Dataset Information

Transcriptomic Analysis Reveals Genes Mediating Salt Tolerance through Calcineurin/CchA-Independent Signaling in Aspergillus nidulans.

ABSTRACT: Adaptation to changes in the environment is crucial for the viability of all organisms. Although the importance of calcineurin in the stress response has been highlighted in filamentous fungi, little is known about the involvement of ion-responsive genes and pathways in conferring salt tolerance without calcium signaling. In this study, high-throughput RNA-seq was used to investigate salt stress-induced genes in the parent, ?cnaB, and ?cnaB?cchA strains of Aspergillus nidulans, which differ greatly in salt adaption. In total, 2,884 differentially expressed genes including 1,382 up- and 1,502 downregulated genes were identified. Secondary transporters, which were upregulated to a greater extent in ?cnaB?cchA than in the parent or ?cnaB strains, are likely to play important roles in response to salt stress. Furthermore, 36 genes were exclusively upregulated in the ?cnaB?cchA under salt stress. Functional analysis of differentially expressed genes revealed that genes involved in transport, heat shock protein binding, and cell division processes were exclusively activated in ?cnaB?cchA. Overall, our findings reveal that secondary transporters and stress-responsive genes may play crucial roles in salt tolerance to bypass the requirement for the CchA-calcineurin pathway, contributing to a deeper understanding of the mechanisms that influence fungal salt stress adaption in Aspergillus.

SUBMITTER: Wang S

PROVIDER: S-EPMC5585587 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Transcriptomic Analysis Reveals Genes Mediating Salt Tolerance through Calcineurin/CchA-Independent Signaling in Aspergillus nidulans.

Wang Sha S Zhou Hongchang H Wu Jun J Han Jiangyu J Li Shasha S Shao Shengwen S

BioMed research international 20170820

Adaptation to changes in the environment is crucial for the viability of all organisms. Although the importance of calcineurin in the stress response has been highlighted in filamentous fungi, little is known about the involvement of ion-responsive genes and pathways in conferring salt tolerance without calcium signaling. In this study, high-throughput RNA-seq was used to investigate salt stress-induced genes in the parent, ΔcnaB, and ΔcnaBΔcchA strains of Aspergillus nid ...[more]

PMID: 28904958

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Project description:The eukaryotic calcium/calmodulin-dependent protein phosphatase calcineurin is crucial for the environmental adaption of fungi. However, the mechanism of coordinate regulation of the response to salt stress by calcineurin and the high-affinity calcium channel CchA in fungi is not well understood. Here we show that the deletion of cchA suppresses the hyphal growth defects caused by the loss of calcineurin under salt stress in Aspergillus nidulans Additionally, the hypersensitivity of the ?cnaA strain to extracellular calcium and cell-wall-damaging agents can be suppressed by cchA deletion. Using the calcium-sensitive photoprotein aequorin to monitor the cytoplasmic Ca(2+) concentration ([Ca(2+)]c) in living cells, we found that calcineurin negatively regulates CchA on calcium uptake in response to external calcium in normally cultured cells. However, in salt-stress-pretreated cells, loss of either cnaA or cchA significantly decreased the [Ca(2+)]c, but a deficiency in both cnaA and cchA switches the [Ca(2+)]c to the reference strain level, indicating that calcineurin and CchA synergistically coordinate calcium influx under salt stress. Moreover, real-time PCR results showed that the dysfunction of cchA in the ?cnaA strain dramatically restored the expression of enaA (a major determinant for sodium detoxification), which was abolished in the ?cnaA strain under salt stress. These results suggest that double deficiencies of cnaA and cchA could bypass the requirement of calcineurin to induce enaA expression under salt stress. Finally, YvcA, a member of the transient receptor potential channel (TRPC) protein family of vacuolar Ca(2+) channels, was proven to compensate for calcineurin-CchA in fungal salt stress adaption.IMPORTANCE The feedback inhibition relationship between calcineurin and the calcium channel Cch1/Mid1 has been well recognized from yeast. Interestingly, our previous study (S. Wang et al., PLoS One 7:e46564, 2012, http://dx.doi.org/10.1371/journal.pone.0046564) showed that the deletion of cchA could suppress the hyphal growth defects caused by the loss of calcineurin under salt stress in Aspergillus nidulans In this study, our findings suggest that fungi are able to develop a unique mechanism for adapting to environmental salt stress. Compared to cells cultured normally, the NaCl-pretreated cells had a remarkable increase in transient [Ca(2+)]c Furthermore, we show that calcineurin and CchA are required to modulate cellular calcium levels and synergistically coordinate calcium influx under salt stress. Finally, YvcA, a member of of the TRPC family of vacuolar Ca(2+) channels, was proven to compensate for calcineurin-CchA in fungal salt stress adaption. The findings in this study provide insights into the complex regulatory links between calcineurin and CchA to maintain cytoplasmic Ca(2+) homeostasis in response to different environments.

Project description:Considering the complex nature of salinity tolerance mechanisms, the use of isogenic lines or mutants possessing the same genetic background albeit different tolerance to salinity is a suitable method for reduction of analytical complexity to study these mechanisms. In the present study, whole transcriptome analysis was evaluated using RNA-seq method between a salt-tolerant mutant line "M4-73-30" and its wild-type "Zarjou" cultivar at seedling stage after six hours of exposure to salt stress (300 mM NaCl). Transcriptome sequencing yielded 20 million reads for each genotype. A total number of 7116 transcripts with differential expression were identified, 1586 and 1479 of which were obtained with significantly increased expression in the mutant and the wild-type, respectively. In addition, the families of WRKY, ERF, AP2/EREBP, NAC, CTR/DRE, AP2/ERF, MAD, MIKC, HSF, and bZIP were identified as the important transcription factors with specific expression in the mutant genotype. The RNA-seq results were confirmed at several time points using qRT-PCR for some important salt-responsive genes. In general, the results revealed that the mutant accumulated higher levels of sodium ion in the root and decreased its transfer to the shoot. Also, the mutant increased the amount of potassium ion leading to the maintenance a high ratio [K+]/[Na+] in the shoot compared to its wild-type via fast stomata closure and consequently transpiration reduction under the salt stress. Moreover, a reduction in photosynthesis and respiration was observed in the mutant, resulting in utilization of the stored energy and the carbon for maintaining the plant tissues, which is considered as a mechanism of salt tolerance in plants. Up-regulation of catalase, peroxidase, and ascorbate peroxidase genes has resulted in higher accumulation of H2O2 in the wild-type compared to the mutant. Therefore, the wild-type initiated rapid ROS signals which led to less oxidative scavenging in comparison with the mutant. The mutant increased expression in the ion transporters and the channels related to the salinity to maintain the ion homeostasis. In overall, the results demonstrated that the mutant responded better to the salt stress under both osmotic and ionic stress phases and lower damage was observed in the mutant compared to its wild-type under the salt stress.

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Transcriptomic Analysis Reveals Genes Mediating Salt Tolerance through Calcineurin/CchA-Independent Signaling in Aspergillus nidulans.

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Transcriptomic Analysis Reveals Genes Mediating Salt Tolerance through Calcineurin/CchA-Independent Signaling in <i>Aspergillus nidulans</i>.

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