The small GTPase BcCdc42 affects nuclear division, germination and virulence of the gray mold fungus Botrytis cinerea

Kokkelink, Leonie; Minz, Anna; Al-Masri, Muhamad; Giesbert, Sabine; Barakat, Radwan; Sharon, Amir; Tudzynski, Paul

doi:10.1016/j.fgb.2011.07.007

Cited by 34 publications

(26 citation statements)

References 42 publications

(54 reference statements)

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“…Previously, synchronous division of individual nuclei in germinating B. cinerea conidia has been observed, using a B. cinerea strain with GFP-expressing nuclei (33). An explanation for this discrepancy from our result is difficult, but it might be related to the different surfaces used, namely, untreated glass slides in the work of Kokkelink et al (33) and apple wax-coated surfaces in our study, resulting in germination kinetics that differed by more than 1 h (Fig. 2).…”

Section: Discussionmentioning

confidence: 99%

“…The MAPK cascade ste11, ste7, bmp1, and ste50 mutants did not form appressoria on hard surfaces, they failed to penetrate into host tissue, and they were nonpathogenic (27,30). Other signaling elements found to be involved in germination are the small GTPase Cdc42 and phospholipase C (Plc1) (33). Taken together, these findings show that germination induction is a complex process involving several signaling pathways which is currently not fully understood.…”

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confidence: 95%

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Transcriptome Profiling of Botrytis cinerea Conidial Germination Reveals Upregulation of Infection-Related Genes during the Prepenetration Stage

et al. 2013

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Botrytis cinerea causes gray mold on a great number of host plants. Infection is initiated by airborne conidia that invade the host tissue, often by penetration of intact epidermal cells. To mimic the surface properties of natural plant surfaces, conidia were incubated on apple wax-coated surfaces, resulting in rapid germination and appressorium formation. Global changes in gene expression were analyzed by microarray hybridization between conidia incubated for 0 h (dormant), 1 h (pregermination), 2.5 h (postgermination), 4 h (appressoria), and 15 h (early mycelium). Considerable changes were observed, in particular between 0 h and 1 h. Genes induced during germination were enriched in those genes encoding secreted proteins, including lytic enzymes. Comparison of wild-type and a nonpathogenic MAP kinase mutant (bmp1) revealed marked differences in germination-related gene expression, in particular related to secretory proteins. Using promoter-GFP reporter strains, we detected a strictly germination-specific expression pattern of a putative chitin deacetylase gene (cda1). In contrast, a cutinase gene (cutB) was found to be expressed only in the presence of plant lipids, in a developmentally less stringent pattern. We also identified a coregulated gene cluster possibly involved in secondary metabolite synthesis which was found to be controlled by a transcription factor also encoded in this cluster. Our data demonstrate that early conidial development in B. cinerea is accompanied by rapid shifts in gene expression that prepare the fungus for germ tube outgrowth and host cell invasion.

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Section: Discussionmentioning

confidence: 99%

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confidence: 95%

Transcriptome Profiling of Botrytis cinerea Conidial Germination Reveals Upregulation of Infection-Related Genes during the Prepenetration Stage

et al. 2013

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“…None of the transgenic strains produced conidia, and therefore the putative roles of BcRAS1 and BcRAC in germination could not be studied in these strains. To address this question, we therefore used a strain that expresses H1-GFP, in which nuclei can be followed by fluorescence microscopy (38). First, we treated conidia of the H1-GFP strain with cell cycle-and RAC-inhibiting compounds and determined the effects on germination and division of nuclei.…”

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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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“…In fungi, highly conserved members of the Rho-GTPase family, Cdc42 and Rac1, are crucial for establishing and maintaining polarity during filament formation and budding (7)(8)(9)(10). The importance of Rac homologues in comparison with Cdc42 homologues seems to increase with the developmental complexity of the fungal species (10)(11)(12)(13)(14). In C. purpurea, the two GTPases show overlapping and differing functions.…”

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Small-GTPase-Associated Signaling by the Guanine Nucleotide Exchange Factors CpDock180 and CpCdc24, the GTPase Effector CpSte20, and the Scaffold Protein CpBem1 in Claviceps purpurea

et al. 2014

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bMonomeric GTPases of the Rho subfamily are important mediators of polar growth and NADPH (Nox) signaling in a variety of organisms. These pathways influence the ability of Claviceps purpurea to infect host plants. GTPase regulators contribute to the nucleotide loading cycle that is essential for proper functionality of the GTPases. Scaffold proteins gather GTPase complexes to facilitate proper function. The guanine nucleotide exchange factors (GEFs) CpCdc24 and CpDock180 activate GTPase signaling by triggering nucleotide exchange of the GTPases. Here we show that CpCdc24 harbors nucleotide exchange activity for both Rac and Cdc42 homologues. The GEFs partly share the cellular distribution of the GTPases and interact with the putative upstream GTPase CpRas1. Interaction studies show the formation of higher-order protein complexes, mediated by the scaffold protein CpBem1. Besides the GTPases and GEFs, these complexes also contain the GTPase effectors CpSte20 and CpCla4, as well as the regulatory protein CpNoxR. Functional characterizations suggest a role of CpCdc24 mainly in polarity, whereas CpDock180 is involved in stress tolerance mechanisms. These findings indicate the dynamic formation of small GTPase complexes and improve the model for GTPase-associated signaling in C. purpurea.

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The small GTPase BcCdc42 affects nuclear division, germination and virulence of the gray mold fungus Botrytis cinerea

Cited by 34 publications

References 42 publications

Transcriptome Profiling of Botrytis cinerea Conidial Germination Reveals Upregulation of Infection-Related Genes during the Prepenetration Stage

Transcriptome Profiling of Botrytis cinerea Conidial Germination Reveals Upregulation of Infection-Related Genes during the Prepenetration Stage

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

Small-GTPase-Associated Signaling by the Guanine Nucleotide Exchange Factors CpDock180 and CpCdc24, the GTPase Effector CpSte20, and the Scaffold Protein CpBem1 in Claviceps purpurea

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