Polymorphic change of appressoria by the tomato powdery mildew Oidium neolycopersici on host tomato leaves reflects multiple unsuccessful penetration attempts

Nonomura, Teruo; Nishitomi, Ayae; Matsuda, Yoshinori; Soma, Chiyomi; Xu, Lingfei; Kakutani, Koji; Takikawa, Yuichi; Toyoda, Hideyoshi

doi:10.1016/j.funbio.2010.08.008

Cited by 17 publications

(16 citation statements)

References 28 publications

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“…However, in our tests a potential penetration site was not visible in this position within extracellular material left behind on the PDL. We now know the distal lobe would have been the last formed, and this fits well with a recent finding that germ tubes of O. neolycopersici on a susceptible tomato leaf remain unlobed if they immediately succeed in penetrating the epidermal cell wall and form a haustorium, but if for any reason there is no penetration or if the peg is blocked by a host papilla and the haustorium fails to develop, then lobes are produced successively until a haustorium is produced (Nonomura et al 2010). This agrees with our finding that multilobed species will sometimes produce more lobes on the host surface than on the PDL.…”

Section: Discussionsupporting

confidence: 86%

Development of appressoria on conidial germ tubes of Erysiphe species

2011

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Modes of branching of appressoria on conidial germ tubes of 36 Erysiphe spp. were studied. Only unlobed appressoria, termed alobatus pattern, were seen in E. lonicerae, E. magnifica and E. symphoricarpi. Viewed from above with light or scanning electron microscopes, other species had ± irregular lobing, but from below in the plane of contact with the substrate successive dichotomous branchings at 120°were seen to produce a five-lobed appressorium within 6 h. Each division produced a temporarily dormant outward-facing lobe and an inward limb that continued growth and division to form the axis of curved, hooked, single-or double-headed symmetrical or asymmetrical structures in a helicoid cyme-like pattern. Outlines of extracellular material after removal of germinated conidia confirmed this manner of branching. After 36 h some lobes re-divided forming botryose or jigsaw patterns even extending with extra appressoria to form candelabra-like structures. Conidia developed only one true germ tube; rarely secondary unswollen tubes emerged from spare shoulders or ends. The same true germ tubes developed initially on host surfaces, where secondary tubes and/ or extensions from appressorial lobes grew into colonyforming hyphae. Lobed appressoria of Neoerysphe and Phyllactinia also branched at 120°. Podosphaera xanthii exhibited a simpler branching pattern.

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Section: Discussionsupporting

confidence: 86%

Development of appressoria on conidial germ tubes of Erysiphe species

2011

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“…Appressoria of conidia, which were immediately successful in penetration, were simple; however, after some unsuccessful atempts they became multilobed. This shape was also observed in conidia which germinated on resistant genotypes of wild tomatoes (L. peruvianum, recently S. peruvianum) or on a non-host plant (barley) (Nonomura et al 2010).…”

Section: Appressoria and Haustoria Formationmentioning

confidence: 62%

“…4). A study on the shape of appressoria of O. neolycopersici was carried out by Nonomura et al (2010). These authors studied in detail the initial stages of pathogen development and found that the original shape of appressoria of O. neolycopersici was rather simple, non-lobed, nippleshaped, and that the formation of a lobed appressorium came after unsuccessful attempts at penetration.…”

Section: Appressoria and Haustoria Formationmentioning

confidence: 99%

Resistance mechanisms of wild tomato germplasm to infection of Oidium neolycopersici

et al. 2013

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Tomato powdery mildew (Oidium neolycopersici) is one of the most devastating diseases of cultivated tomatoes worldwide. Although the first epidemics were recorded more than 25 years ago many aspects of this host-pathogen interaction are still not well understood. Detailed morphological and molecular studies of the anamorphs confirmed that O. neolycopersici is phylogeneticaly close to Erysiphe aquilegiae var. ranunculi. Host range is rather broad, apart from Solanaceae hosts were found in the families Apocynaceae, Campanulaceae, Crassulaceae, Cistaceae, Cucurbitaceae, Linaceae, Malvaceae, Papaveraceae, Pedialiaceae, Scrophulariaceae, Valerianaceae a Violaceae. Non-host resistance within these families is not based on inhibition of formation of primary haustorium, however, on post-haustorial hypersensitive reponse and another type of non-hypersensitive resistance. Screening of wild Solanum species (previous Lycopersicon spp.) germplasm revealed valuable sources of resistance (S. habrochaites, S. pennellii, S. cheesmaniae, S. chilense, S. peruvianum). The main resistance mechanism was found to be a hypersensitive response (HR), in some cases followed by limited development of the pathogen. However, there is a broad variation in resistance response on the histological and cytological level. Interaction between many wild Solanum spp. and O. neolycopersici is race-specific, at least three races were differentiated. In some interspecific crosses (S. lycopersicum × S. habrochaites) adult plant resistance was observed. Biochemical studies focusing on production of reactive oxygen species (ROS) and peroxidase activity during infection of O. neolycopersici showed that production of ROS and activity of corresponding enzymes is related to activation of defence responses in genotypes of wild Solanum sect. Lycopersicon. The significance of nitric oxide (NO) in O. neolycopersici pathogenesis was supported by experiments with NO donors and scavengers. In moderately resistant genotype S. chmielewskii, treatment by heat stress caused slight deceleration of pathogen development, increased production of jasmonic acid (JA) and abscisic acid (ABA) and increased peroxidase activity in infected plants. The different degree of tomato resistance/ susceptibility did not markedly change the rate and extent of photosynthetic response to O. neolycopersici; only minimal impairment of photosynthesis was found in both susceptible and moderately resistant genotypes during the Harper Adams University, Newport, Shropshire TF10 8NB, UK first 9 days after inoculation. The accumulated evidence confirm a crucial role of localised increased production of ROS and reactive nitrogen species (RNS) in response to pathogen penetration into plant tissue and its involvement in the plant resistance responses including the initiation and progression of plant cell death in host wild Solanum species. Crucial points of further research are discussed.

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“…In our previous paper (Nonomura et al 2010), appressorial shapes (nonlobed, nipple-shaped and lobed appressoria) of the tomato powdery mildew (Oidium neolycopersici) were determined as a result of repeated unsuccessful attempts at penetration by the infection pegs generated from the appressoria. In addition, germ tube length was shown to be dependent upon the timing of the contact of the germ tube tip with the leaf surface (Nonomura et al 2009).…”

Section: Introductionmentioning

confidence: 99%

“…From this point of view, in the present study, we attempted to clarify whether the tomato powdery mildew conidia initiate germ tubes at a predetermined site or determine the site after they contact the leaves; we used highly germinative O. neolycopersici conidia collected from conidial pseudochains on conidiophores (Nonomura et al 2009), and examined them with a high-fidelity digital microscope. This enables three-dimensional observations of nonfixed conidia inoculated onto leaf or artificial surfaces (Matsuda et al 2005b;Nonomura et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Conidia of the tomato powdery mildew Oidium neolycopersici initiate germ tubes at a predetermined site

Takikawa

Kakutani

et al. 2011

Mycoscience

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The emergence of germ tubes from the conidia of powdery mildew fungi is the first morphological event of the infection process, preceding appressoria formation, peg penetration and primary haustoria formation. Germination patterns of the conidia are specific in powdery mildew fungi and therefore considered useful for identification. In the present study, we examined conidial germination of the tomato powdery mildew Oidium neolycopersici KTP-01 in order to clarify whether germ tube emergence site in KTP-01 conidia is determined by the first contact of the conidia to leaves (as found for the conidia of barley powdery mildew), or alternatively is predetermined and is unrelated to contact stimulus. Highly germinative conidia of KTP-01 were collected from conidial pseudochains on conidiophores in colonies on tomato leaves using two methods involving an electrostatic spore attractor and a blower. In the electrostatic spore attraction method, the conidia were attracted to the electrified insulator probe of the spore collector-this being the first contact stimulus for the conidia. In addition, the blowing method was used as a model of natural infection; pseudochain conidia were transferred to detached leaves by air (1 m/s) from a blower. Thus, landing on the leaves was the first contact for the conidia. Furthermore, conidia were also blown onto an artificial membrane (Parafilm-coated glass slides forming a hydrophobic surface) or solidified agar plates in Petri dishes (hydrophilic surface). Eventually, almost all conidia on the probe and on tomato leaves or artificial hydrophobic and hydrophilic surfaces synchronously germinated within 6 h of incubation, indicating that the first contact of the conidia with any of the aforementioned substrata was an effective germination induction signal. Germ tube emergence sites were exclusively subterminal on the conidia. Moreover, the germ tubes emerged without any relation to the sites touched first on the conidia. Thus, the present study strongly indicates that conidia of O. neolycopersici produce germ tubes at a predetermined site.

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Polymorphic change of appressoria by the tomato powdery mildew Oidium neolycopersici on host tomato leaves reflects multiple unsuccessful penetration attempts

Cited by 17 publications

References 28 publications

Development of appressoria on conidial germ tubes of Erysiphe species

Development of appressoria on conidial germ tubes of Erysiphe species

Resistance mechanisms of wild tomato germplasm to infection of Oidium neolycopersici

Conidia of the tomato powdery mildew Oidium neolycopersici initiate germ tubes at a predetermined site

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