The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

Abstract

Sensing environmental factors and responding swiftly to them is essential for all living organisms. For instance, predators must act rapidly once prey is sensed. Nematode-trapping fungi (NTF) are predators that use “traps” differentiated from vegetative hyphae to capture, kill, and consume nematodes. These traps undergo drastic and rapid morphological changes upon nematode induction. Multiple signaling hubs have been shown to regulate this remarkable process. Here, we demonstrate that the conserved cAMP-PKA signaling pathway exerts a crucial role in trap morphogenesis of the NTF Arthrobotrys oligospora. A gene deletion mutant of the PKA catalytic subunit TPK2 proved insensitive towards nematode presence. Moreover, we show that the G protein alpha subunit GPA2 acts upstream of adenylate cyclase, with GPA2 deletion resulting in substantially reduced trap formation, whereas exogenous provision of cAMP rescued the prey-sensing and trap morphogenesis defects of a gpa2 mutant. Thus, we show that cAMP production triggered by G protein signaling and downstream PKA activity are vital for prey-sensing and trap development in A. oligospora, demonstrating that this highly conserved signaling pathway is critical for NTF and nematode predator-prey interactions.

The cAMP‐PKA signalling pathway regulates hyphal growth, conidiation, trap morphogenesis, stress tolerance, and autophagy in Arthrobotrys oligospora

“…In the plant pathogen F. graminearum, double mutants of the PKA catalytic subunit-encoding genes cpk1 and cpk2 are severely defective in pathogenicity (Hu et al, 2014). Here, the results showed that ΔAoacy and ΔAopkaC1 mutants lost the ability to form traps and capture nematodes (Figure 2), which was consistent with the analysis in A. oligospora (strain TWF154); the absence of the PKA catalytic subunit Tpk2 (an orthologue of PkaC1) abolishes trap morphogenesis (Chen et al, 2022). Therefore, the cAMP-PKA signalling pathway is required for the morphogenesis of infection structures in NT fungi and other pathogenic fungi.…”

“…In addition, mitogen‐activated protein kinase (MAPK) signalling and Ca 2+ ‐related signalling are involved in the regulation of trap formation and hyphal development (Kuo et al, 2020; Xie et al, 2021, 2022a; Jiang et al, 2022). Recently, a gene deletion mutant of the PKA catalytic subunit Tpk2 in A. oligospora was shown to be insensitive to nematode presence (Chen et al, 2022). However, the function of the cAMP‐PKA signalling pathway in A. oligospora and other NT fungi remains largely unclear.…”

“…Recently, a gene deletion mutant of the PKA catalytic subunit Tpk2 in A. oligospora was shown to be insensitive to nematode presence (Chen et al, 2022). However, the function of the cAMP-PKA signalling pathway in A. oligospora and other NT fungi remains largely unclear.…”

Characterizing the Role of AosfgA and AofluG in Mycelial and Conidial Development in Arthrobotrys oligospora and Their Role in Secondary Metabolism

“…Using the amino acid sequences of spore-producing genes in model fungi such as the Aspergillus nidulans , Aspergillus fumigatus , and Neurospora crassa as references, the homologs of AosfgA and AofluG in A. oligospora were obtained through comparison using the NCBI database [ 36 ]. The physicochemical properties of individual amino acid sequences were calculated using ExPASy-ProtParam-tool, and the domains and functional sites of proteins were predicted using InterProScan.…”

p21-activated kinase is involved in the sporulation, pathogenicity, and stress response of Arthrobotrys oligospora under the indirect regulation of Rho GTPase-activating protein

“…Recently, we have demonstrated that AoRac and AoCdc42 play a crucial role in hypha growth, lipid accumulation, DNA damage, sporulation, trap formation, pathogenicity, and stress response ( Yang et al, 2022 ). Subsequently, the cAMP-PKA signaling pathway has been proven to be involved in hyphal growth, sporulation, trap morphogenesis, stress tolerance, and autophagy in A. oligospora ( Chen et al, 2022 ; Zhu et al, 2022b ). In addition, several genes are related to MAPK cascades, such as mkk1 (coding a MAP kinase kinase) and bck1 (coding a MAP kinase kinase kinase; Xie et al, 2021 ), ste7 (coding a MAP kinase kinase) and fus3 (coding a MAP kinase; Chen et al, 2021 ; Xie et al, 2023 ), hog1 (coding a MAP kinase; Kuo et al, 2020 ), and ime2 (coding a MAP kinase; Xie et al, 2020 ), which all participate in the development and pathogenicity of A. oligospora .…”