Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea

* Botrytis cinerea is a necrotrophic fungus that causes grey mould on a wide range of food plants, especially grapevine, tomato, soft fruits and vegetables. This disease brings about important economic losses in both pre- and postharvest crops. Successful protection of host plants against this pathogen is severely hampered by a lack of resistance genes in the hosts and the considerable phenotypic diversity of the fungus. * The aim of this study was to test whether B. cinerea manipulates the immunity-signalling pathways in plants to restore its disease. * We showed that B. cinerea caused disease in Nicotiana benthamiana through the activation of two plant signalling genes, EDS1 and SGT1, which have been shown to be essential for resistance against biotrophic pathogens; and more interestingly, virus-induced gene silencing of these two plant signalling components enhanced N. benthamiana resistance to B. cinerea. Finally, plants expressing the baculovirus antiapoptotic protein p35 were more resistant to this necrotrophic pathogen than wild-type plants. * This work highlights a new strategy used by B. cinerea to establish disease. This information is important for the design of strategies to improve plant pathogen resistance.     

Plant resistance signalling hijacked by a necrotrophic fungal pathogen

The strategies used by necrotrophic fungal pathogens to infect plants are often perceived as lacking the sophistication of their haustorium producing, host defence suppressing, biotrophic counterparts. There is also a relative paucity of knowledge regarding how effective gene-for-gene based resistance reactions might function against necrotrophic plant pathogens. However, recent data has emerged from a number of systems which has highlighted that particular species of necrotrophic (and/or hemibiotrophic) fungi, have evolved very sophisticated strategies for plant infection which appear, in fact, to hijack the host resistance responses that are commonly deployed against biotrophs. Both disease resistance (R) protein homologues and mitogen-activated protein kinase (MAPK) cascades commonly associated with incompatible disease resistance responses; appear to be targeted by necrotrophic fungi during compatible disease interactions. These findings highlight an emerging sophistication in the strategies deployed by necrotrophic fungi to infect plants.Key words: Mycosphaerella graminicola, Septoria tritici, Triticum aestivum, mitogen-activated protein kinase, programmed cell death, fungal pathogen, disease resistance, disease susceptibility, toxin     

Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea

The genetic architecture of plant defense against microbial pathogens may be influenced by pathogen lifestyle. While plant interactions with biotrophic pathogens are frequently controlled by the action of large-effect resistance genes that follow classic Mendelian inheritance, our study suggests that plant defense against the necrotrophic pathogen Botrytis cinerea is primarily quantitative and genetically complex. Few studies of quantitative resistance to necrotrophic pathogens have used large plant mapping populations to dissect the genetic structure of resistance. Using a large structured mapping population of Arabidopsis thaliana, we identified quantitative trait loci influencing plant response to B. cinerea, measured as expansion of necrotic lesions on leaves and accumulation of the antimicrobial compound camalexin. Testing multiple B. cinerea isolates, we identified 23 separate QTL in this population, ranging in isolate-specificity from being identified with a single isolate to controlling resistance against all isolates tested. We identified a set of QTL controlling accumulation of camalexin in response to pathogen infection that largely colocalized with lesion QTL. The identified resistance QTL appear to function in epistatic networks involving three or more loci. Detection of multilocus connections suggests that natural variation in specific signaling or response networks may control A. thaliana-B. cinerea interaction in this population.     

Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests

The term green island was first used to describe an area of living, green tissue surrounding a site of infection by an obligately biotrophic fungal pathogen, differentiated from neighbouring yellowing, senescent tissue. However, it has now been used to describe symptoms formed in response to necrotrophic fungal pathogens, virus infection and infestation by certain insects. In leaves infected by obligate biotrophs such as rust and powdery mildew pathogens, green islands are areas where senescence is retarded, photosynthetic activity is maintained and polyamines accumulate. We propose such areas, in which both host and pathogen cells are alive, be termed green bionissia. By contrast, we propose that green areas associated with leaf damage caused by toxins produced by necrotrophic fungal pathogens be termed green necronissia. A range of biotrophic/hemibiotrophic fungi and leaf-mining insects produce cytokinins and it has been suggested that this cytokinin secretion may be responsible for the green island formation. Indeed, localised cytokinin accumulation may be a common mechanism responsible for green island formation in interactions of plants with biotrophic fungi, viruses and insects. Models have been developed to study if green island formation is pathogen-mediated or host-mediated. They suggest that green bionissia on leaves infected by biotrophic fungal pathogens represent zones of host tissue, altered physiologically to allow the pathogen maximum access to nutrients early in the interaction, thus supporting early sporulation and increasing pathogen fitness. They lead to the suggestion that green islands are 'red herrings', representing no more than the consequence of the infection process and discrete changes in leaf senescence.     

Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3

Oligogalacturonides (OGs) released from plant cell walls by pathogen polygalacturonases induce a variety of host defense responses. Here we show that in Arabidopsis (Arabidopsis thaliana), OGs increase resistance to the necrotrophic fungal pathogen Botrytis cinerea independently of jasmonate (JA)-, salicylic acid (SA)-, and ethylene (ET)-mediated signaling. Microarray analysis showed that about 50% of the genes regulated by OGs, including genes encoding enzymes involved in secondary metabolism, show a similar change of expression during B. cinerea infection. In particular, expression of PHYTOALEXIN DEFICIENT3 (PAD3) is strongly up-regulated by both OGs and infection independently of SA, JA, and ET. OG treatments do not enhance resistance to B. cinerea in the pad3 mutant or in underinducer after pathogen and stress1, a mutant with severely impaired PAD3 expression in response to OGs. Similarly to OGs, the bacterial flagellin peptide elicitor flg22 also enhanced resistance to B. cinerea in a PAD3-dependent manner, independently of SA, JA, and ET. This work suggests, therefore, that elicitors released from the cell wall during pathogen infection contribute to basal resistance against fungal pathogens through a signaling pathway also activated by pathogen-associated molecular pattern molecules.     

Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection

Necrotrophic fungi are unable to occupy living plant cells. How such pathogens survive first contact with living host tissue and initiate infection is therefore unclear. Here, we show that the necrotrophic grey mold fungus Botrytis cinerea undergoes massive apoptotic-like programmed cell death (PCD) following germination on the host plant. Manipulation of an anti-apoptotic gene BcBIR1 modified fungal response to PCD-inducing conditions. As a consequence, strains with reduced sensitivity to PCD were hyper virulent, while strains in which PCD was over-stimulated showed reduced pathogenicity. Similarly, reduced levels of PCD in the fungus were recorded following infection of Arabidopsis mutants that show enhanced susceptibility to B. cinerea. When considered together, these results suggest that Botrytis PCD machinery is targeted by plant defense molecules, and that the fungal anti-apoptotic machinery is essential for overcoming this host-induced PCD and hence, for establishment of infection. As such, fungal PCD machinery represents a novel target for fungicides and antifungal drugs.     

Cell biology of plant-oomycete interactions

The last 4 years have seen significant advances in our understanding of the cellular processes that underlie the infection of plants by a range of biotrophic and necrotrophic oomycete pathogens. Given that oomycete and fungal pathogens must overcome the same sets of physical and chemical barriers presented by plants, it is not surprising that many aspects of oomycete infection strategies are similar to those of fungal pathogens. A major difference, however, centres on the role of motile oomycete zoospores in actively moving the pathogen to favourable infection sites. Recent studies have shown that the plant defence response to invading oomycetes is similar to that mounted against fungi, but biochemical differences between oomycete and fungal surface molecules must have implications for plant recognition of and defence against oomycete pathogens. The aim of this short review is to provide a cell biological framework within which emerging data on the molecular basis of oomycete-plant interactions may be placed.     

Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato

Plants have evolved sophisticated mechanisms to sense and respond to pathogen attacks. Resistance against necrotrophic pathogens generally requires the activation of the jasmonic acid (JA) signaling pathway, whereas the salicylic acid (SA) signaling pathway is mainly activated against biotrophic pathogens. SA can antagonize JA signaling and vice versa. Here, we report that the necrotrophic pathogen Botrytis cinerea exploits this antagonism as a strategy to cause disease development. We show that B. cinerea produces an exopolysaccharide, which acts as an elicitor of the SA pathway. In turn, the SA pathway antagonizes the JA signaling pathway, thereby allowing the fungus to develop its disease in tomato (Solanum lycopersicum). SA-promoted disease development occurs through Nonexpressed Pathogen Related1. We also show that the JA signaling pathway required for tomato resistance against B. cinerea is mediated by the systemin elicitor. These data highlight a new strategy used by B. cinerea to overcome the plant's defense system and to spread within the host.     

Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea

Polygalacturonases (PGs) hydrolyze the homogalacturonan of plant cell-wall pectin and are important virulence factors of several phytopathogenic fungi. In response to abiotic and biotic stress, plants accumulate PG-inhibiting proteins (PGIPs) that reduce the activity of fungal PGs. In Arabidopsis thaliana, PGIPs with comparable activity against BcPG1, an important pathogenicity factor of the necrotrophic fungus Botrytis cinerea, are encoded by two genes, AtPGIP1 and AtPGIP2. Both genes are induced by fungal infection through different signaling pathways. We show here that transgenic Arabidopsis plants expressing an antisense AtPGIP1 gene have reduced AtPGIP1 inhibitory activity and are more susceptible to B. cinerea infection. These results indicate that PGIP contributes to basal resistance to this pathogen and strongly support the vision that this protein plays a role in Arabidopsis innate immunity.     

Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions

In ecological systems, indirect interactions between plant pathogens and phytophagous arthropods can arise when infestation by a first attacker alters the common host plant so that although a second attacker could be spatially or temporally separated from the first one, the former could be affected. The induction of plant defense reactions leading to the production of secondary metabolites is thought to have an important role since it involves antagonistic and/or synergistic cross-talks that may determine the outcome of such interactions. We carried out experiments under controlled conditions on young rose plants in order to assess the impact of these indirect interactions on life history traits of three pests: the necrotrophic fungus Botrytis cinerea Pers.: Fr. (Helotiales: Sclerotiniaceae), the aphid Rhodobium porosum Sanderson (Hemiptera: Aphididae) and the thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Our results indicated (i) a bi-directional negative interaction between B. cinerea and R. porosum, which is conveyed by decreased aphid growth rate and reduced fungal lesion area, as well as (ii) an indirect negative effect of B. cinerea on insect behavior. No indirect effect was observed between thrips and aphids. This research highlights several complex interactions that may be involved in structuring herbivore and plant pathogen communities within natural and managed ecosystems.