Systemic resistance against Botrytis cinerea in Arabidopsis triggered by an olive marc compost substrate requires functional SA signalling

Abstract

Compost is used as a peat substitute and soil amendment because of its suppressive properties against soilborne plant diseases. It is also effective in reducing foliar diseases, which suggests that compost systemically affects the plant. The improvement of plant nutrition due to the compost has been suggested as an important factor. In this study, we found higher resistance of Arabidopsis plants grown in an olive marc compost against Botrytis cinerea than in plants grown in perlite. There was no difference in the leaf nutrients of the plants grown in the two substrates. Hence, the compost does not have a nutritional effect on this system. In Col-0 plants, the incidence of diseased leaves was reduced by 30% and an equal reduction in disease was induced in jar1-1 mutants. However, there was no disease reduction in sid2-1. This suggests the need for SA signalling in compost-induced resistance. Furthermore, PR-1 expression was higher in compost-grown plants than in perlite-grown plants before and after pathogen inoculation. VSP2 expression in artificially wounded plants was lower in compost-grown plants than in perlite-grown plants, which suggests that there was negative crosstalk between compost-induced and wound-induced signals.

Introduction

Compost has been used as a substitute for peat to control soilborne plant diseases for almost 50 years [1]. This practise is doubly beneficial, as peat is extracted from endangered environments, whilst compost is a renewable product that contributes to closing the organic matter cycle. A vast number of scientific studies support the suppressive capacities of compost against many plant pathogens in several plant species [2]. The mechanisms underlying this suppressiveness have been related to both chemical and biological components of the compost, acting directly on the pathogen [3].

In addition, a small but growing number of reports indicate that foliar diseases are reduced when compost is used in the growing medium. This raises questions about the mechanisms involved in this phenomenon, since the compost is not in direct contact with the pathogen, and the most suitable explanation is that compost systemically affects the plant. Enhancement of basal resistance is a common reaction of plants against biotic and abiotic stresses and is often called induced resistance. One of the two archetypal cases of induced resistance is systemic acquired resistance (SAR) [4], in which attack by a pathogen triggers defence responses, while a local signal is generated that travels systemically and the entire plant increases its resistance to future attacks from various pathogens. SAR is dependent on the production of and responsiveness to salicylic acid (SA) [5], [6], and is related to the induction of pathogenesis-related (PR) proteins [7]. The other case is that of induced systemic resistance (ISR), in which treatment of the plant with certain beneficial microorganisms condition it to respond more quickly and intensely to future pathogen attacks, even though no defence changes are detected prior to pathogen infection [8], [9], [10]. The signalling of this pathway is dependent on the production of jasmonic acid (JA) and ethylene (ET) and the capacity of the plant to respond to those hormones [11]. Plant wound responses are also mediated through JA [12].

Some authors have suggested that foliar disease reduction by composts is mediated through induced resistance [13], [14]. However, this possibility has not yet been studied in depth. The effect of compost on the nutrition of plants has also been proposed as an alternative or additional explanation for increased resistance [14], [15]. The importance of nutrition in compost vs. peat or perlite assays has been largely overlooked. Plants grown in compost and fertilized in the same way as plants grown in a standard substrate may have increased nutrient availability, which could affect plant resistance to pathogens.

To study the systemic effects of compost on plant resistance Botrytis cinerea was selected as a pathogen able to produce foliar disease. B. cinerea recently appeared as number 2 in a Top 10 list of plant fungal pathogens on the basis of their perceived scientific and economic importance [16], mainly because its broad host range and the severe damages it produces. The fungus is considered as a typical necrotroph and has been often used in induced resistance studies [17], [18], [19] as well as in plant defence mechanisms studies [20], [21], [22].

The objective of this study was to establish whether: i) a mature olive marc compost is able to induce systemic resistance against the foliar pathogen B. cinerea, ii) any such induced resistance was similar to SAR or ISR, and iii) nutrition was involved in any increased resistance.