Induction of Defense-Related Responses in Cf9 Tomato Cells by the AVR9 Elicitor Peptide of <i>Cladosporium fulvum</i> Is Developmentally Regulated1

Honée, G.; Buitink, Julia; Jabs, Thorsten; Kloe, José De; Sijbolts, Fred; Apotheker, Marion; Weide, R.; Sijen, Titia; Stuiver, Maarten H.; Wit, P.J.G.M. de

doi:10.1104/pp.117.3.809

Cited by 48 publications

(25 citation statements)

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“…The rapid death of periveinal cells also has been observed in tomato leaves inoculated with racespecific elicitors from the fungus Cladosporium (HammondKosack et al, 1994). The occurrence of specialized ROSgenerating cells associated with differentiated vascular tissues also is suggested by the observations that the induction of defense-related responses and the hypersensitive cell death are developmentally regulated in tomato plants and cell cultures (Hammond-Kosack et al, 1994;Honne et al, 1998). Together, these observations suggest that the vascular bundles must play an important role in the generation of signals, such as H 2 O 2 , that regulate the defense response of plants against pathogens and herbivores.…”

Section: Discussionmentioning

confidence: 94%

Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

2001

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The systemic accumulation of both hydrogen peroxide (H 2 O 2 ) and proteinase inhibitor proteins in tomato leaves in response to wounding was inhibited by the NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridine. The expression of several defense genes in response to wounding, systemin, oligosaccharides, and methyl jasmonate also was inhibited by DPI. These genes, including those of four proteinase inhibitors and polyphenol oxidase, are expressed within 4 to 12 hr after wounding. However, DPI did not inhibit the wound-inducible expression of genes encoding prosystemin, lipoxygenase, and allene oxide synthase, which are associated with the octadecanoid signaling pathway and are expressed 0.5 to 2 hr after wounding. Accordingly, treatment of plants with the H 2 O 2 -generating enzyme glucose oxidase plus glucose resulted in the induction of only the later-expressed defensive genes and not the early-expressed signaling-related genes. H 2 O 2 was cytochemically detected in the cell walls of vascular parenchyma cells and spongy mesophyll cells within 4 hr after wounding of wild-type tomato leaves, but not earlier. The cumulative results suggest that active oxygen species are generated near cell walls of vascular bundle cells by oligogalacturonide fragments produced by wound-inducible polygalacturonase and that the resulting H 2 O 2 acts as a second messenger for the activation of defense genes in mesophyll cells. These data provide a rationale for the sequential, coordinated, and functional roles of systemin, jasmonic acid, oligogalacturonides, and H 2 O 2 signals for systemic signaling in tomato plants in response to wounding. INTRODUCTIONReactive oxygen species (ROS) are common components of the defense responses of plants against pathogen and herbivore attacks. Inoculation of plant tissues with pathogens or treatment of cell cultures with microbial elicitors causes an oxidative burst characterized by the rapid generation of hydrogen peroxide (H 2 O 2 ; reviewed by Low and Merida, 1996;Lamb and Dixon, 1997; Bolwell, 1999). Similarly, ROS are generated in plant tissues in response to wounding (Angelini et al., 1990; Bradley et al., 1992;Olson and Varner, 1993; Felton et al., 1994; Bi and Felton, 1995; OrozcoCárdenas and Ryan, 1999). Mechanical stimulation of isolated cells (Yahraus et al., 1995; Gus-Mayer et al., 1998) and the treatment of cell suspension cultures with plant cell wallderived oligogalacturonic acid (OGA; Legendre et al., 1993;Stennis et al., 1998) also generate H 2 O 2 accumulation. Woundinduced H 2 O 2 accumulation is observed both locally and systemically in leaves of several plant species, apparently caused by OGA that was released by a systemically woundinduced polygalacturonase (PG; Bergey et al., 1999; OrozcoCárdenas and Ryan, 1999).H 2 O 2 can act as a local signal for hypersensitive cell death and also as a diffusible signal for the induction of defensive genes in adjacent cells (Alvarez et al., 1998). For example, transgenic potato plants that overexpress a fungal gl...

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Section: Discussionmentioning

confidence: 94%

Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

2001

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“…PCR products were sequenced in both directions (Supplemental Table S2) and with overlapping sequencing products directly or, alternatively, cloned into a pBluescript variant with BamHI and AscI restriction sites, after which multiple clones from independent PCRs were sequenced (BaseClear). For constitutive expression, the Ve1 and Ve2 CDSs were cloned into a binary vector pmog800 variant (Honée et al, 1998), resulting in P35S:Ve1 and P35S:Ve2 (Supplemental Fig. S4).…”

Section: Cloning Of Ve Sequencesmentioning

confidence: 99%

Genetic Dissection ofVerticilliumWilt Resistance Mediated by Tomato Ve1

et al. 2009

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Vascular wilt diseases caused by soil-borne pathogens are among the most devastating plant diseases worldwide. The Verticillium genus includes vascular wilt pathogens with a wide host range. Although V. longisporum infects various hosts belonging to the Cruciferaceae, V. dahliae and V. albo-atrum cause vascular wilt diseases in over 200 dicotyledonous species, including economically important crops. A locus responsible for resistance against race 1 strains of V. dahliae and V. albo-atrum has been cloned from tomato (Solanum lycopersicum) only. This locus, known as Ve, comprises two closely linked inversely oriented genes, Ve1 and Ve2, that encode cell surface receptor proteins of the extracellular leucine-rich repeat receptor-like protein class of disease resistance proteins. Here, we show that Ve1, but not Ve2, provides resistance in tomato against race 1 strains of V. dahliae and V. albo-atrum and not against race 2 strains. Using virus-induced gene silencing in tomato, the signaling cascade downstream of Ve1 is shown to require both EDS1 and NDR1. In addition, NRC1, ACIF, MEK2, and SERK3/ BAK1 also act as positive regulators of Ve1 in tomato. In conclusion, Ve1-mediated resistance signaling only partially overlaps with signaling mediated by Cf proteins, type members of the receptor-like protein class of resistance proteins.

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“…When a biotrophic pathogen enters such an Avr9-transgenic Cf-9 plant an HR is induced, leading to resistance. We found proof of concept (41). Selling the patent to the biotechnology company Mogen International provided the funds for two new postdocs at the Laboratory of Phytopathology.…”

Section: Avr9 Gene-enabled Cloning Of the Cf-9 Resistance Genementioning

confidence: 83%

“…It became known as the Avr9 gene cassette (41,83) (Figure 3). We proposed to transform Cf-9 tomato plants with the Avr9 gene under the control of a pathogen-inducible promoter.…”

Section: Avr9 Gene-enabled Cloning Of the Cf-9 Resistance Genementioning

confidence: 99%

Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato

Wit

2016

Annu. Rev. Phytopathol.

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In this review, I recount my personal history. My drive to study hostpathogen interactions was to find alternatives for agrochemicals, which was triggered after reading the book "Silent Spring" by Rachel Carson. I reflect on my research at the Laboratory of Phytopathology at Wageningen University, where I have worked for my entire career on the interaction between Cladosporium fulvum and tomato, and related gene-for-gene pathosystems. I describe different methods used to identify and sequence avirulence (Avr) genes from the pathogen and resistance (R) genes from the host. The major genes involved in classical gene-for-gene interactions have now been identified, and breeders can produce plants with multiple R genes providing durable and environmentally safe protection against pathogens. In some cases, this might require the use of genetically modified plants when R genes cannot be introduced by classical breeding. MY MOTIVATION TO STUDY PLANT PATHOLOGYI grew up after World War II on a farm in Limburg, the most southern province of The Netherlands. In those days farming was very labor-intensive and still very much dependent on horsepower. I loved to work with horses, but soon they were replaced by tractors. In Limburg, farms were relatively small and not specialized. Apart from growing crops like cereals, sugar beets, and potatoes, most farmers also kept dairy cattle, pigs, and chickens. My eldest brother was going to succeed my father, and I knew that my future would not be in farming. After primary school, I went to high school, where although I spent my time mainly studying languages (Dutch, English, French, German, Greek, and Latin), I was more interested in chemistry and biology. I was fascinated by crop plants that could grow out of tiny seeds into adult plants within one season, and by majestic trees like the chestnut tree that overlooked our farm for more than hundred years. If that chestnut tree could talk, it would have told me how it survived shell bursts during World War II while the farm was completely destroyed. I had a small garden of my own where I experimented with seeds of pea and bean, digging them up from the soil a few days after I had sowed them, curious to find out how far they had developed. My father and my biology teacher at high school stimulated my interest in plant biology. After high school, I went to Wageningen University, where I followed a broad BS program in (bio)chemistry and biology. I did my MS in crop protection, which included three research projects of six months at the Laboratories of Biochemistry, Plant Physiology, and Phytopathology. Apart from these research projects, the MS program included practical training abroad, for which I spent three months at Imperial Chemical Industries (ICI) in Bracknell, UK, working on a bioassay to test the effectiveness of fungicides against powdery mildew of wheat. In those days, protection of crops against fungal pathogens was mainly achieved by applying fungicides. After having read the book "Silent Spring" by Rachel Carson (8),...

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Induction of Defense-Related Responses in Cf9 Tomato Cells by the AVR9 Elicitor Peptide of Cladosporium fulvum Is Developmentally Regulated1

Cited by 48 publications

References 56 publications

Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

Genetic Dissection ofVerticilliumWilt Resistance Mediated by Tomato Ve1

Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato

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