SCR96, a small cysteine‐rich secretory protein of Phytophthora cactorum, can trigger cell death in the Solanaceae and is important for pathogenicity and oxidative stress tolerance

Abstract

Peptides and small molecules produced by both the plant pathogen Phytophthora and host plants in the apoplastic space mediate the relationship between the interplaying organisms. Various Phytophthora apoplastic effectors, including small cysteine-rich (SCR) secretory proteins, have been identified, but their roles during interaction remain to be determined. Here, we identified an SCR effector encoded by scr96, one of three novel genes encoding SCR proteins in P. cactorum with similarity to the P. cactorum phytotoxic protein PcF. Together with the other two genes, scr96 was transcriptionally induced throughout the developmental and infection stages of the pathogen. These genes triggered plant cell death (PCD) in the Solanaceae, including Nicotiana benthamiana and tomato. The scr96 gene did not show single nucleotide polymorphisms in a collection of P. cactorum isolates from different countries and host plants, suggesting that its role is essential and non-redundant during infection. Homologues of SCR96 were identified only in oomycetes, but not in fungi and other organisms. A stable protoplast transformation protocol was adapted for P. cactorum using green fluorescent protein as a marker. The silencing of scr96 in P. cactorum caused gene-silenced transformants to lose their pathogenicity on host plants and these transformants were significantly more sensitive to oxidative stress. Transient expression of scr96 partially recovered the virulence of gene-silenced transformants on plants. Overall, our results indicate that the P. cactorum scr96 gene encodes an important virulence factor that not only causes PCD in host plants, but is also important for pathogenicity and oxidative stress tolerance.

Phytophthora cinnamomi

“…The first representative, P. cactorum PcF, induces the expression of plant pathogenicity genes and programmed cell death (Orsomando et al ., ). Previously analysed Phytophthora species contain 3–19 SCR genes (Chen et al ., ; Orsomando et al ., ). A search using P. cactorum SCR genes has revealed that the P. cinnamomi genome contains one homologue of PcF , eight homologues of Scr96 , 15 homologues of Scr99 and one homologue of Scr121 (Table ), and thus appears to have the largest PcF/SCR gene family reported so far.…”

“…A search using P. cactorum SCR genes has revealed that the P. cinnamomi genome contains one homologue of PcF , eight homologues of Scr96 , 15 homologues of Scr99 and one homologue of Scr121 (Table ), and thus appears to have the largest PcF/SCR gene family reported so far. Silencing of P. cactorum Scr96 reduces pathogen virulence on Nicotiana benthamiana leaves and makes it more sensitive to oxidative stress (Chen et al ., ), indicating that Phytophthora SCR proteins are effectors that function as virulence factors under the same circumstances in which they trigger plant cell death.…”

Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae

“…Some SCPs are required for full virulence in many pathogens that have been analysed (Bolton et al ., ; Doehlemann et al , ; Chen et al , ; Qin et al , ). In our study, we found that deletion of VdSCP27 , VdSCP113 , or VdSCP126 independently did not affect the virulence of V. dahliae in tobacco and cotton plants (Figure ).…”

“…Verticillium dahliae is a notorious fungal pathogen that attacks a wide range of hosts, targets the xylem tissue, and causes verticillium wilt disease on many economically important crops (Klosterman et al , ; Inderbitzin and Subbarao, ). Previous studies have shown that secreted proteins probably play a critical role in the pathogenesis of V. dahliae (Fradin and Thomma, ; Chu et al , ; Chen et al , ; ; Zhang et al , ), and the function or the activity of several secreted proteins have been elucidated (de Sain and Rep, ; Klimes et al , ; Wang et al , ; Zhang et al , ). Similar to the mechanisms discovered in other phytopathogens, V. dahliae secretes proteins to manipulate host immunity during infection (de Jonge et al , ; Zhou et al , ; Santhanam et al , ; Liu et al , ; Gui et al , , ; Kombrink et al , ; Zhang et al , ; Qin et al , ).…”

Transcriptomic Analysis of Calonectria pseudoreteaudii during Various Stages of Eucalyptus Infection

“…sclerotiorum by interaction with QCR8, a subunit of the cytochrome b-c1 complex of mitochondrial respiratory chain in plants [39]. Another small cysteine-rich secretory protein, SCR96, from Phytophthora cactorum , was transcriptionally induced throughout the developmental and infection stages [40]. It can trigger cell death in the Solanaceae and is important for pathogenicity and oxidative stress tolerance.…”