Roles of plant hormones in the regulation of host-virus interactions

Abstract

Hormones are tuners of plant responses to biotic and abiotic stresses. They are involved in various complicated networks, through which they modulate responses to different stimuli. Four hormones primarily regulate plant defence to pathogens: salicylic acid (SA), jasmonic acid (JA), ethylene (Et) and abscisic acid (ABA). In susceptible plants, viral infections result in hormonal disruption, which manifests as the simultaneous induction of several antagonistic hormones. However, these antagonistic hormones may exhibit some sequential accumulation in resistant lines. Virus propagation is usually restricted by the activation of the small interfering RNA (siRNA) antiviral machinery and/or SA signalling pathway. Several studies have investigated these two systems, using different model viruses. However, the roles of hormones other than SA, especially those with antagonistic properties, such as ABA, have been neglected. Increasing evidence indicates that hormones control components of the small RNA system, which regulates many processes (including the siRNA antiviral machinery and the microRNA system) at the transcriptional or post-transcriptional level. Consequently, cross-talk between the antagonistic SA and ABA pathways modulates plant responses at multiple levels. In this review, we summarize recent findings on the different roles of hormones in the regulation of plant-virus interactions, which are helping us to elucidate the fine tuning of viral and plant systems by hormones.

Keywords: defence pathways; host-virus interaction; plant hormones; plant virus.

Figure 1

Hormone–virus inter‐relations: general effects of hormones on plant defence against viruses. Hormones in light green circles have positive effects on defence against viruses. Salicylic acid (SA) signalling, which is tightly connected to the majority of NB‐LRR (NUCLEOTIDE‐BINDING‐LEUCINE‐RICH REPEAT) genes, constitutes the major defensive pathway against viruses. The recognition of viral effectors by R proteins initiates defensive pathways, including the activation of SA and small interfering RNA (siRNA) pathways, induction of reactive oxygen species (ROS) and the hypersensitive response (HR) (Baebler et al., 2014). These responses limit viral spread in necrotic lesions, and activate siRNA antiviral mechanisms. SA activates systemic acquired resistance (SAR) and siRNA machinery at distal sites (Alamillo et al., 2006; Loake & Grant, 2007; Vlot et al., 2009). Cytokeratins (CKs) improve plant defences to biotrophs in an SA‐mediated manner. CK‐responsive factors, such as ARR3 (ARABIDOPSIS RESPONSE REGULATOR 3), ARR4, ARR5, ARR6, ARR8 and ARR9, are involved in the cross‐talk between SA and CKs (Argueso et al., 2012). Brassinosteroids (BRs) act independently of SA in enhancing resistance to biotrophs. Hormones in red circles have primarily negative effects on plant defences to viruses. Auxin is known to antagonize the SA pathway, and a subset of Auxin response factors (ARFs) is important for the replication and movement of certain viruses, such as Tobacco mosaic virus (TMV) (Padmanabhan et al., 2008, 2005). Ethylene (Et) also antagonizes the pathway downstream of SA signalling, and is involved in symptom development on Cauliflower mosaic virus (CaMV) infection, systemic movement of TMVcg and the formation of necrotic lesions following infection by other viruses (Chen et al., 2013, Geri et al., 2004). Jasmonis acid (JA) and abscisic acid (ABA) have both positive and negative effects on defence against viruses; JA seems to support plant defence at early stages of infection, but, if it is induced or applied at later stages, it decreases plant resistance (Garcia‐Marcos et al., 2013, Pacheco et al., 2012). ABA has multifaceted roles in plant defence; on the one hand, it increases callose deposition on plasmodesmata (PD) and restricts cell‐to‐cell movement of viruses, such as TMV and Tobacco necrosis virus (TNV), whereas, on the other, it antagonizes the SA pathway and reduces resistance at local sites of infection by repressing HR induction, decreasing the production of ROS and SA, and weakening distal SAR and siRNA systems (Alazem et al., 2014, Iriti & Faoro, 2008, Whenham et al., 1986).

Figure 2

Roles of abscisic acid (ABA) in modulating plant defence and hormone responses. I. SA pathway: ABA suppresses the salicylic acid (SA) pathway. Certain temperature‐sensitive R proteins [Toll/interleukin‐1 receptor‐nucleotide‐binding site‐leucine‐rich repeat (TIR‐NBS‐LRR)‐type] translocate from the cytosol to the nucleus at low temperatures. In ABA‐deficient mutants, such proteins lose their temperature sensitivity, localize in the nucleus and act against their specific pathogens (Mang et al., 2012). Pretreatment with ABA suppresses certain genes involved in SA biosynthesis and signalling (e.g. SID1 and NPR1), and thereby negates SA‐induced resistance against biotrophic pathogens (Yasuda et al., 2008). II. miRNA pathway: ABA affects microRNA (miRNA) biosynthesis at several levels. Certain mutants, such as hyl1 (HYPONASTIC LEAVES 1) and dcl1 (DICER‐LIKE 1), are hypersensitive to ABA, whereas AGO1 homeostasis is regulated by ABA through miR168a. At the protein level, ABA stabilizes CBP20 and CBP80 (CAP‐BINDING PROTEINS 20 and 80), which are required for capping of the 5′ untranslated region (UTR) of synthesized miRNAs (Kim et al., 2008; Li et al., 2012). III. siRNA machinery: ABA indirectly affects the small interfering RNA (siRNA) pathway. The mutants dcl2, dcl3, dcl4 and sgs3 (SUPPRESSOR OF GENE SILENCING 3) are hypersensitive to ABA (Zhang et al., 2008).