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Review
. 2021 May 6;13(5):840.
doi: 10.3390/v13050840.

Geminivirus-Host Interactions: Action and Reaction in Receptor-Mediated Antiviral Immunity

Marco Aurélio Ferreira  1 , Ruan M Teixeira  1 , Elizabeth P B Fontes  1
Affiliations
Review

Geminivirus-Host Interactions: Action and Reaction in Receptor-Mediated Antiviral Immunity

Marco Aurélio Ferreira et al. Viruses. .

Abstract

In plant-virus interactions, the plant immune system and virulence strategies are under constant pressure for dominance, and the balance of these opposing selection pressures can result in disease or resistance. The naturally evolving plant antiviral immune defense consists of a multilayered perception system represented by pattern recognition receptors (PRR) and resistance (R) proteins similarly to the nonviral pathogen innate defenses. Another layer of antiviral immunity, signaling via a cell surface receptor-like kinase to inhibit host and viral mRNA translation, has been identified as a virulence target of the geminivirus nuclear shuttle protein. The Geminiviridae family comprises broad-host range viruses that cause devastating plant diseases in a large variety of relevant crops and vegetables and hence have evolved a repertoire of immune-suppressing functions. In this review, we discuss the primary layers of the receptor-mediated antiviral immune system, focusing on the mechanisms developed by geminiviruses to overcome plant immunity.

Keywords: ETI; NIK1; NIK1 antiviral defense; PAMP-triggered immunity; PTI; effector-triggered immunity; effectors; geminiviruses; viral suppressors.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Genomic organization of geminiviruses (Geminiviridae family): The Geminiviridae family includes nine genera represented by monopartite or bipartite species. LIR denotes the long intergenic region, SIR, the short intergenic region, and CR, the common region. The viral proteins replication initiator protein, Rep (C1), and replication enhancer protein, Ren (C3), are associated with replication, and the transcription activator protein, Trap (C2), with the transcription of viral and host genes; AC4 is a virulence factor. The capsid protein (CP) is indicated in the monopartite and bipartite genomes. In monopartite species, V2 represents the movement protein (MP). In bipartite begomoviruses, MP (BC1) is encoded by the DNA-B that also encodes the nuclear shuttle protein, NSP (BV1), which facilitates the nucleocytoplasmic movement of viral DNA. Bipartite begomoviruses are often associated with DNA satellites: the alphasatellites, which encode a replication protein (Rep), and the betasatellites that encode the virulence-related βC1 protein. A-rich is a conserved adenine rich region of the DNA satellites, and SCR is the satellite conserved region. As with βC1, the encoded products of ORFs V1, V2, BV1, C2, C4, and AC3 from some geminivirus species are also reported as virulence factors. Adapted from [19].
Figure 2
Figure 2
Domain organization of the LRR-RLK subfamily II members: Leucine-rich repeat receptor-like kinases (LRR-RLKs) belonging to the subfamily II harbor a signal peptide (SP) and an LRR domain with 5 repeats at the N-terminal extracellular region, a transmembrane segment (TM), and a kinase domain at the cytosolic side. The relative positions of the nucleotide-binding site (NBS), the active site (AS), and the activation loop (AL) of the kinase are indicated. In the A-loop sequence comparison of LRR-RLK subfamily II representatives, the phosphorylation-dependent activation site of the kinase is highlighted in red.
Figure 3
Figure 3
Receptor-mediated innate immunity against geminiviruses and counterdefensive viral activities: Like any other plant virus, geminiviruses are obligate intracellular parasites delivered into the cytoplasm of plant cells by the insect vector. The viral particle unpacking is likely to occur in the cytoplasm. Then, viral (v) CP-bound ssDNA is directed to the nucleus where v-ssDNA is converted to v-dsDNA to replicate the viral genome via the rolling circle mechanism and for transcribing the viral genes. The geminivirus infection both induces and suppresses the plant innate immunity. Geminivirus-derived nucleic acids may act as a viral PAMP to induce the dimerization of a yet-to-be-identified PRR with its coreceptor SERK1 to initiate the PTI signaling pathway. SERK1 has been shown to be required for viral PTI elicited by dsRNA, but no direct evidence exists for its participation in geminiviral PTI. FLS2 may function as a geminiviral PRR because C4 acts as a virulence effector by binding to FLS2 and inhibiting early PTI responses. Likewise, the betasatellite βC1 virulence effector affects the MAPKinase cascade. In a resistant Phaseolus vulgaris genotype to bean dwarf mosaic virus (BDMV), NSP acts as an avirulence factor; it is recognized by an unknown intracellular receptor and activates HR, cell death, and ETI-like responses. A typical NLR intracellular receptor of ETI (TYNBS1) confers resistance to TYLCV, yet the cognate geminivirus avirulence factor is unknown. Rep has been shown to induce ROS and SA-mediated defenses. As virulence effectors, C4 and C2 counter ETI activation by suppressing HR and cell death. C4 also inhibits SA-mediated defenses. The question marks indicate either events not well clarified or unknown. Solid line arrows describe experimentally demonstrated events and dotted line arrows denote genetically implicated events. See Figure 1 for the designations of the viral proteins. The figure was created with BioRender 101 (BioRender.com; https://biorender.com/, accessed on 1 April 2021).
Figure 4
Figure 4
NIK1-mediated antiviral signaling and crosstalk with antibacterial immunity: In noninfected cells, (1) NIK1 pools are bound to the PRR FLS2 and the PTI coreceptor BAK1 to prevent autoimmunity. (2) At the onset of infection, CP-bound ssDNA is transported to the nucleus for replication of the viral genome and transcription of viral genes. (3) In the infected cells, geminivirus-derived nucleic acids act as viral PAMPs and induce the dimerization of NIK1 with itself or with another unknown receptor (PRR-like) for transphosphorylation of the kinase intracellular domains. NIK1 phosphorylation at Thr-474 activates the kinase that in turn mediates the RPL10 phosphorylation. (4) Phosphorylated RPL10 is redirected to the nucleus, where it interacts with LIMYB to repress the expression of ribosomal proteins (RBs) and translational machinery-related genes, culminating in suppressing host and viral mRNA translation. (5) NSP counters this antiviral mechanism’s activation by binding to the NIK1 kinase domain, thereby preventing NIK1 phosphorylation and activation. (6) Bacterial infection (Pseudomonas spp) provides the apoplastic bacterial PAMP flagellin (flg22), which is recognized by PRR FLS2, thereby inducing the formation of the active immune complex FLS2-BAK1 to initiate PTI. FLS2-BAK1-bound NIK1 is then phosphorylated at Thr-474 by the activated BAK1, (7) enhancing NIK1 suppression of PTI but (8) activating the NIK1-mediated antiviral signaling that results in suppression of global translation. (9) C4 from geminiviruses binds to FLS2 and inhibits the early PTI responses and subsequent NIK1 activation creating an environment that favors virus infection. The question marks indicate either events not well clarified or unknown. The figure was created with BioRender 101.
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