The Mitogen-Activated Protein Kinase BcSak1 of <i>Botrytis cinerea</i> Is Required for Pathogenic Development and Has Broad Regulatory Functions Beyond Stress Response

Heller, Jens; Ruhnke, Nadja; Espino, José J.; Massaroli, Michelli; Collado, Isidro G.; Tudzynski, Paul

doi:10.1094/mpmi-11-11-0299

Cited by 57 publications

(59 citation statements)

References 77 publications

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“…Deletion of this gene constitutively activates the BcSak1 module and leads to sensitivity to hydrogen peroxide and osmotic stress, fungicide tolerance, reduced production of macroconidia, increased pigmentation, and impaired virulence (25,26). As expected, the lack of bcsak1 (and likewise the upstream kinases Bos4 and Bos5) affects the same parameters as deletion of bos1, apart from the resistance against fungicides (26,30,75,77,86,87). The response regulator Brrg1 seems to be necessary for the activation of BcSak1 as the MAPK is not phosphorylated in mutants lacking brrg1.…”

Section: Regulatory Functions Of Bap1 Andmentioning

confidence: 57%

Unraveling the Function of the Response Regulator BcSkn7 in the Stress Signaling Network of Botrytis cinerea

et al. 2015

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Important for the lifestyle and survival of every organism is the ability to respond to changing environmental conditions. The necrotrophic plant pathogen Botrytis cinerea triggers an oxidative burst in the course of plant infection and therefore needs efficient signal transduction to cope with this stress. The factors involved in this process and their precise roles are still not well known. Here, we show that the transcription factor Bap1 and the response regulator (RR) B. cinerea Skn7 (BcSkn7) are two key players in the oxidative stress response (OSR) of B. cinerea; both have a major influence on the regulation of classical OSR genes. A yeast-one-hybrid (Y1H) approach proved direct binding to the promoters of gsh1 and grx1 by Bap1 and of glr1 by BcSkn7. While the function of Bap1 is restricted to the regulation of oxidative stress, analyses of ⌬bcskn7 mutants revealed functions beyond the OSR. Involvement of BcSkn7 in development and virulence could be demonstrated, indicated by reduced vegetative growth, impaired formation of reproductive structures, and reduced infection cushion-mediated penetration of the host by the mutants. Furthermore, ⌬bcskn7 mutants were highly sensitive to oxidative, osmotic, and cell wall stress. Analyses of ⌬bap1 bcskn7 double mutants indicated that loss of BcSkn7 uncovers an underlying phenotype of Bap1. In contrast to Saccharomyces cerevisiae, the ortholog of the glutathione peroxidase Gpx3p is not required for nuclear translocation of Bap1. The presented results contribute to the understanding of the OSR in B. cinerea and prove that it differs substantially from that of yeast, demonstrating the complexity and versatility of components involved in signaling pathways.

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Section: Regulatory Functions Of Bap1 Andmentioning

confidence: 57%

Unraveling the Function of the Response Regulator BcSkn7 in the Stress Signaling Network of Botrytis cinerea

et al. 2015

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“…bcbop1, Opsin-1; bccat2, catalase 2; bctrr, thioredoxin reductase; bcddr48, stress protein. bcbop1, bccat2, and bcddr48 are under the control of BcSAK1 (6,41), and bctrr is regulated by the transcription factor BcBAP1 (40).…”

Section: Figmentioning

confidence: 99%

Involvement of Botrytis cinerea Small GTPases BcRAS1 and BcRAC in Differentiation, Virulence, and the Cell Cycle

et al. 2013

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bSmall GTPases of the Ras superfamily are highly conserved proteins that are involved in various cellular processes, in particular morphogenesis, differentiation, and polar growth. Here we report on the analysis of RAS1 and RAC homologues from the gray mold fungus Botrytis cinerea. We show that these small GTPases are individually necessary for polar growth, reproduction, and pathogenicity, required for cell cycle progression through mitosis (BcRAC), and may lie upstream of the stress-related mitogenactivated protein kinase (MAPK) signaling pathway. bcras1 and bcrac deletion strains had reduced growth rates, and their hyphae were hyperbranched and deformed. In addition, both strains were vegetatively sterile and nonpathogenic. A strain expressing a constitutively active (CA) allele of the BcRAC protein had partially similar but milder phenotypes. Similar to the deletion strains, the CA-BcRAC strain did not produce any conidia and had swollen hyphae. In contrast to the two deletion strains, however, the growth rate of the CA-BcRAC strain was normal, and it caused delayed but well-developed disease symptoms. Microscopic examination revealed an increased number of nuclei and disturbance of actin localization in the CA-BcRAC strain. Further work with cell cycle-and RAC-specific inhibitory compounds associated the BcRAC protein with progression of the cell cycle through mitosis, possibly via an effect on microtubules. Together, these results show that the multinucleate phenotype of the CA-BcRAC strain could result from at least two defects: disruption of polar growth through disturbed actin localization and uncontrolled nuclear division due to constitutive activity of BcRAC.

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“…SakA was also identified as HogA (26) and together with AtfA was shown to be involved in gene regulation in response to osmotic stress (27). In many other filamentous fungi, SakA orthologs have been found to be involved in osmotic and/or oxidative-stress resistance and the regulation of development and/or pathogenicity (28)(29)(30)(31)(32). A. nidulans sakA-null mutants also show premature sexual development and produce asexual spores (conidia) that progressively lose their viability (24,25).…”

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The SrkA Kinase Is Part of the SakA Mitogen-Activated Protein Kinase Interactome and Regulates Stress Responses and Development in Aspergillus nidulans

et al. 2015

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cFungi and many other eukaryotes use specialized mitogen-activated protein kinases (MAPK) of the Hog1/p38 family to transduce environmental stress signals. In Aspergillus nidulans, the MAPK SakA and the transcription factor AtfA are components of a central multiple stress-signaling pathway that also regulates development. Here we characterize SrkA, a putative MAPK-activated protein kinase, as a novel component of this pathway. ⌬srkA and ⌬sakA mutants share a derepressed sexual development phenotype. However, ⌬srkA mutants are not sensitive to oxidative stress, and in fact, srkA inactivation partially suppresses the sensitivity of ⌬sakA mutant conidia to H 2 O 2 , tert-butyl-hydroperoxide (t-BOOH), and menadione. In the absence of stress, SrkA shows physical interaction with nonphosphorylated SakA in the cytosol. We show that H 2 O 2 induces a drastic change in mitochondrial morphology consistent with a fission process and the relocalization of SrkA to nuclei and mitochondria, depending on the presence of SakA. SakA-SrkA nuclear interaction is also observed during normal asexual development in dormant spores. Using SakA and SrkA S-tag pulldown and purification studies coupled to mass spectrometry, we found that SakA interacts with SrkA, the stress MAPK MpkC, the PPT1-type phosphatase AN6892, and other proteins involved in cell cycle regulation, DNA damage response, mRNA stability and protein synthesis, mitochondrial function, and other stress-related responses. We propose that oxidative stress induces DNA damage and mitochondrial fission and that SakA and SrkA mediate cell cycle arrest and regulate mitochondrial function during stress. Our results provide new insights into the mechanisms by which SakA and SrkA regulate the remodelling of cell physiology during oxidative stress and development. W e have proposed that when life was confronted with oxidative stress, cells evolved mechanisms not only to defend against reactive oxygen species (ROS) but also to use this ancestral form of stress to regulate their own growth and differentiation (1, 2). Indeed, the regulated production of ROS by enzymes of the NADPH oxidase family (NOX) is essential for sexual differentiation in Aspergillus nidulans (3) and Neurospora crassa and for polar growth and cell fusion in N. crassa (4), and NOX enzymes play multiple signaling functions in other fungal (5-10), animal, and plant species (11). However, little is known about ROS perception and the mechanisms by which ROS exert their signaling functions.The use of phosphorelay systems to perceive oxidative stress and other types of environmental stress is conserved in bacteria, plants (12), and fungi (13). The fission yeast Schizosaccharomyces pombe uses a multistep phosphorelay composed of the Mak2/3 sensor histidine kinases, Mpr1 HPt protein, and Mcs4 response regulator to transmit H 2 O 2 stress signals to the Spc1 (also known as StyI) mitogen-activated protein kinase (MAPK) cascade (14,15). Spc1 is homologous to Saccharomyces cerevisiae Hog1 and mammalian p38 MAPKs, which are also...

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The Mitogen-Activated Protein Kinase BcSak1 of Botrytis cinerea Is Required for Pathogenic Development and Has Broad Regulatory Functions Beyond Stress Response

Cited by 57 publications

References 77 publications

Unraveling the Function of the Response Regulator BcSkn7 in the Stress Signaling Network of Botrytis cinerea

Unraveling the Function of the Response Regulator BcSkn7 in the Stress Signaling Network of Botrytis cinerea

Involvement of Botrytis cinerea Small GTPases BcRAS1 and BcRAC in Differentiation, Virulence, and the Cell Cycle

The SrkA Kinase Is Part of the SakA Mitogen-Activated Protein Kinase Interactome and Regulates Stress Responses and Development in Aspergillus nidulans

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