Transcription Factor Functional Protein-Protein Interactions in Plant Defense Responses

Abstract

Responses to biotic stress in plants lead to dramatic reprogramming of gene expression, favoring stress responses at the expense of normal cellular functions. Transcription factors are master regulators of gene expression at the transcriptional level, and controlling the activity of these factors alters the transcriptome of the plant, leading to metabolic and phenotypic changes in response to stress. The functional analysis of interactions between transcription factors and other proteins is very important for elucidating the role of these transcriptional regulators in different signaling cascades. In this review, we present an overview of protein-protein interactions for the six major families of transcription factors involved in plant defense: basic leucine zipper containing domain proteins (bZIP), amino-acid sequence WRKYGQK (WRKY), myelocytomatosis related proteins (MYC), myeloblastosis related proteins (MYB), APETALA2/ ETHYLENE-RESPONSIVE ELEMENT BINDING FACTORS (AP2/EREBP) and no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), and cup-shaped cotyledon (CUC) (NAC). We describe the interaction partners of these transcription factors as molecular responses during pathogen attack and the key components of signal transduction pathways that take place during plant defense responses. These interactions determine the activation or repression of response pathways and are crucial to understanding the regulatory networks that modulate plant defense responses.

Keywords: biotic stress; signaling cascades; transcription factor.

Figure 1

Two distinct mechanisms of basic leucine zipper containing domain proteins (bZIP) protein actions during plant defense responses. (A) The attack of a biotrophic pathogen triggers a signaling pathway mediated by salicylic acid resulting in the dissociation of the non-expresser of pathogen-related (PR) (NPR1) protein, which translocates to the nucleus and activates the expression of SA-responsive genes by interaction with the TGACGTCA cis-element-binding protein (TGA) bZIP trans-acting factors. The NPR1 protein is ubiquitinated and targeted for degradation by the 26S proteasome complex; (B) Recognition of elicitors after pathogen attack promotes the dissociation of the BZI1/ANK1 and AtbZIP10/LSD1 complexes, favoring the positive transcriptional regulation of hypersensitive response (HR)- and basal defense-related genes.

Figure 2

Types of interactions among APETALA2/ETHYLENE-RESPONSIVE ELEMENT BINDING FACTORS (AP2/ERF) factors and other proteins in response to biotic stress. (A) Association with other transcription factors: the protein AtEBP binds to OCTOPINE SYNTHASE (ocs) ELEMENTS BINDING FACTOR (OBF) protein, which is a bZIP protein, resulting in increased transcription of PR genes; (B) Phosphorylation: the AP2/ERF factor octadecanoid-responsive-Catharanthus-APETALA2-domain protein (ORC1) is phosphorylated by kinase JAM1 and promotes expression of genes related to nicotine synthesis; (C) Dissociation: after ethylene induction or pathogen infection, the protein EREBP dissociates from NLP protein. This dissociation results in the translocation of EREBP to the nucleus and leads to expression of PR genes.

Figure 3

Repression mechanisms of myeloblastosis related proteins (MYB)30 function during pathogen attack. XopDXcv interacts with MYB30 in plant cell nucleus, retaining MYB30 in nuclear bodies and preventing the transcription of the very long chain fatty acid biosynthesis genes (VLCFA) genes. Ubiquitin ligase E3 MYB30-INTERACTING E3 LIGASE1 (E3 MIEL1) interacts with MYB30 in the nucleus and promotes its ubiquitination and consequent degradation by the 26S proteasome complex (UPS26). AtsPLAα binds with MYB30 and they translocate from the cytoplasmic vesicles into the nucleus, but the interaction of AtsPLAα with target DNA is prevented.

Figure 4

The transcription factor, BOTRYTIS SUSCEPTIBLE (BOS), interacts with E3 BOTRYTIS SUSCEPTIBLE1 INTERACTOR (BOI) in the plant cell nucleus. E3 BOI promotes BOS ubiquitination and the consequent degradation by the 26S proteasome complex, restricting the biotic and abiotic stress responses mediated by BOS.

Figure 5

Regulation of jasmonate-responsive gene expression by MYC2 and JAZ proteins. In absence of JA-Ileu, JAZ protein interacts through its N-terminal domain with MYC2, causing the transcription factor to remain inactive. When the JA-Ileu level increases, JA-Ileu binds to Jas domain of JAZ protein and promotes interaction of JAZ protein with COI1 leading to the formation of the SCF^COI1 complex. The SCF^COI1 complex causes ubiquitination of JAZ protein in its Jas domain and the protein is degraded by the 26S proteasome complex. MYC2 is released and promotes transcription of target genes.

Figure 6

Overview of AtWRKY33 interactions during biotic stress responses. During an attack by a necrotrophic pathogen, AtWRKY33 interacts with the proteins SIGMA FACTOR-INTERACTING PROTEIN 1 (SIB1) and SIGMA FACTOR-INTERACTING PROTEIN 2 (SIB2) in the nucleus. These interaction leads to transcription of genes responsive to the pathogen, causing an increased resistance in the plant (in this case against B. cinerea, a necrotrophic fungus). In a second interaction, AtWRKY33 can be phosphorylated by two MITOGEN-ACTIVATED PROTEIN (MAP) kinases, MITOGEN-ACTIVATED PROTEIN KINASE 3 (MPK3) and MPK6. This interaction leads to an increase in the transcription of related genes of camalexin biosynthesis, which is an important pathway utilized by the plant defense against pathogens. Another interaction leads to increased transcription of camalexin related genes. After induction by Pseudomonas syringae or flagellin, the protein MPK4 is activated and phosphorylates its substrate, the MAP KINASE SUBSTRATE1 (MSK1) protein. Phosphorylation of MSK1 releases AtWRKY33 of protein complex allowing the protein to exert its role as a transcriptional activator of plant defense genes. Finally, during attack of fungus B. cinerea, AtWRKY33 interacts with ATG18a in the nucleus. ATG18a is an important protein of the autophagy pathway in Arabidopsis, and its interaction with AtWRKY33 along with the activation of the autophagy pathway is important for signaling the response of plant defense against necrotrophic pathogens.

Figure 7

Repression mechanisms of NAC transcription factors mediated by proteins of pathogens. The effector LxLR (Pi03192) of Phytophthora infestans interacts with two transcription factors from the no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), and cup-shaped cotyledon (CUC) (NAC) family (NAC TARGETED BY PHYTOPHTHORA 1 and 2 (NTP1 and NTP2)) in the endoplasmic reticulum, thus preventing the localization of these factors to the nucleus. The viral capsid protein from the turnip crinkle virus (TCV) virus binds to TCV-INTERACTING PROTEIN (TIP) factor, repressing the expression of defense genes, favoring systemic infection by plant viruses. The helicase domain of the Tobacco mosaic virus (TMV) virus replicase interacts with Arabidopsis transcription activation factor 2 (ATAF2)-suppressing plant defenses.