<scp>P</scp>hytophthora capsici homologue of the cell cycle regulator <scp>SDA1</scp> is required for sporangial morphology, mycelial growth and plant infection

Zhu, Chunyuan; Yang, Xiaoyan; Lv, Rong-Fei; Li, Zhuang; Ding, Xiaomeng; Tyler, Brett M.; Zhang, Xiuguo

doi:10.1111/mpp.12285

Cited by 15 publications

(7 citation statements)

References 64 publications

(97 reference statements)

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“…The expression levels of each CHS gene were determined by qRT-PCR using the primers listed in the Supporting Information Table S1. The P. capsici housekeeping genes Actin and β-tubulin, and the P. sojae housekeeping genes Actin and RpL13a, served as endogenous controls (Wang et al, 2011;Zhu et al, 2016).…”

Section: Rna-seq and Quantitative Real-time Pcrmentioning

confidence: 99%

Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora sojae

Wei

Lin

et al. 2019

Environmental Microbiology

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Summary Chitin is a structural and functional component of the fungal cell wall and also serves as a pathogen‐associated molecular pattern (PAMP) that triggers the innate immune responses of host plants. However, no or very little chitin is found in the fungus‐like oomycetes. In Phytophthora spp., the presence of chitin has not been demonstrated so far, although putative chitin synthase (CHS) genes, which encode the enzymes that synthesize chitin, are present in their genomes. Here, we revealed that chitin is present in the zoospores and released sporangia of Phytophthora, and this is most consistent with the transcriptional pattern of PcCHS in Phytophthora capsici and PsCHS1 in Phytophthora sojae. Disruption of the CHS genes indicated that PcCHS and PsCHS1, but not PsCHS2 (which exhibited very weak transcription), have similar functions involved in mycelial growth, sporangial production, zoospore release and the pathogenesis of P. capsici and P. sojae. We also suggest that chitin in the zoospores of P. capsici can act as a PAMP that is recognized by the chitin receptors AtLYK5 or AtCERK1 of Arabidopsis. These results provide new insights into the biological significance of chitin and CHSs in Phytophthora and help with the identification of potential targets for disease control.

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Section: Rna-seq and Quantitative Real-time Pcrmentioning

confidence: 99%

Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora sojae

Wei

Lin

et al. 2019

Environmental Microbiology

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“…Previous investigations proved that the cell cycle‐related genes PiCdc14 and PcSDA1 are associated with oomycete sporulation (Ah‐Fong and Judelson, ; Zhu et al , ). Consequently, we analysed the expression levels of PiCdc14 ( PITG_18578 ) and PiSDA1 ( PITG_18755 ; homolog of PcSDA1 in P. capsici ) in the STs and OTs.…”

Section: Resultsmentioning

confidence: 99%

“…In oomycetes, Cdc14 ‐silenced transformants are reportedly defective regarding sporangia production and development (Ah‐Fong and Judelson, ). Moreover, silencing and overexpressing PcSDA1 inhibited sporangiophore formation, sporangial development, zoospore release, cyst germination, and decreased pathogenicity (Zhu et al , ). In this study, the production of sporangia as well as the zoospore release rate and the sporangial germination rate were adversely affected in the STs and OTs, in which PiCdc14 expression levels decreased and PiSDA1 expression levels increased.…”

Section: Discussionmentioning

confidence: 99%

“…Many factors, such as nutrient availability, humidity, oxygen levels, and pH, affect the formation of sporangia and the production of zoospores in Phytophthora species (Erwin and Ribeiro, 1996). Previous studies revealed that many genes, including those encoding cell cycle regulators, PiCdc14 (Ah-Fong and Judelson, 2003) and PcSDA1 (Zhu et al, 2016), G protein β and γ subunits (Latijnhouwers and Govers, 2003;van den Hoogen et al, 2018), Myb and MADS-box transcription factors (Xiang and Judelson, 2014;Leesutthiphonchai and Judelson, 2018), and the loricrin-like protein PiLLP (Guo et al, 2017), are associated with the sporulation and pathogenicity of Phytophthora species. However, whether catalase activity affects the sporulation and pathogenicity of Phytophthora species remains unclear.…”

Section: Introductionmentioning

confidence: 99%

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A proper PiCAT2 level is critical for sporulation, sporangium function, and pathogenicity of Phytophthora infestans

Wang

Zhu

et al. 2020

Molecular Plant Pathology

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Catalase is present in prokaryotic and eukaryotic organisms and is important for the protective effects of the antioxidant system against free radicals. Many studies have confirmed that catalase is required for the growth, development, and pathogenesis of bacteria, plants, animals, and fungi. However, there has been relatively little research on the catalases in oomycetes, which form an important group of fungus‐like eukaryotes that produce zoosporangia. In this study, we detected two Phytophthora infestans genes encoding catalases, but only PiCAT2 exhibited catalase activity in the sporulation stage and was highly produced during asexual reproduction and in the late infection stage. Compared with the wild‐type strain, the PiCAT2‐silenced P. infestans transformants were more sensitive to abiotic stress, were less pathogenic, and had a lower colony expansion rate and lower PiMPK7, PiVPS1, and PiGPG1 expression levels. In contrast, the PiCAT2‐overexpressed transformants were slightly less sensitive to abiotic stress. Interestingly, increasing and decreasing PiCAT2 expression from the normal level inhibited sporulation, germination, and infectivity, and down‐regulated PiCdc14 expression, but up‐regulated PiSDA1 expression. These results suggest that PiCAT2 is required for P. infestans mycelial growth, asexual reproduction, abiotic stress tolerance, and pathogenicity. However, a proper PiCAT2 level is critical for the formation and normal function of sporangia. Furthermore, PiCAT2 affects P. infestans sporangial formation and function, pathogenicity, and abiotic stress tolerance by regulating the expression of cell cycle‐related genes (PiCdc14 and PiSDA1) and MAPK pathway genes. Our findings provide new insights into catalase functions in eukaryotic pathogens.

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“…Pioneering work based on staining methods revealed elongated nuclei, suggesting a potential movement in cysts of the diatom-infecting oomycete Lagenisma coscinodisci (24) as well as in hyphae and germinating cysts of P. infestans (25, 26). Similarly to fungi, oomycete nuclei are known to distribute equally within coenocytic (aseptate) hyphae, and this distribution is altered by the actin polymerization inhibitor latrunculin B (27–29) or by silencing the Phytophthora capsici cell cycle regulator homologue sda1 (30).…”

Section: Introductionmentioning

confidence: 99%

Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen

Evangelisti

Shenhav

Yunusov

et al. 2019

mBio

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Multinucleate fungi and oomycetes are phylogenetically distant but structurally similar. To address whether they share similar nuclear dynamics, we carried out time-lapse imaging of fluorescently labeled Phytophthora palmivora nuclei. Nuclei underwent coordinated bidirectional movements during plant infection. Within hyphal networks growing in planta or in axenic culture, nuclei either are dragged passively with the cytoplasm or actively become rerouted toward nucleus-depleted hyphal sections and often display a very stretched shape. Benomyl-induced depolymerization of microtubules reduced active movements and the occurrence of stretched nuclei. A centrosome protein localized at the leading end of stretched nuclei, suggesting that, as in fungi, astral microtubule-guided movements contribute to nuclear distribution within oomycete hyphae. The remarkable hydrodynamic shape adaptations of Phytophthora nuclei contrast with those in fungi and likely enable them to migrate over longer distances. Therefore, our work summarizes mechanisms which enable a near-equal nuclear distribution in an oomycete. We provide a basis for computational modeling of hydrodynamic nuclear deformation within branched tubular networks. IMPORTANCE Despite their fungal morphology, oomycetes constitute a distinct group of protists related to brown algae and diatoms. Many oomycetes are pathogens and cause diseases of plants, insects, mammals, and humans. Extensive efforts have been made to understand the molecular basis of oomycete infection, but durable protection against these pathogens is yet to be achieved. We use a plant-pathogenic oomycete to decipher a key physiological aspect of oomycete growth and infection. We show that oomycete nuclei travel actively and over long distances within hyphae and during infection. Such movements require microtubules anchored on the centrosome. Nuclei hydrodynamically adapt their shape to travel in or against the flow. In contrast, fungi lack a centrosome and have much less flexible nuclei. Our findings provide a basis for modeling of flexible nuclear shapes in branched hyphal networks and may help in finding hard-to-evade targets to develop specific antioomycete strategies and achieve durable crop disease protection.

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Phytophthora capsici homologue of the cell cycle regulator SDA1 is required for sporangial morphology, mycelial growth and plant infection

Cited by 15 publications

References 64 publications

Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora sojae

Chitin synthase is involved in vegetative growth, asexual reproduction and pathogenesis of Phytophthora capsici and Phytophthora sojae

A proper PiCAT2 level is critical for sporulation, sporangium function, and pathogenicity of Phytophthora infestans

Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen

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