J. Phytopathology 153, 377–383 (2005) Ó 2005 Blackwell Verlag, Berlin Review Laboratory of Biochemistry, University of Neuchaˆtel, Neuchaˆtel, Switzerland Abscisic Acid and Callose: Team Players in Defence Against Pathogens? V.Flors 1, J.Ton 2, G.Jakab 3 and B.Mauch-Mani 3 AuthorsÕ addresses: 1Department of Experimental Sciences, Plant Physiology Section, University of Jaume, Borriol, 12071 Castellon, Spain; 2Section of Phytopathology, Faculty of Biology, Utrecht University, 3584 CA Utrecht, The Netherlands; 3Faculty of Science, Laboratory of Biochemistry, University of Neuchaˆ tel, 2007 Neuchaˆ tel, Switzerland (correspondence to B. Mauch-Mani. E-mail: [email protected]) Received March 6, 2005; accepted March 22, 2005 Keywords: abscisic acid, basal resistance, callose, callose deposition, papillae, plant–pathogen interactions, resistance response, systemic acquired resistance Abstract to the heightened defensive capacity of the systemic Abscisic acid (ABA) plays an important role as a plant tissues in SAR. At the cellular level these defence reac- hormone and as such is involved in many different tions are preceded by numerous changes including the steps of plant development. It has also been shown to synthesis of salicylic acid, reactive oxygen species modulate plant responses to abiotic stress situations (ROS), nitric oxide (NO) and the hypersensitive reac- and in recent years, it has become evident that it is tion to name a few (Veronese et al., 2003). All these partaking in processes of plant defence against patho- changes occur in a well-defined sequential order and gens. Although ABA’s role in influencing the outcome are mediated by distinct signal transduction pathways of plant-pathogen interactions is controversial, with picking up the signal upon recognition of the pathogen most research pointing into the direction of increased by the host and leading to the final induction of defen- susceptibility, recent results have shown that ABA can sive measures. Classically, two different signalling also be involved in rendering plants more resistant to pathways have been distinguished (Kunkel and pathogen attack. In these cases, ABA interacts with Brooks, 2002). One of the pathways is based on SA- callose deposition allowing an early and efficient build dependent signalling (Ryals et al., 1996), the other is up of papillae at the sites of infection. The present dependent on a functional jasmonate/ethylene signal- review tries to shed some light on a possible interplay ling (Thomma et al., 2001). While the former has been between ABA and callose in the protection of plants shown to be implicated in the defence against biotrophs against invading pathogens. such as Hyaloperonospora parasitica and Erysiphe orontii or the hemibiotroph Pseudomonas syringae in Introduction Arabidopsis, the latter one is implicated when plants are When plants are attacked by pathogens they activate a challenged by necrotrophic organisms such as Botrytis battery of reactions including both chemical and phys- cinerea, Alternaria brassicicola or Erwinia carotovora ical defences (Agrios, 1997). Among the chemical (Rojo et al., 1999; Thomma et al., 2001). This clear dis- defences the synthesis of antimicrobial compounds tinction observed in Arabidopsis, however, might not be such as phytoalexins and defensins have been well valid for every plant species. Achuo et al. (2004) showed documented to play a role in the outcome of an inter- that the SA pathway was effective against Botrytis in action between a host plant and a pathogen (Kuc, tomato, but not in tobacco, while the SA pathway was 1995; Penninckx et al., 1998). The pathogenesis-related effective against Oidium in tobacco but not in tomato. (PR) proteins, comprising enzymes capable of degra- Recently, increasing evidence has also been pointing to ding pathogen cell walls, are another example of a suc- the involvement of yet another plant hormone, abscisic cessful plant defence mechanism (Van Loon and Van acid (ABA), in plant–pathogen interactions (Audenaert Strien, 1999). They play an important role in basal et al., 2002; Anderson et al., 2004; Thaler and Bostock, resistance as well as in systemic acquired resistance 2004; Thaler et al., 2004; Ton and Mauch-Mani, 2004; (SAR) where they have been shown to be induced not Ton et al., 2005). only locally in the attacked plant parts but also sys- When a pathogen tries to invade plant tissues, the temically in distant areas of the plant (Sticher et al., first barrier it encounters is the plant cell wall. If 1997). This systemic induction is thought to contribute ingress can be stopped at this stage, these results in a www.blackwell-synergy.com 378 Flors et al. large reduction of cellular damage and can also make generally lead to excessive papilla growth causing a further defensive actions as described above obsolete. very high level of resistance to powdery mildew A typical reaction of an attacked plant is the build up (although it made the plants more susceptible to patho- of papillae (Zeyen et al., 2002). Such papillae are gens such as Magnaporthe and Bipolaris). In mlo- apposed on the inner side of epidermal cell walls in the mutants the absence of the regulatory function of the apoplasm directly below the attempted entry point of Mlo gene although often leads to pleiotropic effects a pathogen. A major constituent of such papillae is (Wolter et al., 1993). Another example illustrating the callose, a b-1,3-glucan, but other substances such as importance callose deposits can have for the outcome polysaccharides, phenolic compounds, reactive oxygen of a host–pathogen interaction has been shown for the intermediates and proteins have also been found interaction between lettuce and Plasmopara lactucae- (Smart et al., 1986; Bolwell, 1993; Bestwick et al., radicis. Resistance of lettuce to this oomycete is based 1997; Thordal-Christensen et al., 1997; Heath, 2002). on callose deposits around the haustoria. Treatment of In the present review we will try to shed some light a genetically resistant lettuce cultivar with 2-deoxy-d- on the role of callose and ABA in plant resistance glucose (DDG), an inhibitor of callose synthesis, resul- against pathogens and discuss what connections might ted in susceptibility (Stanghellini et al., 1993). DDG exist between these two compounds. also allowed highlighting the role of callose in the inter- action between Arabidopsis and the two necrotrophs Where is Callose Found and Where Does it Come A. brassisicola and Plectospherella cucumerina, respect- From? ively. Here too, resistance was tightly correlated to the Callose is an amorphous b-1,3-d-glucan found in presence of callose-containing papillae (Ton and numerous locations in higher plants. It is easily visual- Mauch-Mani, 2004). In Arabidopsis, induction of resist- ized through its UV light-induced fluorescence with ance against H. parasitica with the non-protein amino the aniline blue fluorochrome (Stone et al., 1985). Cal- acid b-aminobutyric acid (BABA) functions via depos- lose has been observed on sieve plates in dormant ition of callose at the point of attempted penetration of phloem and in abscission zones, it appears transitorily the oomycete (Zimmerli et al., 2000). In a collection of during cell plate formation, is a major component of Arabidopsis mutants with increased resistance towards pollen and pollen tube cell walls, and is also found in the powdery mildew pathogen E. cichoracearum, one plasmodesmata (Stone and Clarke, 1992). Callose mutant, pmr4, has been isolated that shows loss of cal- deposition can be induced by biotic and abiotic stres- lose deposition following wounding or pathogen ses and the polymer is then deposited between the attack. Interestingly, in this case the absence of callose plasma membrane and the cell wall (Stone and Clarke, deposition, due to a mutation in a CalS gene, lead not 1992). Upon pathogen attack a rapid deposition of cal- as expected to a higher susceptibility but to resistance lose at the point of attempted penetration by the (Nishimura et al., 2003). By crossing this mutant with pathogen has been observed (Zimmerli et al., 2000; mutants in the SA pathway the authors were able to Donofrio and Delaney, 2001; Roetschi et al., 2001; show that a block in the SA pathway was sufficient to Zeyen et al., 2002; Ton and Mauch-Mani, 2004). restore the susceptibility of the plants pointing to a Callose is supposed to be generated by callose syn- negative regulation of the SA pathway by callose or thase (CalS) complexes encoded by glucan synthase- CalS (Nishimura et al., 2003). like genes. There are 12 CalS isozymes in Arabidopsis, and each may be tissue-specific and/or regulated under ABA Interactions with other Hormones and different physiological conditions responding to biotic Pathways involved in Resistance and abiotic stresses (Verma and Hong, 2001). The sesquiterpenoid plant hormone ABA participates in the control of numerous essential physiological pro- The Role of Callose in Plant Defense cesses, such as seed development and germination, but A role for callose as constituent of papillae in plant also in plant responses to different stresses (Zeevaart defence has been accepted for a long time (Aist, 1976). and Creelman, 1988; Koornneef and Karssen, 1994; One of the best-investigated systems in this field is the Rock and Quatrano, 1995; Leung and Giraudat, interaction between barley and the powdery mildew 1998). The level of ABA increases in plants during fungus Blumeria graminis f. sp. hordei. Blumeria attacks seed development and under many environmental cereal epidermal cells and tries to grow a haustorium stresses, particularly drought and salinity. An increas- inside of them. To prevent penetration, these cells ing body of information also points to an involvement respond by local reinforcement of the cell wall beneath of ABA in the plantsÕ responses to pathogen attack the site of the penetration attempt by forming a papilla. (Audenaert et al., 2002; Anderson et al., 2004; Ton This process involves deposition of the callose matrix and Mauch-Mani, 2004; Ton et al., 2005).