A Gene Expressed during Sexual and Asexual Sporulation in
            <i>Phytophthora infestans</i>
            Is a Member of the Puf Family of Translational Regulators

Cvitanich, Cristina; Judelson, Howard S.

doi:10.1128/ec.2.3.465-473.2003

Cited by 36 publications

(30 citation statements)

References 36 publications

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“…That M96 is expressed relatively late during mating was indicated by comparisons with mating-induced gene M90 (Cvitanich and Judelson 2003). Based on hybridizations against the same blots, M96 expression peaked after M90 (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Concerted evolution of a tandemly arrayed family of mating-specific genes in Phytophthora analyzed through inter- and intraspecific comparisons

2005

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Multigene families are features of most eukaryotic genomes, which evolve through a variety of mechanisms. This study describes the structure, expression, and evolution of a novel family in the oomycete Phytophthora. In the heterothallic species P. infestans, M96 is expressed specifically during sexual sporogenesis, and encodes a low-complexity extracellular protein that may be a component of oospore walls. Intriguingly, M96 exists in P. infestans as 22 relatively homogeneous loci tandemly repeated at a single site, which is partitioned by inversions and retroelements into subclusters exhibiting semi-independent evolution. M96 relatives were detected in other heterothallic and homothallic oomycetes including species closely (P. mirabilis, P. phaseoli) or distantly (P. ramorum, P. sojae) related to P. infestans. Those M96 relatives also exhibit oosporogenesis-specific expression and are arrayed multigene families. Nucleotide changes and repeat expansion diversify M96 in each species, however, paralogues are more related than orthologues. Concerted evolution through gene conversion and not strong purifying selection appears to be the major contributor to intraspecific homogenization. Divergence and concerted evolution was also detected between isolates of P. infestans. The divergence of M96 proteins between P. infestans, P. ramorum, and P. sojae exceeds that of typical proteins, reflecting trends in reproductive proteins from other kingdoms.

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Section: Resultsmentioning

confidence: 99%

“…Mating, carbon or nitrogen-starved, and nonmating cultures were as described (Judelson and Roberts 2002;Cvitanich and Judelson 2003). Tissue low in oospores from the homothallics (strain 6.11 and P. phaseoli) was obtained by growing hyphae submerged in clarified rye broth.…”

Section: Methodsmentioning

confidence: 99%

Concerted evolution of a tandemly arrayed family of mating-specific genes in Phytophthora analyzed through inter- and intraspecific comparisons

2005

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“…Previous RNA blot analyses from our laboratory indicated that traditional standards, such as actin and EF1, varied relative to rRNA in sporangia versus hyphae and thus would be inappropriate for normalization (10). Levels of EF1 were lower in sporangia than in hyphae, for example (Fig.…”

Section: Identification Of Genes Up-regulated In Asexual Sporangiamentioning

confidence: 99%

Sporangium-Specific Gene Expression in theOomycete Phytopathogen Phytophthorainfestans

Kim

Judelson

2003

Eukaryot Cell

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The oomycete genus Phytophthora includes many of the world's most destructive plant pathogens, which are generally disseminated by asexual sporangia. To identify factors relevant to the biology of these propagules, genes induced in sporangia of the potato late blight pathogen Phytophthora infestans were isolated using cDNA macroarrays. Of ϳ1,900 genes known to be expressed in sporangia, 61 were up-regulated >5-fold in sporangia versus hyphae based on the arrays, including 17 that were induced >100-fold. A subset were also activated by starvation and in a nonsporulating mutant. mRNAs of some genes declined in abundance after germination, while others persisted through the germinated zoospore cyst stage. Functions were predicted for about three-quarters of the genes, including potential regulators (protein kinases and phosphatases, transcription factors, and G-protein subunits), transporters, and metabolic enzymes. Predominant among the last were several dehydrogenases, especially a highly expressed sorbitol dehydrogenase that accounted for 3% of the mRNA. Sorbitol dehydrogenase activity also rose during sporulation and several stress treatments, paralleling the expression of the gene. Another interesting metabolic enzyme resembled creatine kinases, which previously were reported only in animals and trypanosomes. These results provide insight into the transcriptional and cellular processes occurring in sporangia and identify potential targets for crop protection strategies.Sporulation is central to the life cycles of most plant-pathogenic lower eukaryotes, including true fungi and oomycetes. The latter group encompasses important pathogens, such as Phytophthora, Pythium, and the downy mildews, which infect many economically significant hosts (14). The molecular biology of sporulation has been characterized in detail for several true fungi (1,11,28,43). However, little information exists on oomycetes, which despite their "fungus-like" appearance are more closely related to organisms such as diatoms and brown algae (3).Asexual sporangia play the major role in spreading Phytophthora infestans, which causes late blight of potato and tomato (17). The roles of nutrients, pH, aeration, light, and humidity in sporulation are well described (33,41). In older portions of plant lesions and in laboratory cultures, sporangia form upon aerial sporangiophores branched from hyphae. In some members of the genus, such as P. infestans, this occurs spontaneously as cultures age, but in others significant sporulation requires washing nutrients from media (41). In both cases, nuclear divisions rapidly occur within sporangiophores, and then nuclei and cytoplasm quickly flow into terminal swellings, which develop into sporangia (7, 32). These mature by forming a basal plug, which delimits the multinucleate sporangium from the coenocytic hypha, and an apical papilla, which is a future site of germination. Two modes of germination are possible in most oomycetes, including P. infestans. Indirect germination by way of zoospores predominates ...

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“…Stable transformants were obtained using a protoplast method and stained histochemically for ␤-glucuronidase (GUS) activity (24). This involved derivatives of pOGUS (14) into which wild-type or mutagenized portions of the PinifC1, PinifC3, and M82 promoters were inserted into the ApaI and ClaI sites upstream of GUS. pOGUS also contains an npt gene for G418 selection.…”

Section: Methodsmentioning

confidence: 99%

Activation of Zoosporogenesis-Specific Genes in Phytophthora infestans Involves a 7-Nucleotide Promoter Motif and Cold-Induced Membrane Rigidity

Tani

Judelson

2006

Eukaryot Cell

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Infections of plants by the oomycete Phytophthora infestans typically result from zoospores, which develop from sporangia at cold temperatures. To help understand the relevant cold-induced signaling pathway, factors regulating the transcription of the zoosporogenesis-specific NIF (nuclear LIM-interactor-interacting factor) gene family were examined. Sequences required for inducing PinifC3 were identified by analyzing truncated and mutated promoters using the ␤-glucuronidase reporter in stable transformants. A 7-nucleotide (nt) sequence located 139 bases upstream of the major transcription start point (GGACGAG) proved essential for the induction of PinifC3 when sporangia were shifted from ambient to cold temperatures. The motif, named the cold box, also conferred cold inducibility to a promoter normally activated only during sexual development. An identical motif was detected in the two other zoosporogenesis-specific NIF genes from P. infestans and three Phytophthora sojae orthologues, and a closely related sequence was found in Phytophthora ramorum orthologues. The 7-nt motif was also found in the promoters of other zoosporogenesis-induced genes. The presence of a cold box-interacting protein in nuclear extracts of P. infestans sporangia was demonstrated using electrophoretic mobility shift assays. Furthermore, zoospore release and cold box-regulated transcription were stimulated by the membrane rigidizer dimethyl sulfoxide and inhibited by the membrane fluidizer benzyl alcohol. The data therefore delineate a pathway in which sporangia perceive cold temperatures through membrane rigidity, which activates signals that drive both zoosporogenesis and cold-box-mediated transcription.

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A Gene Expressed during Sexual and Asexual Sporulation in Phytophthora infestans Is a Member of the Puf Family of Translational Regulators

Cited by 36 publications

References 36 publications

Concerted evolution of a tandemly arrayed family of mating-specific genes in Phytophthora analyzed through inter- and intraspecific comparisons

Concerted evolution of a tandemly arrayed family of mating-specific genes in Phytophthora analyzed through inter- and intraspecific comparisons

Sporangium-Specific Gene Expression in theOomycete Phytopathogen Phytophthorainfestans

Activation of Zoosporogenesis-Specific Genes in Phytophthora infestans Involves a 7-Nucleotide Promoter Motif and Cold-Induced Membrane Rigidity

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