HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>

ABSTRACT In pathogenic filamentous fungi, conidial germination not only is fundamental for propagation in the environment but is also a critical step of infection. In the insect mycopathogen Beauveria bassiana, we genetically characterized the role of the basic leucine zipper (bZIP) transcription fa...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Yue-Jin Peng, Jia-Jia Wang, Hai-Yan Lin, Jin-Li Ding, Ming-Guang Feng, Sheng-Hua Ying
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	HapX gene conidial reserve phospholipid homeostasis membrane functionality virulence Beauveria bassiana Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/efc63291430c471885cbbe9c612e4b54
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:efc63291430c471885cbbe9c612e4b54
record_format	dspace
spelling	oai:doaj.org-article:efc63291430c471885cbbe9c612e4b542021-12-02T19:46:19ZHapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>10.1128/mSystems.00695-202379-5077https://doaj.org/article/efc63291430c471885cbbe9c612e4b542020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00695-20https://doaj.org/toc/2379-5077ABSTRACT In pathogenic filamentous fungi, conidial germination not only is fundamental for propagation in the environment but is also a critical step of infection. In the insect mycopathogen Beauveria bassiana, we genetically characterized the role of the basic leucine zipper (bZIP) transcription factor HapX (BbHapX) in conidial nutrient reserves and pathogen-host interaction. Ablation of BbHapX resulted in an almost complete loss of virulence in the topical inoculation and intrahemocoel injection assays. Comparative transcriptomic analysis revealed that BbHapX is required for fatty acid (FA)/lipid metabolism, and biochemical analyses indicated that BbHapX loss caused a significant reduction in conidial FA contents. Exogenous oleic acid could partially or completely restore the impaired phenotypes of the ΔBbHapX mutant, including germination rate, membrane integrity, vegetative growth, and virulence. BbHapX mediates fungal iron acquisition which is not required for desaturation of stearic acid. Additionally, inactivation of the Δ9-fatty acid desaturase gene (BbOle1) generated defects similar to those of the ΔBbHapX mutant; oleic acid also had significant restorative effects on the defective phenotypes of the ΔBbOle1 mutant. A gel retarding assay revealed that BbHapX directly regulated the expression of BbOle1. Lipidomic analyses indicated that both BbHapX and BbOle1 contributed to the homeostasis of phospholipids with nonpolar tails derived from oleic acid; therefore, exogenous phospholipids could significantly restore membrane integrity. These data reveal that the HapX-Ole1 pathway contributes to conidial fatty acid/lipid reserves and that there are important links between the lipid biology and membrane functionality involved in the early stages of infection caused by B. bassiana. IMPORTANCE Conidial maturation and germination are highly coupled physiological processes in filamentous fungi that are critical for the pathogenicity of mycopathogens. Compared to the mechanisms involved in conidial germination, those of conidial reserves during maturation are less understood. The insect-pathogenic fungus Beauveria bassiana, as a representative species of filamentous fungi, is important for applied and fundamental research. In addition to its conserved roles in fungal adaptation to iron status, the bZIP transcription factor HapX acts as a master regulator involved in conidial virulence and regulates fatty acid/lipid metabolism. Further investigation revealed that the Δ9-fatty acid desaturase gene (Ole1) is a direct downstream target of HapX. This study reveals the HapX-Ole1 pathway involved in the fatty acid/lipid accumulation associated with conidial maturation and provides new insights into the startup mechanism of infection caused by spores from pathogenic fungi.Yue-Jin PengJia-Jia WangHai-Yan LinJin-Li DingMing-Guang FengSheng-Hua YingAmerican Society for MicrobiologyarticleHapX geneconidial reservephospholipid homeostasismembrane functionalityvirulenceBeauveria bassianaMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	HapX gene conidial reserve phospholipid homeostasis membrane functionality virulence Beauveria bassiana Microbiology QR1-502
spellingShingle	HapX gene conidial reserve phospholipid homeostasis membrane functionality virulence Beauveria bassiana Microbiology QR1-502 Yue-Jin Peng Jia-Jia Wang Hai-Yan Lin Jin-Li Ding Ming-Guang Feng Sheng-Hua Ying HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
description	ABSTRACT In pathogenic filamentous fungi, conidial germination not only is fundamental for propagation in the environment but is also a critical step of infection. In the insect mycopathogen Beauveria bassiana, we genetically characterized the role of the basic leucine zipper (bZIP) transcription factor HapX (BbHapX) in conidial nutrient reserves and pathogen-host interaction. Ablation of BbHapX resulted in an almost complete loss of virulence in the topical inoculation and intrahemocoel injection assays. Comparative transcriptomic analysis revealed that BbHapX is required for fatty acid (FA)/lipid metabolism, and biochemical analyses indicated that BbHapX loss caused a significant reduction in conidial FA contents. Exogenous oleic acid could partially or completely restore the impaired phenotypes of the ΔBbHapX mutant, including germination rate, membrane integrity, vegetative growth, and virulence. BbHapX mediates fungal iron acquisition which is not required for desaturation of stearic acid. Additionally, inactivation of the Δ9-fatty acid desaturase gene (BbOle1) generated defects similar to those of the ΔBbHapX mutant; oleic acid also had significant restorative effects on the defective phenotypes of the ΔBbOle1 mutant. A gel retarding assay revealed that BbHapX directly regulated the expression of BbOle1. Lipidomic analyses indicated that both BbHapX and BbOle1 contributed to the homeostasis of phospholipids with nonpolar tails derived from oleic acid; therefore, exogenous phospholipids could significantly restore membrane integrity. These data reveal that the HapX-Ole1 pathway contributes to conidial fatty acid/lipid reserves and that there are important links between the lipid biology and membrane functionality involved in the early stages of infection caused by B. bassiana. IMPORTANCE Conidial maturation and germination are highly coupled physiological processes in filamentous fungi that are critical for the pathogenicity of mycopathogens. Compared to the mechanisms involved in conidial germination, those of conidial reserves during maturation are less understood. The insect-pathogenic fungus Beauveria bassiana, as a representative species of filamentous fungi, is important for applied and fundamental research. In addition to its conserved roles in fungal adaptation to iron status, the bZIP transcription factor HapX acts as a master regulator involved in conidial virulence and regulates fatty acid/lipid metabolism. Further investigation revealed that the Δ9-fatty acid desaturase gene (Ole1) is a direct downstream target of HapX. This study reveals the HapX-Ole1 pathway involved in the fatty acid/lipid accumulation associated with conidial maturation and provides new insights into the startup mechanism of infection caused by spores from pathogenic fungi.
format	article
author	Yue-Jin Peng Jia-Jia Wang Hai-Yan Lin Jin-Li Ding Ming-Guang Feng Sheng-Hua Ying
author_facet	Yue-Jin Peng Jia-Jia Wang Hai-Yan Lin Jin-Li Ding Ming-Guang Feng Sheng-Hua Ying
author_sort	Yue-Jin Peng
title	HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
title_short	HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
title_full	HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
title_fullStr	HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
title_full_unstemmed	HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>
title_sort	hapx, an indispensable bzip transcription factor for iron acquisition, regulates infection initiation by orchestrating conidial oleic acid homeostasis and cytomembrane functionality in mycopathogen <named-content content-type="genus-species">beauveria bassiana</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/efc63291430c471885cbbe9c612e4b54
work_keys_str_mv	AT yuejinpeng hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent AT jiajiawang hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent AT haiyanlin hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent AT jinliding hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent AT mingguangfeng hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent AT shenghuaying hapxanindispensablebziptranscriptionfactorforironacquisitionregulatesinfectioninitiationbyorchestratingconidialoleicacidhomeostasisandcytomembranefunctionalityinmycopathogennamedcontentcontenttypegenusspeciesbeauveriabassiananamedcontent
_version_	1718376059324334080

HapX, an Indispensable bZIP Transcription Factor for Iron Acquisition, Regulates Infection Initiation by Orchestrating Conidial Oleic Acid Homeostasis and Cytomembrane Functionality in Mycopathogen <named-content content-type="genus-species">Beauveria bassiana</named-content>

Ejemplares similares