Interactions between Phytophthora cactorum, Armillaria gallica and Betula pendula Roth. Seedlings Subjected to Defoliation

Justyna Anna Nowakowska,Miłosz Tkaczyk,Natalia Stocka,Mirela Tulik,Tom Hsiang,João Maria Caetano,Marcin Stocki,Tomasz Oszako,Sławomir Ślusarski

doi:10.3390/f11101107

Abstract

The purpose of this study was to better understand the interactive impact of two soil-borne pathogens, Phytophthora cactorum and Armillaria gallica, on seedlings of silver birch (Betula pendula Roth.) subjected to stress caused by mechanical defoliation, simulating primary insect feeding. This is the first experimental confirmation of silver birch seedling root damage (and in consequence shoot mortality) caused by the additive effect of defoliation stress and P. cactorum inoculation via soil. However, the most severe damage to roots occurred after A. gallica inoculation. One year after treatments, chlorophyll fluorescence measurement, and gas chromatography coupled with mass spectrometry (GC-MS) were used to analyze the photosynthetic activity in leaves, the volatile organic compounds (VOCs) emitted by the birch leaves, and chemical compounds from the roots. The cumulative effect of the two pathogens and partial defoliation reduced photosynthetic activity, suggesting dysfunction of photosystem PSII due to the applied stresses. In summary, it seems that the main differences in photosynthetic performance could be attributed to Armillaria infection. The birch leaves in seedlings exposed to 50% defoliation, and inoculation with P.cactorum and A. gallica, emitted more aromatic carbonyls and alcohols, as well as half as much aliphatic esters, compared to controls. In infected birch roots, the production of phenols, triterpenes, and fatty alcohols increased, but fatty acids decreased. Higher levels of aromatic carbonyls and alcohols in leaves, as well as phenolic compounds in the roots of stressed birches (compared to control) suggest an activation of plant systemic acquired resistance (SAR).

Highlights

Silver birch (Betula pendula Roth.) is common throughout the lowlands and lower mountainous regions in Europe, and is subject to attack by Phytophthora cactorum (Lebert and Cohn) J
In 2019, after a year of growth in the greenhouse, the 64 four-year-old seedlings were subjected to the following analyses: (i) baiting-based, and molecular, detection of the P. cactorum and A. gallica in the soil and/or in plants; (ii) health state assessment of seedlings; (iii) evaluation of the response to stress factors, via biometric and photosynthetic measurements; and (iv) detection and measurement of volatiles emitted by leaves and compounds extracted from roots
The effects of interactions between soil borne pathogens on the production of secondary metabolites by birch have not been sufficiently studied, and we focused on the effects of the fungus (A. gallica) and the oomycete (P. cactorum) on the chemical composition of compounds secreted by leaves and roots

Summary

Introduction

Silver birch (Betula pendula Roth.) is common throughout the lowlands and lower mountainous regions in Europe, and is subject to attack by Phytophthora cactorum (Lebert and Cohn) J. 150 Phytophthora species (Oomycetes) have been described from a broad range of hosts, including forest tree species and ornamental plants [3,4]. These groups of pathogens have led to extensive mortality of different forest tree species, but are responsible for negative ecological impacts in many countries across the world. In the last few decades, interest in the Phytophthora species as plant pathogens has been growing in Europe and on other continents, since these pathogens are causing emerging diseases of many forest tree species [6,7,8,9]. The risk of transferring phytophthoras from nurseries to forest plantations is considered high, as P. ramorum was transmitted in seedlings from nurseries in California, and it affected production in over 20 US states [14]

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