Different Pathogen Defense Strategies in Arabidopsis: More than Pathogen Recognition

Abstract

Plants constantly suffer from simultaneous infection by multiple pathogens, which can be divided into biotrophic, hemibiotrophic, and necrotrophic pathogens, according to their lifestyles. Many studies have contributed to improving our knowledge of how plants can defend against pathogens, involving different layers of defense mechanisms. In this sense, the review discusses: (1) the functions of PAMP (pathogen-associated molecular pattern)-triggered immunity (PTI) and effector-triggered immunity (ETI), (2) evidence highlighting the functions of salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET)-mediated signaling pathways downstream of PTI and ETI, and (3) other defense aspects, including many novel small molecules that are involved in defense and phenomena, including systemic acquired resistance (SAR) and priming. In particular, we mainly focus on SA and (JA)/ET-mediated signaling pathways. Interactions among them, including synergistic effects and antagonistic effects, are intensively explored. This might be critical to understanding dynamic disease regulation.

Keywords: ETI; PTI; SAR; hormone pathways; pathogen defense; priming; small molecules.

Figure 1

Model of salicylic acid (SA) synthesis and SA signal transduction. Enhanced disease susceptibility 1 (EDS1), phytoalexin-deficient 4 (PAD4), and avrpphb susceptible 3 (PBS3) are involved upstream of SA synthesis, and can be induced by positive SA feedback. The redox state alteration caused by the SA burst leads to the monomerization of non-expressor of PR genes 1 (NPR1). The monomerization of NPR1 by thioredoxins (TRXs) such as TRX-H3 and TRX-H5 cause the translocation of NPR1 in the nucleus and subsequent interaction with the positive transcription activators TGACG sequence-specific binding proteins (TGAs), the negative regulators non-inducible immunity (NIM1)-interacting proteins (NIMINs) and Suppressor of npr1-inducible 1 (SNI1). NPR1 is imported into the nucleus through nuclear pores. S-nitrosoglutathione (GSNO) can facilitate the oligomerization of NPR1. During systemic acquired resistance (SAR), the kinase SnRK2.8 is required for the phosphorylation of NPR1, which is not triggered by SA; it is triggered by an unknown signal. A possible working model would be that SA triggers the formation of NPR1 monomers. Then, NPR1 monomers are phosphorylated by sucrose non-fermenting 1 (SNF1)-related protein kinase 2.8 (SnRK2.8) for its nuclear import. The transcription factor whirly 1 (WHY1) is probably involved in the NPR1-independent SA response. Suppressor of SA insensitivity 2 (SSI2) is a negative regulator, independent from NPR1, which regulates the SA-mediated response. Overexpression of glutaredoxin C9 (GRXC9) could regulate the SA pathway independent from NPR1. Pathogen-related 1 (PR1), PR2, and PR5 are SA-responsive marker genes. Activation (closed arrowhead), suppression (⊥), and important genes are indicated.

Figure 2

Model of biosynthesis and signal transduction of jasmonic acid (JA) and ethylene (ET). JA and ET can synergistically activate ethylene insensitive 3 (EIN3) and ethylene insensitive 1 (EIL1), which are positive regulators of ERF1 and octadecanoid-responsive Arabidopsis AP2 59 (ORA59), leading to the induction of plant defensin 1.2 (PDF1.2). The active form jasmonoyl-l-isoleucine (JA-Ile) can be recognized by coronatine insensitive 1 (COI1) and the co-receptor Inositolpentakis phosphate 5 (InsP5), causing the degradation of jasmonate ZIMs (JAZs). There are two antagonistic branches in the JA response: the MYC branch and the ERF branch. JAZ proteins can suppress the activity of MYC2, the positive regulator of Vegetative storage protein 2 (VSP2), by enrolling the negative regulator Topless (TPL) via the novel interactor of JAZ (NINJA). MYC2 can directly interact with mediator 25 (MED25, which is a subunit of the mediator. MYC2 can activate the expression of NAC domain containing proteins (ANACs) to upregulate VSP2. MYC3 and MYC4 can activate JA response additively with MYC2 by binding to the G-box. JAZs could also suppress the activity of jasmonate associated MYC2 like proteins (JAMs), which are a group of transcriptional repressors that could bind to the MYC2 target sequence G-box to negatively regulate the JA response. The MYC2 protein is regulated at protein levels. MYC2 can be ubiquitinated during the JA response for degradation. Thus, JA-mediated defense is suppressed. Conversely, MYC2 can be inversely deubiquitinated to stay stable, triggering a positive regulation on JA response. In the ERF branch, JAZs can inhibit the activity of EIN3 and EIN3-like 1 (EIL1) by direct association with them and enrollment of the histone deacetylase 6 (HDA6). In the ET pathway, there are five ethylene receptors localized in the ER membrane. A copper ion interacts with the ethylene-binding domain. The interaction is required for high-affinity ethylene-binding activity. By binding to ET, constitutive triple response 1 (CTR1) is deactivated by ET receptors. CTR1 can inhibit EIN2, which activates EIN3 and EIL1 by preventing their degradation of them via EIN3-binding F box protein 1 and 2 (EBF1 and EBF2). Activation (closed arrowhead), suppression (⊥), and important genes are indicated.

Figure 3

Interactions between the SA and the JA/ET pathways. ET can synergistically induce PR1 via an unknown mechanism. SA and JA/ET are mostly antagonistic to each other. On the left-hand (SA) side, the cytosolic localization of NPR1 is sufficient for the suppression of the JA/ET response. Some components that are regulated by NPR1, such as WRKY62, TGAs, and glutaredoxin 480 (GRX480), can confer the suppression on the JA response. Some WRKYs such as WRKY50, WRKY51, and WRKY70, can suppress the JA response independent from NPR1. The suppression of the JA pathway by the SA pathway is downstream of JA synthesis, having no influence on JAZs accumulation; however, it results in the degradation of ORA59. On the right-hand (JA) side, JA can suppress the SA response by inducing ANACs, which are regulated by MYC2. ANACs can inhibit isochorismate synthase 1 (ICS1); however, they can enhance the basal transcript level of the SA methyl transferase 1 (BSMT1) and UDP-glucosyltransferase 74F2 (UGT74F2) to elevate SA accumulation. Furthermore, EIN3 and EIL1 can suppress ICS1 activity by directly binding to the promoter of ICS1. Activation (closed arrowhead), suppression (⊥), and important genes are indicated.