Elsevier

Fungal Biology

Volume 121, Issue 12, December 2017, Pages 1054-1062
Fungal Biology

Ascospore release in apple scab underlies infrared sensation

https://doi.org/10.1016/j.funbio.2017.09.001Get rights and content

Abstract

The agent of apple scab disease (Venturia inaequalis) is the most common pathogen in apple cultivation. Its ascospores are released in spring, mainly during daylight hours and triggered by rain events. To investigate the causes of diurnal rhythm of ascospore dissemination of the apple scab fungus ascospore releases were examined continuously with spore traps in the orchard and with laboratory assays. One of the spore traps was illuminated at night with different light sources in each year during 2011–2015. The laboratory assays were performed with different light sources with varying wavelengths and intensities. In field and laboratory conditions only light including infrared radiation stimulated ascospore release, but not with light in the visible spectrum only. Artificial illumination during night was correlated with an increase of up to 46 % of ascospores released overnight in the field. We proved that infrared radiation induces V. inaequalis to release its spores. This is the first report in which spore discharge could be stimulated during night under field conditions.

Introduction

The perception of light is essentially linked with life on earth and the daily light–dark-cycle is the strongest trigger for almost all living organisms (Aschoff et al., 1992, Fleissner, 1996). The reaction to light is also known from many fungi. The spectrum of light from UV-C to far-red could affect different reactions in fungi. An often reported effect of light on fungi is the stimulation or repression of spore production and spore discharge (Corrochano and Galland, 2006, Idnurm et al., 2010) or the formation of fruiting bodies in course of the life cycle (Kües & Navarro-González 2015). Even infrared radiation is known to influence the spore release (Leach 1975). Physiological investigations and genome sequencing have shown that the four classes of photoreceptors found in other kingdoms also exist in the fungi (Idnurm & Heitman 2005). These are Phytochrome, Opsin, Phototropin, and Cryptochrome. If opsins play a light-regulatory role in fungi is yet not known (Rodriguez-Romero et al. 2010).

The first identified and best studied photoreceptor system in fungi is the blue-light sensing system in Neurospora crassa. The system is known as White Collar and consists of the protein WC-1 and WC-2 which interact and form the White Collar complex (WCC) (Crosthwaite et al., 1997, Froehlich et al., 2002, Dunlap and Loros, 2004). The phototropin-like photoreceptor system is a flavin-binding photoreceptor which has been studied in a number of fungi (Ambra et al., 2004, Casas-Flores et al., 2006, Idnurm et al., 2006, Lee et al., 2006, Avalos and Estrada, 2010, Kamada et al., 2010, Olmedo et al., 2010, Sand, 2011).

Venturia inaequalis, the agent of apple scab disease, has been subjected to research since the 19th century with basic and applied topics concerning its biology, epidemiology, and disease management (MacHardy 1996). Ascospores of the pathogen are released during spring as the primary inoculum. The release of ascospores is triggered by different environmental stimuli, especially rain (Alt & Kollar 2010). Only low numbers of ascospores are liberated during dew (Frey and Keitt, 1925, Miller and Waggoner, 1958, Moore, 1958, Hirst and Stedman, 1962a, Brook, 1969a, MacHardy and Gadoury, 1986). The concentration of airborne ascospores shows a daytime maximum which cannot be explained by the distribution of rain (Hirst & Stedman 1962a). After nocturnal rains ascospores are normally released during the following morning hours (Brook 1966). Therefore light (Frey and Keitt, 1925, Hirst and Stedman, 1962b, Brook, 1966, Brook, 1969a, Brook, 1969b, MacHardy and Gadoury, 1986, Palm, 1988) or other daylight correlated factors were considered as possible additional triggers necessary for spore release of V. inaequalis.

Numerous field studies (Hirst and Stedman, 1962a, Brook, 1966, Brook, 1969a, MacHardy and Gadoury, 1986, Aylor and Sutton, 1992, Warner and Braun, 1992, Rossi et al., 2001) were in accordance with these findings and reported a diurnal pattern of ascospore dissemination with an effect of light intensity and light quality to the rate of ascospore discharge. The highest amount of ascospores was released between sunrise and sunset in the bright daylight hours. In the mentioned studies the amount of spores discharged in darkness was between 0.5 and 20 % of the season's ascospores. Ascospore release in V. inaequalis at daylight and its suppression during night could not yet be influenced or changed under field conditions. The suppression of the ascospore release during darkness could also not be proven clearly under laboratory conditions (Warner and Braun, 1992, Stensvand et al., 2000).

In the last decades research was focussed to the effect of brightness and light quality. Palm (1988) draws the line between day and night for V. inaequalis at a value of 2000 lx. In nature 2000 lx equals approximately 8 μW cm2 global radiation of daylight. This radiation level is reached approximately 1–1.5 h after sunrise on a rainy day. A similar level was found to be sufficient to stimulate spore release in the field (Stensvand et al. 2009) and in the laboratory (Gadoury et al. 1998).

Nearly 50 y ago Brook, 1969b, Brook, 1975 described experiments on the impact of light on ascospore release of V. inaequalis. In laboratory experiments a stimulation of the spore discharge by V. inaequalis by light was detected, particularly by red light with wavelengths between 710 and 730 nm (Brook, 1969b, Gadoury et al., 1998). Light intensities from 0.5 μW cm2 at 725 nm initiated spore release in wind tunnel experiments (Gadoury et al. 1998). Spore release was very low in darkness or under light below 620 nm (blue and green).

The purpose of this study was to investigate the causes of diurnal rhythm of ascospore dissemination of the apple scab fungus. Therefore ascospore releases were examined continuously under natural conditions in the field using spore traps and with laboratory assays. The aim of the field experiments was to investigate the impairment of diurnal periodicity of ascospore release through specific illumination during the night-time hours for at least one season for one lighting condition. Furthermore an important scope was to develop a simple laboratory method which reproduces consistently the suppression of ascospore release in darkness. The effect of different light sources, intensities, and brightness as well as the effect of different compositions of wavelengths on ascospore release should be examined in laboratory experiments.

Section snippets

Leaf material

Apple leaves of the apple cultivar ‘Jonagold’ infected by Venturia inaequalis were collected in autumn 2011–2014 in a commercial orchard in Buechold near Wuerzburg, Germany. The leaves were placed in plastic trays (550 × 300 × 70 mm) and overwintered on the ground in the apple tree orchard of Julius Kuehn-Institut (JKI, coordinates: 49.449720, 8.639683). In order to protect the leaves from wind the trays were covered with a wire mesh (one mesh 10 × 10 mm2). The base of the trays was perforated

Results

Monitoring conducted in the field during the years 2004–2010 showed that of the total number of ascospores released from infected apple leaves in the tray and recorded by the spore trap over complete days, on average 7.3 % are liberated from sunset till sunrise, i.e., during night. In 2011 during night time, 9.93 % of all ascospores were released at the depot with the illuminated leaves and 6.62 % in the control. There was no difference in the diurnal time pattern of ascospore release. In 2012,

Discussion

The results indicated that after night rain ascospore release in Venturia inaequalis can be induced by infrared light in the range from 1000 to 2000 nm with intensities above 6 μW cm2 nm−1. Attention should be paid to the effect of mechanical disturbance in the stimulation of ascospore release. During the preliminary laboratory studies with the standard waterbath method (Kollar 2000) with infected leaves floating in water, there was no difference in ascospore release in light produced by a

Acknowledgements

We thank K. Piwowarczyk for technical assistance, F.M. Porsche for comments, A. Engelhardt for leaf collection, and M. Ehlert and T. Ehlert for proof reading. The project was supported by funds of the German Government's Special Purpose Fund held at the Landwirtschaftliche Rentenbank.

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