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Review
. 2014 Jun;26(6):2285-2309.
doi: 10.1105/tpc.114.125419. Epub 2014 Jun 10.

Intervention of Phytohormone Pathways by Pathogen Effectors

Kemal Kazan  1 , Rebecca Lyons  2
Affiliations
Review

Intervention of Phytohormone Pathways by Pathogen Effectors

Kemal Kazan et al. Plant Cell. 2014 Jun.

Abstract

The constant struggle between plants and microbes has driven the evolution of multiple defense strategies in the host as well as offense strategies in the pathogen. To defend themselves from pathogen attack, plants often rely on elaborate signaling networks regulated by phytohormones. In turn, pathogens have adopted innovative strategies to manipulate phytohormone-regulated defenses. Tactics frequently employed by plant pathogens involve hijacking, evading, or disrupting hormone signaling pathways and/or crosstalk. As reviewed here, this is achieved mechanistically via pathogen-derived molecules known as effectors, which target phytohormone receptors, transcriptional activators and repressors, and other components of phytohormone signaling in the host plant. Herbivores and sap-sucking insects employ obligate pathogens such as viruses, phytoplasma, or symbiotic bacteria to intervene with phytohormone-regulated defenses. Overall, an improved understanding of phytohormone intervention strategies employed by pests and pathogens during their interactions with plants will ultimately lead to the development of new crop protection strategies.

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Figures

Figure 1.
Figure 1.
A Simplified View of Plant–Pathogen Interactions. Pathogen-derived conserved molecules known as MAMPs are detected by plasma membrane–located PRRs, and this recognition triggers PTI. Pathogens interfere with immune signaling through effectors to induce susceptibility, and this is known as effector-triggered susceptibility (ETS). In return, plants have evolved effector recognition proteins (R proteins) that trigger an immune reaction following effector recognition to stop pathogen growth, and this phenomenon is known as ETI.
Figure 2.
Figure 2.
Complex Signaling Interactions among Phytohormone Pathways Regulate Both Disease Resistance and Susceptibility in Plants in an Attacker-Dependent Manner. The plant hormones JA, SA, and ET are primarily involved in plant defense, while ABA, auxins (IAA), CK, BR, GA, and strigolactones (STR) also regulate plant defense, either alone or in conjunction with the primary defense hormones. Pathogens have developed strategies via their effector repertoire to either interfere with or hijack phytohormone pathways to induce resistance or susceptibility. Forward and blunt arrows indicate positive and negative interactions, respectively. See text for details.
Figure 3.
Figure 3.
Effectors from Diverse Pathogens Indirectly Target NPR1, a Master Regulator of SA Signaling, to Promote Disease Development. An exopolysaccharide produced by the necrotrophic fungus B. cinerea (the causative agent of the gray mold disease) activates SA signaling via a tomato NPR1 homolog to exploit the antagonistic crosstalk between SA and JA signaling (El Oirdi et al., 2011). Victorin, a toxin produced by the necrotrophic fungus C. victoriae (the causative agent of Victoria blight disease) indirectly targets NPR1 by binding to TRX-h5, which is required for the nuclear localization of NPR1 (Tada et al., 2008). The 2b protein of CMV targets NPR1 to exploit SA-JA antagonism, while the CMV P6 protein interferes with the nuclear localization of NPR1 to suppress SA and activate JA signaling (Lewsey et al., 2010; Love et al., 2012). Syringolin A, a toxin and proteasome inhibitor produced by the bacterial pathogen P. syringae pv syringae, has been proposed to inhibit the degradation of NPR1 (Schellenberg et al., 2010), which is required for the activation of SA-mediated defenses (Spoel et al., 2009). Unrelated effectors from bacterial (e.g., P. syringae), viral (e.g., Geminivirus), and oomycete (e.g., H. arabidopsidis) pathogens interact with CSN5 (Mukhtar et al., 2011), which in turn interacts with NIMIN1 (Weigel et al., 2005), a regulatory protein and interacting partner of NPR1. See text for details.
Figure 4.
Figure 4.
Pathogen Effectors Target Phytohormone Repressors to Activate Phytohormone Pathways. Under low phytohormone levels, JA, IAA, and GA phytohormone signaling pathways are suppressed by JAZ, AUX/IAA, and DELLA repressors, respectively. Binding of JA, IAA, and GA to their respective receptors COI1, TIR1, and GID1 leads to proteasome-dependent degradation of repressors and subsequent activation of the respective signaling pathways. HopZ1a and HopX1, type III effectors from the pathogenic bacterium P. syringae, physically interact with JAZ repressors to activate the JA pathway (Jiang et al., 2013; Gimenez-Ibanez et al., 2014), which confers susceptibility to this pathogen. Similarly, the type III effector AvrRpt2, a cysteine protease, stimulates proteasome-mediated degradation of AUX/IAA repressors to activate the auxin pathway (Cui et al., 2013), which directly and/or indirectly (e.g., in crosstalk with the SA pathway) provides susceptibility to this pathogen. Similarly, diverse microbes target DELLA proteins to manipulate plant defense and development (Navarro et al., 2008; Jacobs et al., 2011), although effectors that interact with DELLA repressors are currently unknown. See text for additional information.
Figure 5.
Figure 5.
Insect Pests Employ Effectors from Obligate Pathogens to Interfere with Host Phytohormone Pathways. Diverse insects have adopted common strategies in complex tritrophic (insect-microbe-plant) interactions to disable host jasmonate-dependent defenses that confer resistance to insect pests. See text for additional information.
Figure 6.
Figure 6.
Pathogens Manipulate the Signaling and Transport Pathway of Auxin to Promote Disease on Plants. Top panel: Sensing of flg22, a conserved MAMP from the bacterial pathogen P. syringae, activates Arabidopsis miR393, which then attenuates the expression of auxin receptor genes such as TIR1 to suppress the auxin pathway, which promotes susceptibility to this bacteria (Navarro et al., 2006). In return, AvrRpt2, a type III effector from P. syringae, activates the auxin pathway by promoting 26S proteasome-mediated degradation of AUX/IAA repressors (Cui et al., 2013). The TAL effector AvrBs3 from the pathogenic bacteria X. campestris pv vesicatoria activates auxin responses by binding to the promoter of a transcription factor involved in the regulation of auxin responses (Kay et al., 2007). Finally, the effector TENGU produced by insect-transmitted phytoplasma pathogens suppresses auxin responses to alter plant development during disease progression (Hoshi et al., 2009). Bottom panel: PSE1, an RXLR effector secreted by P. parasitica, interferes with root auxin transport during pathogenesis by altering the distribution of PIN4 and PIN7 auxin efflux proteins (Evangelisti et al., 2013). The effector 19C07 produced by cyst nematodes interacts with the Arabidopsis auxin transport protein LAX3 to exploit root auxin transport processes and induce feeding structures. The root image shown in the bottom panel is from an Arabidopsis seedling expressing the auxin reporter DR5-GUS construct (Ulmasov et al., 1997). The blue color (GUS staining) corresponds to auxin rich root regions. See text for details.
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