Cytosolic pH Controls Fungal MAPK Signaling and Pathogenicity

Fernandes, Tania; Mariscal, Melani; Serrano, Antonio; Segorbe, David; Fernández-Acero, Teresa; Martı́n, Humberto; Turrà, David; Pietro, Antonio Di

doi:10.1128/mbio.00285-23

Cited by 9 publications

(6 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Repression of pmaA was also implicated in negative chemotropism to nitrate ( S4B Fig ). Since repression of pmaA affects plasma membrane integrity and MAPK signaling as well as growth inhibition [ 27 ], it may also exert indirect effects, such as altering the localization of nitrate transporters.…”

Section: Resultsmentioning

confidence: 99%

Hyphae of the fungus Aspergillus nidulans demonstrate chemotropism to nutrients and pH

Yamamoto,

Miki,

Itani

et al. 2024

PLoS Biol

View full text Add to dashboard Cite

The importance of fungi in ecological systems and pathogenicity hinges on their ability to search for nutrients, substrates, and hosts. Despite this, the question of whether fungal hyphae exhibit chemotropism toward them remains largely unresolved and requires close examination at the cellular level. Here, we designed a microfluidic device to assess hyphal chemotropism of Aspergillus nidulans in response to carbon and nitrogen sources, as well as pH. Within this device, hyphae could determine their growth direction in a two-layer flow with distinct compositions that were adjacent but non-mixing. Under conditions with and without a carbon source, hyphae changed growth direction to remain in the presence of a carbon source, but it was still difficult to distinguish between differences in growth and chemotropism. Although nitrogen sources such as ammonia and nitrate are important for growth, the hyphae indicated negative chemotropism to avoid them depending on the specific transporters. This fungus grows equally well at the colony level in the pH range of 4 to 9, but the hyphae exhibited chemotropism to acidic pH. The proton pump PmaA is vital for the chemotropism to acid pH, while the master regulatory for pH adaptation PacC is not involved, suggesting that chemotropism and adaptive growth via gene expression regulation are distinct regulatory mechanisms. Despite various plasma membrane transporters are distributed across membranes except at the hyphal tip, the control of growth direction occurs at the tip. Finally, we explored the mechanisms linking these two phenomena, tip growth and chemotropism.

show abstract

Section: Resultsmentioning

confidence: 99%

Hyphae of the fungus Aspergillus nidulans demonstrate chemotropism to nutrients and pH

Yamamoto,

Miki,

Itani

et al. 2024

PLoS Biol

View full text Add to dashboard Cite

show abstract

“…It was reported that plasma membrane P-type ATPase is a type of transport protein localized in the plasma membrane and is responsible for pumping hydrogen proteins from the cytoplasm to the extracellular space to maintain intracellular pH and ion homeostasis [7][8][9]. There are two plasma membrane H + -ATPases, PMA1 and PMA2, in fungi [10][11][12]. Many studies have shown that PMA1 is localized in lipid microdomains of the plasma membrane and plays an important role in cell growth and virulence in pathogenic fungi [16,17].…”

Section: Discussionmentioning

confidence: 99%

“…Among these subtypes, plasma membrane H + -ATPase is a type of hydrogen proton pump driven by ATP, which is responsible for pumping hydrogen protons from the cytoplasm to the extracellular space to maintain intracellular pH and ion homeostasis, form transmembrane electrochemical potential, and promote nutrient transportation and the expulsion of secondary metabolites [7][8][9]. Most fungi have two plasma membrane H + -ATPases, PMA1 and PMA2 [10][11][12][13]. The structure and function of plasma membrane H + -ATPases, especially PMA1, have been extensively studied in some fungi, such as Fusarium graminearum, Valsa mali, and Ustilago maydis [14,15].…”

Section: Introductionmentioning

confidence: 99%

The Plasma Membrane H+ ATPase CsPMA2 Regulates Lipid Droplet Formation, Appressorial Development and Virulence in Colletotrichum siamense

Liu,

Xi,

et al. 2023

IJMS

View full text Add to dashboard Cite

Plasma membrane H+-ATPases (PMAs) play an important role in the pathogenicity of pathogenic fungi. Lipid droplets are important storage sites for neutral lipids in fungal conidia and hyphae and can be used by plant pathogenic fungi for infection. However, the relationship between plasma membrane H+-ATPase, lipid droplets and virulence remains unclear. Here, we characterized a plasma membrane H+-ATPase, CsPMA2, that plays a key role in lipid droplet formation, appresorial development and virulence in C. siamense. Deletion of CsPMA2 impaired C. siamense conidial size, conidial germination, appressorial development and virulence but did not affect hyphal growth. ΔCsPMA2 increased the sensitivity of C. siamense to phytic acid and oxalic acid. CsPMA2 was localized to lipids on the plasma membrane and intracellular membrane. Deletion of CsPMA2 significantly inhibited the accumulation of lipid droplets and significantly affected the contents of some species of lipids, including 12 species with decreased lipid contents and 3 species with increased lipid contents. Furthermore, low pH can inhibit CsPMA2 expression and lipid droplet accumulation. Overall, our data revealed that the plasma membrane H+-ATPase CsPMA2 is involved in the regulation of lipid droplet formation and affects appressorial development and virulence in C. siamense.

show abstract

“…The success of fungal infections is affected by environmental factors, particularly pH (Xu et al 2015 , Barda et al 2020 , Han et al 2021 , Jimdjio et al 2021 , Li et al 2022 , Yang et al 2022 ). Recent findings indicated that extracellular or cytosolic acidification rapidly induce the highly conserved mitogen-activated protein kinase signaling cascades, which regulate various aspects of fungal pathogenicity and promote infection of host plant (Fernandes et al 2023 ). Pathogenic fungi have the ability to manipulate the pH of the surrounding environment when infecting plants, creating a more favorable condition for their growth and reproduction (Kesten et al 2019 ).…”

Section: Crops Protection: Ph-dependent Pathogenicity and Possible In...mentioning

confidence: 99%

Exploitation of microbial activities at low pH to enhance planetary health

Atasoy,

Álvarez Ordóñez,

Cenian

et al. 2023

FEMS Microbiology Reviews

View full text Add to dashboard Cite

Awareness is growing that human health cannot be considered in isolation but is inextricably woven with the health of the environment in which we live. It is however under-recognised that the sustainability of human activities strongly relies on preserving the equilibrium of the microbial communities living in/on/around us. Microbial metabolic activities are instrumental for production, functionalization, processing and preservation of food. For circular economy, microbial metabolism would be exploited to produce building blocks for the chemical industry, to achieve effective crop protection, agri-food waste revalorization or biofuel production, as well as in bioremediation and bioaugmentation of contaminated areas. Low pH is undoubtedly a key physical-chemical parameter that needs to be considered for exploiting the powerful microbial metabolic arsenal. Deviation from optimal pH conditions has profound effects on shaping the microbial communities responsible for carrying out essential processes. Furthermore, novel strategies to combat contaminations and infections by pathogens rely on microbial-derived acidic molecules that suppress/inhibit their growth. Herein, we present the state-of-the-art of the knowledge on the impact of acidic pH in many applied areas and how this knowledge can guide us to use the immense arsenal of microbial metabolic activities for their more impactful exploitation in a Planetary Health perspective.

show abstract

Cytosolic pH Controls Fungal MAPK Signaling and Pathogenicity

Abstract: Fungal phytopathogens cause devastating losses in global agriculture. All plant-infecting fungi use conserved MAPK signaling pathways to successfully locate, enter, and colonize their hosts.

Cited by 9 publications

References 80 publications

Hyphae of the fungus Aspergillus nidulans demonstrate chemotropism to nutrients and pH

Hyphae of the fungus Aspergillus nidulans demonstrate chemotropism to nutrients and pH

The Plasma Membrane H+ ATPase CsPMA2 Regulates Lipid Droplet Formation, Appressorial Development and Virulence in Colletotrichum siamense

Exploitation of microbial activities at low pH to enhance planetary health

Contact Info

Product

Resources

About