Chitin, a polymer of N-acetyl-D-glucosamine, is an important component of fungal pathogenicity, since fungal pathogens with defects in chitin synthesis are significantly less virulent on the original susceptible hosts.^5,24 Although plants lack chitin, they do secrete chitin-degrading enzymes.^18,22 During fungal infection, plant cells secrete chitinases that release chitin fragments (chitooligosaccharides or chitin oligomers) from fungal cell walls that can act as an elicitor to induce plant innate immunity against the invading pathogen.^{3,18,22,23,25} In agreement with this, overexpression of chitinase in plants led to enhanced resistance to fungal pathogens.^4,11,18 Furthermore, pretreatment of plants with chitooligosaccharides enhances plant resistance against various pathogens.^26,29 Additionally, recent gene expression profiling studies demonstrated that chitooligosaccharides were a potent regulator of plant gene expression.^6,20,29,30 All this suggests that a chitin perception and signal transduction pathway is present in plants to mediate plant disease resistance.

The identification of the chitin receptor(s) complex is pivotal for our understanding of the chitin signaling pathway. Previously, several chitin-binding proteins were detected using biochemical approaches.^7,10,17 Recently, Kaku et al.,¹³ showed that a LysM domain-containing protein CEBiP (chitin elicitor binding protein) binds chitin and plays a critical role in chitin signaling in rice. Since this CEBiP protein does not have an obvious intracellular domain, it very likely needs a partner, such as a receptor-like kinase, to translate the perceived chitin signal into intracellular events. Indeed, very recently, Miya et al.,¹⁶ and Wan et al.,²⁹ independently reported that a LysM domain-containing receptor-like kinase 1(LysM RLK1)/chitin-elicitor receptor kinase 1 (CERK1) is critical for chitin signaling in Arabidopsis. Insertional mutations in this gene blocked the induction of virtually all chitin-responsive genes (CRGs) and resulted in greater susceptibility to fungal pathogens. LysM RLK1/CERK1 is a receptor-like kinase with an extracellular LysM domain, which was first identified as a protein module that binds peptidoglycan in bacteria.^2,12 Indeed, the legume LysM RLKs, NFR1 and NFR5 in Lotus japonicus, were previously shown to be the putative receptors of Nod factors, which are lipo-chitin molecules essential for nodulation.^15,19 Therefore, LysM RLK1/CERK1 very likely plays a critical role in chitin perception, probably through forming a receptor complex with another protein, such as an OsCEBiP-like protein. The Arabidopsis genome harbors three CEBiP-like proteins. We are currently examining the role of each CEBiP-like protein in chitin signaling in Arabidopsis.

Mitogen-activated protein kinases (MAPKs) are important in modulating the response of plant cells to both internal and external stimuli, including pathogen infection.^9,27 Increasing data suggest that they may also play an important role in chitin signaling.^23,28,30 In particular, MAP kinase 3 and 6 (MPK3/6) were shown to be rapidly activated by chitin in Arabidopsis and their activation depended on upstream MAPK kinases (MKK4 and 5),^21,28 suggesting that a MAPK cascade consisting of MKK4/5-MPK3/6 may be involved in chitin signaling.

Transcription factors (TFs) are critical in reprogramming gene expression in plant cells in response to various stimuli. Previous DNA microarray studies suggested plant cells can reprogram gene expression in response to chitin elicitation.^6,20 Recently, the use of quantitative transcriptase-polymerase chain reaction (qRT-PCR), in conjunction with DNA microarrays, revealed 118 TF genes responsive to chitin.¹⁴ Interestingly, many of these TFs were previously implicated in plant defense (e.g., various WRKY TF genes⁸). The induction of a number of the chitin responsive TF genes (e.g., WRKY53 and WRKY33) was previously shown to depend on the activation of the aforementioned MAPK cascade,²⁸ suggesting that these TFs may play an important role in regulating other chitin-responsive genes (CRGs). Considering that a large number of TF genes are induced by chitin, one might expect a significant number of plant genes to respond to chitin elicitation. Indeed, the mRNA levels of approximately 900 Arabidopsis genes were shown by DNA microarray analysis to respond to chitin elicitation.^20,29 Likewise, in rice, a large number of genes were also shown to be regulated by chitin.⁶ Consistent with the elicitor role of chitin, many of these regulated genes are defense-related genes, such as those encoding pathogenesis-related proteins, WRKY TFs, and disease resistance proteins (20,29). Furthermore, the knockout of several selected CRGs (e.g., two disease resistance-like protein genes and a putative E3 ligase gene) led to increased susceptibility to the powdery mildew fungal pathogen Erysiphe cichoracearum,²⁰ suggesting a connection between the gene induction by chitin and fungal resistance.

All together, the above findings strongly support that a chitin signaling pathway, as outlined in Figure 1, is present in plant cells to mediate chitin perception and plant disease resistance. Noteworthy, this pathway is similar to the flagellin and EF-Tu-mediated pathways,^1,31 with the major difference in their corresponding receptors. This is also supported by the observation that a large number of genes (441 genes) were commonly upregulated by all three stimuli.²⁹ This similarity suggests that plant cells may have evolved a way to save energy and genetic resources to deal with different pathogens by detecting different PAMPs via different receptors and then employing a similar, conserved pathway to combat different pathogens. Interestingly, the chitin signaling pathway appears to be independent of the pathways mediated by SA, JA and ethylene, at least at the early time points.^29,30 However, the detailed relationships, especially at the later time points, between these pathways and those responsive to PAMPs needs to be further investigated.

Open in a separate window

Figure 1

Chitin signaling pathway vs. flagellin-and EF-Tu-mediated pathways. Increasing evidence suggests these pathways share a common, downstream pathway to mediate plant innate immunity against different pathogens, although the initial stages are different, as partially reflected by different receptors. Blue circle: LysM motif, Yellow column: leucine-rich repeats; Red oval: kinase domain.