Cellulose Synthesis in<i>Phytophthora infestans</i>Is Required for Normal Appressorium Formation and Successful Infection of Potato

Grenville‐Briggs, Laura J.; Anderson, Victoria; Fugelstad, Johanna; Avrova, Anna O.; Bouzenzana, Jamel; Williams, Alison S.; Wawra, Stephan; Whisson, Stephen C.; Birch, Paul R. J.; Bulone, Vincent; West, Pieter van

doi:10.1105/tpc.107.052043

Cited by 140 publications

(171 citation statements)

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“…Since the diploid nature of oomycetes hampers directed mutagenesis by gene disruption, we chose gene silencing as a method to obtain mutants. Gene silencing has been demonstrated in P. infestans and Phytophthora parasitica and was used for functional analysis of a few genes (7,20,22,52). For P. sojae, however, this is the first report describing successful silencing of a target gene.…”

Section: Discussionmentioning

confidence: 98%

A Phytophthora sojae G-Protein α Subunit Is Involved in Chemotaxis to Soybean Isoflavones

et al. 2008

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For the soybean pathogen Phytophthora sojae, chemotaxis of zoospores to isoflavones is believed to be critical for recognition of the host and for initiating infection. However, the molecular mechanisms underlying this chemotaxis are largely unknown. To investigate the role of G-protein and calcium signaling in chemotaxis, we analyzed the expression of several genes known to be involved in these pathways and selected one that was specifically expressed in sporangia and zoospores but not in mycelium. This gene, named PsGPA1, is a single-copy gene in P. sojae and encodes a G-protein ␣ subunit that shares 96% identity in amino acid sequence with that of Phytophthora infestans. To elucidate the function, expression of PsGPA1 was silenced by introducing antisense constructs into P. sojae. PsGPA1 silencing did not disturb hyphal growth or sporulation but severely affected zoospore behavior, including chemotaxis to the soybean isoflavone daidzein. Zoospore encystment and cyst germination were also altered, resulting in the inability of the PsGPA1-silenced mutants to infect soybean. In addition, the expressions of a calmodulin gene, PsCAM1, and two calcium-and calmodulin-dependent protein kinase genes, PsCMK3 and PsCMK4, were increased in the mutant zoospores, suggesting that PsGPA1 negatively regulates the calcium signaling pathways that are likely involved in zoospore chemotaxis.The ability to recognize host signals may be critical for the behavior of plant pathogens or symbionts. Chemotaxis to a host-specific signal has been described for several plant-microbe associations (11,43,44). In plant-pathogenic Agrobacterium species, for example, chemotaxis to plant exudates appears to enhance virulence on soil-grown plants (24). In nitrogen-fixing bacteria, such as Rhizobium and Bradyrhizobium species, expression of nodulation genes is induced by flavones and isoflavones (19), which are secondary metabolites present in seeds of leguminous plants and are exuded by the roots of those plants. Chemotaxis of zoospores of the oomycete pathogen Phytophthora sojae to isoflavones is believed to be an important step in the disease cycle, particularly in recognition of the host and in initiating infection (42,43). P. sojae is a devastating pathogen on soybean that causes "damping off" of seedlings and root rot on older plants. The annual loss worldwide is estimated to be $1 billion to $2 billion (49).P. sojae zoospores are specifically attracted to the isoflavones daidzein and genistein at concentrations of as low as 10 nM (43). Since zoospores of other Phytophthora spp. are not attracted to these compounds, chemotaxis may be part of the mechanism that determines host range (43). Besides motile zoospores, hyphal germ tubes of P. sojae also respond chemotropically to soybean isoflavones (42, 51). Although there are indications that calcium influx plays a role in chemotaxis (12), the signal transduction pathways governing the response of P. sojae to isoflavones are largely unknown. The first step in unraveling these pathways is identif...

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Section: Discussionmentioning

confidence: 98%

A Phytophthora sojae G-Protein α Subunit Is Involved in Chemotaxis to Soybean Isoflavones

et al. 2008

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“…In the case of the latter, a single construct was made that was expected to silence PITG_09190, PITG_09198, PITG_09199, PITG_09200, and PITG_09201, since these exhibit about 96% sequence identity. Two prior studies in P. infestans have shown that single constructs can silence closely related genes (50,51).…”

Section: Resultsmentioning

confidence: 99%

bZIP Transcription Factors in the Oomycete Phytophthora infestans with Novel DNA-Binding Domains Are Involved in Defense against Oxidative Stress

2013

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Transcription factors of the basic leucine zipper (bZIP) family control development and stress responses in eukaryotes. To date, only one bZIP has been described in any oomycete; oomycetes are members of the stramenopile kingdom. In this study, we describe the identification of 38 bZIPs from the Phytophthora infestans genome. Half contain novel substitutions in the DNAbinding domain at a site that in other eukaryotes is reported to always be Asn. Interspecific comparisons indicated that the novel substitutions (usually Cys, but also Val and Tyr) arose after oomycetes diverged from other stramenopiles. About two-thirds of P. infestans bZIPs show dynamic changes in mRNA levels during the life cycle, with many of the genes being upregulated in sporangia, zoospores, or germinated zoospore cysts. One bZIP with the novel Cys substitution was shown to reside in the nucleus throughout growth and development. Using stable gene silencing, the functions of eight bZIPs with the Cys substitution were tested. All but one were found to play roles in protecting P. infestans from hydrogen peroxide-induced injury, and it is proposed that the novel Cys substitution serves as a redox sensor. A ninth bZIP lacking the novel Asn-to-Cys substitution, but having Cys nearby, was also shown through silencing to contribute to defense against peroxide. Little effect on asexual development, plant pathogenesis, or resistance to osmotic stress was observed in transformants silenced for any of the nine bZIPs.

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“…A feature usually mentioned when distinguishing oomycetes from true fungi is the presence of cellulose and the absence of chitin in their cell wall (40). This assumption stems from early studies mainly focused on the Phytophthora cell wall (6,7) and was recently reinforced by the demonstration that cellulose synthesis is required for normal appressorium formation in Phytophthora infestans (37). However, the cell wall of the closely related hyphochytridiomycetes contains both cellulose and chitin, and chitin was unambiguously detected by biophysical analyses in some oomycete species of the Leptomitale and Saprolegniale orders (2,12).…”

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confidence: 96%

Cell Wall Chitosaccharides Are Essential Components and Exposed Patterns of the Phytopathogenic OomyceteAphanomyces euteiches

et al. 2008

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Chitin is an essential component of fungal cell walls, where it forms a crystalline scaffold, and chitooligosaccharides derived from it are signaling molecules recognized by the hosts of pathogenic fungi. Oomycetes are cellulosic fungus-like microorganisms which most often lack chitin in their cell walls. Here we present the first study of the cell wall of the oomycete Aphanomyces euteiches, a major parasite of legume plants. Biochemical analyses demonstrated the presence of ca. 10% N-acetyl-D-glucosamine (GlcNAc) in the cell wall. Further characterization of the GlcNAc-containing material revealed that it corresponds to noncrystalline chitosaccharides associated with glucans, rather than to chitin per se. Two putative chitin synthase (CHS) genes were identified by data mining of an A. euteiches expressed sequence tag collection and Southern blot analysis, and full-length cDNA sequences of both genes were obtained. Phylogeny analysis indicated that oomycete CHS diversification occurred before the divergence of the major oomycete lineages. Remarkably, lectin labeling showed that the Aphanomyces euteiches chitosaccharides are exposed at the cell wall surface, and study of the effect of the CHS inhibitor nikkomycin Z demonstrated that they are involved in cell wall function. These data open new perspectives for the development of antioomycete drugs and further studies of the molecular mechanisms involved in the recognition of pathogenic oomycetes by the host plants.

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Cellulose Synthesis inPhytophthora infestansIs Required for Normal Appressorium Formation and Successful Infection of Potato

Cited by 140 publications

References 63 publications

A Phytophthora sojae G-Protein α Subunit Is Involved in Chemotaxis to Soybean Isoflavones

A Phytophthora sojae G-Protein α Subunit Is Involved in Chemotaxis to Soybean Isoflavones

bZIP Transcription Factors in the Oomycete Phytophthora infestans with Novel DNA-Binding Domains Are Involved in Defense against Oxidative Stress

Cell Wall Chitosaccharides Are Essential Components and Exposed Patterns of the Phytopathogenic OomyceteAphanomyces euteiches

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