ПРИКЛАДНАЯ БИОХИМИЯ И МИКРОБИОЛОГИЯ, 2012, том 48, № 3, с. 276-281
UDC 632.938
THE INVOLVEMENT OF Pseudomonas BACTERIA IN INDUCED SYSTEMIC
RESISTANCE IN PLANTS (REVIEW)
© 2012 U. Jankiewicz, M. Ko \ tonowicz
Department of Biochemistry, Warsaw University of Life Sciences, 02-776 Warsaw, Poland e-mail: urszula_jankiewicz@sggw.pl, marzenicakol@o2.pl Received May 24, 2011
This article reviews the most recent results of studies on the mechanism of induced systemic resistance (ISR) elicited in plants by non-pathogenic bacteria of the genus Pseudomonas. Several examples of Pseudomonas strains eliciting resistance against fungal phytopathogens in different species of crop plants are presented. Literature data dealing with bacterial elicitors and the effect of their interaction with plant receptors are quoted. Special focus is focused on the controversial issue of the correlation between the synthesis of pathogenesis-related proteins (PRs) and ISR.
Brief characterization of plant resistance types.
Over a long period of time environmental pressure on plants induced the development of mechanisms enabling plants to combat the organisms negatively affecting them. One of these is resistance. Although plants do not have an immune system characteristic for mammals, this term applies to plants as well. In this case, resistance is defined as "the insusceptibility of a plant to infection". Two types of resistance can be distinguished: constitutive (passive), and induced (acquired, active). Constitutive resistance is created by anatomical and physiological barriers. In turn, the state of enhanced plant defense, appearing as a consequence of the activity of a biotic or abiotic factor, is termed induced resistance. Usually enhanced resistance is not limited to the site at which a particular agent acts. A signal induced at one site spreads system-ically to other organs, as a result of which the whole plant is prepared for an attack by a pathogen [1, 2]. Two kinds of induced resistance with systemic range can be distinguished: systemic acquired resistance (SAR) and induced systemic resistance (ISR). SAR is induced by pathogens eliciting necrotic changes in the plant tissues. Their presence within tissues results in increased synthesis of salicylic acid (SA), which in turn activates the expression of pathogenesis-related (PR) genes. The products of the expression of these genes participate in the destruction of the plant pathogen [3, 4]. On the other hand, ISR is mediated by non-pathogenic bacteria and fungi that stimulate plant growth. These are known as the plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). They inhabit the root system, in which resistance is induced. The signaling pathway initiated in the underground plant organs, embraces the above ground parts as well. Jasmonic acid (JA) and ethylene (ET) play an important role in this pathway [5, 6]. These plant hormones participate in the activation of genes, whose transcrip-
tion and translation lead to the formation of compounds that have negative effect on pathogens and plant pests. Activation occurs only after the plant organism is attacked by the phytopathogen [7, 8]. Genes respond more rapidly in the presence of JA and ET and their expression is both enhanced and faster. Resistance thus seems to have economic advantages for the overall plant defense response [9]. PGPR strains, after effective colonization and induction of resistance, maintain a plant in a state of elevated readiness to the occurrence of a pest in the general sense. Thus, there is no constitutive production of compounds by the plant which limits energy losses at the metabolic level [10]. The expression of induced systemic resistance (ISR) has been observed for different plant species, not only in dicotyledons (string bean, Arabidop-sis, carrot, tobacco, radish and tomato), but also in monocotyledons (corn, rice) [11]. It appears that the mechanism of this plant resistance is effective in combating bacteria, fungi, viruses [12], nematodes [13] and insects [14].
ISR inducers. The participation of Pseudomonas bacteria, as well as of other bacteria classified to the PGPR in the induction of systemic resistance, is related to the production by these non-pathogenic bacteria of so-called elicitors (inducers, determinants), activating the defense responses of plant cells. In the case of an immune response to pathogens these compounds have been termed pathogen-associated molecular patterns (PAMPs). Frequently in multicellular organisms recognition of PAMPs by pathogenesis-re-lated proteins (PRs) also enhances a SAR response [16]. A considerable diversity of the elicitors involved in ISR has been observed. They include the building blocks of bacterial cells as well as extracellular compounds synthesized by the microbes [17]. In the case of Pseudomonas they are: siderophores, flagellin, li-popolysaccharides (LPS) [18], an N-alkylated ben-
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zoamine derivative [19], SA, 2,3-butanediol, [20] and antibiotics, including 2,4-diacetylphloroglucinol and pyocyanin [21, 22]. Two important aspects of ISR induction should be pointed out — the time needed for this type of resistance to develop and the number of bacterial cells required for its initiation. ISR can be elicited only when the number of bacterial cells reaches a minimal value equal to 105 CFU/g (colony forming unit/g) of plant root and time of root colonization by the bacteria is not shorter than a few days [23].
Interaction between inducers and plant receptors.
The mechanism of ISR induction is still unclear. It is thought that the induction of resistance in plants by rhizobacteria is analogous to the mechanism of resistance elicited by pathogens in eukaryotic cells. In both cases receptors are recognized by elicitors [24]. The induction of ISR is not a random process. A certain specificity in recognition and binding of PGPR elici-tors to the corresponding root receptor of a given plant species is observed [25]. It appears that some bacterial strains, such as P. fluorescens WCS417r, demonstrate a high effectiveness of the binding in different plant species, whereas others, e.g. P. fluorescens WCS358, are characterized by narrow specificity. The former strain induces resistance via LPS in such plants as Arabidop-sis [26] carnation [27], radish [28]. In turn, flagellin and LPS of P. fluorescens WCS358 are effective inducers of resistance in Arabidopsis but not in the pea and tomato [18]. Initially it was thought that a flagellin conservative motif of all PGPR could be recognized by the most plants. However, studies using two different Pseudomonas strains contradict this theory. P. fluorescens WCS358 and WCS374 strains both have a flagel-lum but only the former induces ISR in Arabidopsis thaliana [26]. As yet, the nature of the receptor binding a given elicitor is not known. It has been assumed that flagellin may be identified by the receptor LRR-NBS (leucine-rich repeat-nucleotide binding site). In Arabidopsis LRR-NBS binds to the most conserved domain of flagellin, triggering a mitogen-activated protein (MAP) kinase pathway. Ultimately, several phosphorylations lead to the formation of a protein belonging to the WRKY family that is a group of proteins being transcription factors for genes encoding proteins involved in defense mechanisms of the plant cell [29].
ISR signaling pathway elicited by P. fluorescens WCS417r. The binding between a root receptor and the PGPR determinant results in activation of ISR signaling pathway. A. thaliana, ecotype Columbia (Col) is a model plant for which this process is studied in detail. This particular species is distinguished by the best studied genetic profile of the interactions between a microorganism and a plant [30]. To induce resistance, Arabidopsis roots were colonized by P. fluorescens WCS417r. A characteristic trait of the strain is its effectiveness in inhibiting the growth of pathogens of not only the model plant [6, 31].
Local response — ETand MYB72-dependent signaling pathway. ET is one of the first elements of a signaling pathway initiated by P. fluorescens WCS417r in the Arabidopsis root. This compound was found to be indispensable for the occurrence of resistance in the above ground plant organs [32]. Besides ET, gene MYB72 also played an important role in the early signaling steps of ISR [33]. It appears that P. fluorescens WCS417 elicits the activation of the transcription of MYB72 (as well as of 96 other genes) in the root. MYB72 belongs to the R2R3-MYB family of genes in the Arabidopsis genome and encodes the transcription factor TF MYB 72. The expression of these genes results in the formation of proteins R2R3-MYB, whose presumable function is related to tolerance to stress, regulation of cell death and resistance to pathogens
[34]. It has been reported that the presence of gene MYB72 is required in the initial stages of ISR induction. This was confirmed in studies using plant mutants carrying the recessive form of the gene, in which bacteria did not elicit ISR [8]. It was also observed that overexpression of gene MYB72 did not translate to increased level of resistance to such pathogens as P. sy-ringae pv tomato, Hyaloperonospora parasitica, Alternaria brassicicola and Botrytis cinerea. This allows concluding that initiation of MYB72 requires the participation of an additional factor for initiating ISR. In view of the fact that under in vitro conditions an interaction between MYB72 and ethylene-insensitive3-like 3 protein (EIL3) has been observed, the latter has been suggested to be the putative factor. EIL3 is a transcription factor of the EIN3 family. Close homologs of EIN3 are transcription factors EIL1 and EIL2 participating in regulation of the ethylene-dependent signaling pathway [35].
Systemic signaling response. The signaling pathway locally initiated by P. fluorescens strain WCS417r in the root spre
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