK-STAT Dome, STAT-regulated anti-dengue restriction factor DVRF1		家蚕 B. mori ^[59]
效应因子 Effectors		对白僵菌的抗性增加;参与CLSP2介导的抗真菌免疫防御应答 Increased the resistance to the fungal challenge and participated in CLSP2-modulated mosquito antifungal defense	含硫酯键蛋白TEP22 Thioester-containing protein TEP22		埃及伊蚊 A. aegypti ^[47]
		PO活性下降、菌丝黑化减少,真菌繁殖加快 Decreased PO activity, abolished completely melanin formation on hyphae and exhibited fungal proliferation	含硫酯键蛋白TEP1 Thioester-containing protein TEP1		冈比亚按蚊 A. gambiae^[20]
		存活率下降,促进真菌繁殖 Reduced survival rate and accelerated fungal proliferation	抗菌肽Tenecin 3 AMP Tenecin3		黄粉虫 T. molitor ^[65]
体表抗菌化合物 Antimicrobial compounds on the		显著削弱了宿主抵抗白僵菌感染的能力 Significantly compromised host defense against the fungal infection	几丁质合成酶1基因CHS1 Chitin synthase 1 gene CHS1		赤拟谷盗 Tribolium castaneum ^[21]
body surface		使白僵菌的防御系统完全崩溃 Destroyed antifungal host defense	漆酶Lac2 Laccase Lac2		赤拟谷盗 T. castaneum ^[22]
其他 Others		促进免疫效应因子的表达,间接抑制家蚕中白僵菌的繁殖 Promoted the expression of immune effectors, and indirectly inhibited the reproduction of B. bassiana in the silkworm	载脂蛋白III BmApoLp-III Apolipophorin-III BmApoLp-III		家蚕 B. mori ^[69]
		酚氧化酶和溶菌酶活性降低、总血细胞计数减少,存活率下降 Significantly decreased phenoloxidase and lysozyme activity, total haemocyte counts, and survival rate against B. bassiana infection	章鱼胺受体MsOctfl2R Octopamine receptor MsOctfl2R		东方黏虫 Mythmina separata^[70]

免疫类型 Immune response type	靶标RNA沉默对昆虫的影响 Effect of target RNA silencing on insect		基因 Gene	宿主昆虫 Host
识别分子 Recognition molecule	抗菌肽表达降低,对白僵菌的敏感性增加 Decreased the expression profiles of AMPs following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana		革兰氏阴性菌结合蛋白TmGNBP3 Gram-negative binding protein TmGNBP3	黄粉虫 Tenebrio molitor^[40]
	PPO活性降低,导致白僵菌毒力增加 Decreased the activities of immune-related phenoloxidase and increased the virulence of B. bassiana		革兰氏阴性菌结合蛋白ApGNBP1 Gram-negative binding protein ApGNBP1	豌豆蚜 Acyrthosiphon pisum^[39]
	抑制JAK/STAT信号通路,抑制黑化反应 Suppressed the JAK/STAT signaling pathway and the PO cascades		C型凝集素BmCTL5 C-type lectin BmCTL5	家蚕 Bombyx mori ^[43]
	PPO1活性下降,对真菌抗性降低 Decreased the expression levels of PPO1 and decreased the resistance to fungal challenge		C型凝集素CTL14 C-type lectin CTL14	棉铃虫 Helicoverpa armigera^[44]
丝氨酸蛋白酶 Serine proteases	Toll通路和黑化反应相关基因表达水平上调 Increased the expression profiles of genes belong to Toll pathway and melanization		丝氨酸蛋白酶CLSP2 Serine protease CLSP2	埃及伊蚊 Aedes aegypti^[47]
	抑制细菌和真菌感染产生的黑化反应 Inhibited melanization caused by bacterial and fungal infection		Clip结构域丝氨酸蛋白酶MP1 Clip domain serine protease MP1	黑腹果蝇 Drosophila melanogaster ^[72]
	主要抑制由真菌感染引起的黑化反应 Inhibited melanization caused by fungal infection		Clip结构域丝氨酸蛋白酶MP2 Clip domain serine protease MP2	黑腹果蝇 D. melanogaster ^[72]
	PO活性下降、菌丝黑化减少,真菌繁殖加快 Decreased PO activity, abolished completely melanin formation on hyphae and exhibited fungal proliferation		Clip结构域丝氨酸蛋白酶CLIPA8 Clip domain serine protease CLIPA8	冈比亚按蚊 Anopheles gambiae ^[20,73]
	共同干扰CLIPB9和CLIPA14基因抑制黑化反应,对真菌易感性增加 Co-silencing of CLIPB9 and CLIPA14 genes reduced melanization and increased susceptibility to the entomopathogenic fungus		Clip结构域丝氨酸蛋白酶CLIPB9和 CLIPA14 Clip domain serine protease CLIPB9 and CLIPA14	埃及伊蚊 A. aegypti ^[74]
调节因子 Regulatory factors	Serpin-27A表达降低,对白僵菌的敏感性增加 Decreased induction of Aedes Serpin-27A following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana		细胞因子Spz1C,受体蛋白Toll5A Cytokine Spatzle Spz1C, Toll receptor Toll5A	埃及伊蚊 A. aegypti ^[52]
		抗菌肽表达降低,对白僵菌的敏感性增加 Decreased the expression profiles of AMPs following fungal challenge and increased susceptibility to the entomopathogenic fungus B. bassiana	骨髓分化因子TmMyD88,肿瘤坏死因子受体相关因子4 Myeloid differentiation factor 8 TmMyD88, Tumour necrosis factor receptor-related factor 4		黄粉虫 T. molitor ^[40], 埃及伊蚊 A. aegypti ^[53]
		对白僵菌的敏感性增加 Increased susceptibility to the entomopathogenic fungus B. bassiana	NF-κB转录因子REL1 NF-κB transcription factor REL1		冈比亚按蚊 A. gambiae ^[50]
		影响serpin-27表达,抑制抗白僵菌免疫应答 Affected the expression profile of serpin-27 and suppressed the immune response against B. bassiana	NF-κB转录因子AaREL1-A和AaREL1-B NF-κB transcription factor AaREL1-A and AaREL1-B		埃及伊蚊 A. aegypti ^[51]
		死亡率增加 Increased the mortality of the host	NF-κB转录因子Sldorsal NF-κB transcription factor Sldorsal		斜纹夜蛾 Spodoptera litura ^[83]
		白僵菌感染蚊子的真菌增殖和存活时间降低 Reduced fungal proliferation and reduced survival times upon B. bassiana infection	NF-κB转录因子REL2 NF-κB transcription factor REL2		埃及伊蚊 A. aegypti ^[55]
		阻止REL1的核转录,对白僵菌的抗性增加 Increased resistance to B. bassiana by blocking the nuclear transcription of REL1	IMD通路的负调节子Caspar A negative regulator of the Imd pathway Caspar		埃及伊蚊 A. aegypti^[55⇓-57]
		白僵菌后感染家蚕存活时间下降 Decreased survival rate of silkworm	JAK/STAT调节因子,STAT调节的抗登革热限制因子DVRF1 Dome Transcription factor of JAK-STAT Dome, STAT-regulated anti-dengue restriction factor DVRF1		家蚕 B. mori ^[59]
效应因子 Effectors		对白僵菌的抗性增加;参与CLSP2介导的抗真菌免疫防御应答 Increased the resistance to the fungal challenge and participated in CLSP2-modulated mosquito antifungal defense	含硫酯键蛋白TEP22 Thioester-containing protein TEP22		埃及伊蚊 A. aegypti ^[47]
		PO活性下降、菌丝黑化减少,真菌繁殖加快 Decreased PO activity, abolished completely melanin formation on hyphae and exhibited fungal proliferation	含硫酯键蛋白TEP1 Thioester-containing protein TEP1		冈比亚按蚊 A. gambiae^[20]
		存活率下降,促进真菌繁殖 Reduced survival rate and accelerated fungal proliferation	抗菌肽Tenecin 3 AMP Tenecin3		黄粉虫 T. molitor ^[65]
体表抗菌化合物 Antimicrobial compounds on the		显著削弱了宿主抵抗白僵菌感染的能力 Significantly compromised host defense against the fungal infection	几丁质合成酶1基因CHS1 Chitin synthase 1 gene CHS1		赤拟谷盗 Tribolium castaneum ^[21]
body surface		使白僵菌的防御系统完全崩溃 Destroyed antifungal host defense	漆酶Lac2 Laccase Lac2		赤拟谷盗 T. castaneum ^[22]
其他 Others		促进免疫效应因子的表达,间接抑制家蚕中白僵菌的繁殖 Promoted the expression of immune effectors, and indirectly inhibited the reproduction of B. bassiana in the silkworm	载脂蛋白III BmApoLp-III Apolipophorin-III BmApoLp-III		家蚕 B. mori ^[69]
		酚氧化酶和溶菌酶活性降低、总血细胞计数减少,存活率下降 Significantly decreased phenoloxidase and lysozyme activity, total haemocyte counts, and survival rate against B. bassiana infection	章鱼胺受体MsOctfl2R Octopamine receptor MsOctfl2R		东方黏虫 Mythmina separata^[70]

The antifungal responses of insects against an entomopathogenic fungi, Beauveria bassiana and their application potential in pest control

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