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Review
. 2019 Jun 26:10:1460.
doi: 10.3389/fmicb.2019.01460. eCollection 2019.

Plant Antiviral Immunity Against Geminiviruses and Viral Counter-Defense for Survival

R Vinoth Kumar  1
Affiliations
Review

Plant Antiviral Immunity Against Geminiviruses and Viral Counter-Defense for Survival

R Vinoth Kumar. Front Microbiol. .

Abstract

The family Geminiviridae includes plant-infecting viruses whose genomes are composed of one or two circular non-enveloped ssDNAs(+) of about 2.5-5.2 kb each in size. These insect-transmissible geminiviruses cause significant crop losses across continents and pose a serious threat to food security. Under the control of promoters generally located within the intergenic region, their genomes encode five to eight ORFs from overlapping viral transcripts. Most proteins encoded by geminiviruses perform multiple functions, such as suppressing defense responses, hijacking ubiquitin-proteasomal pathways, altering hormonal responses, manipulating cell cycle regulation, and exploiting protein-signaling cascades. Geminiviruses establish complex but coordinated interactions with several host elements to spread and facilitate successful infection cycles. Consequently, plants have evolved several multilayered defense strategies against geminivirus infection and distribution. Recent studies on the evasion of host-mediated resistance factors by various geminivirus proteins through novel mechanisms have provided new insights into the development of antiviral strategies against geminiviruses. This review summarizes the current knowledge concerning virus movement within and between cells, as well as the recent advances in our understanding of the biological roles of virus-encoded proteins in manipulating host-mediated responses and insect transmission. This review also highlights unexplored areas that may increase our understanding of the biology of geminiviruses and how to combat these important plant pathogens.

Keywords: antiviral response; hormone signaling; macromolecular trafficking; post-translational modification; vector transmission; viral pathogenesis; virus.

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Figures

FIGURE 1
FIGURE 1
Genomeorganization of viruses belonging to different genera of the family, Geminiviridae. The unfilled circles indicate the origin of replication, and all the coding regions are labeled according to the function of their respective gene products viz., C1/AC1: replication associated protein (Rep); C2/AC2: transcriptional activator protein (TrAP); C3/AC3: replication enhancer protein (REn); V1/AV1: coat protein (CP); V2/AV2: pre-coat protein; BC1: movement protein (MP) and BV1: nuclear shuttle protein (NSP). CR, SCR, SIR, and LIR refer to Common Region, Satellite Conserved Region, Short-Intergenic Region, and Long-Intergenic Region, respectively.
FIGURE 2
FIGURE 2
Cellular trafficking of geminiviral replicated genomes within and between plant cells for (A) monopartite geminiviruses and (B) bipartite geminiviruses. In the infected cells, circular geminiviruses replicate via a dsDNA intermediate, a replicative form of the viral genome. The CP is needed for the export of viral DNA from the nucleus and encapsidation for systemic spread. (A) In monopartite geminiviruses, the CP-bound viral genome (after uncoating) is imported from the cytoplasm to the nucleus by Kapα1 via nuclear pore complex. After replication, the CP binds to newly synthesized viral DNA and facilitates the export of viral genomes to the cytoplasm. For trafficking between cells, the V2 (likely C4) protein binds to this viral DNA-CP complex and traffics it through the endoplasmic reticulum to dock at the PD in the PM. (B) The viral genome-CP complex of bipartite begomoviruses is imported from the cytoplasm to the nucleus by Impα, and nucleo-cytoplasmic shuttling of viral DNA is mediated by a NSP and nuclear envelope-associated NIG. Meanwhile, NSI acetylates the CP and reduces its DNA-binding affinity, thereby assisting the binding of NSP to viral DNA. The MP (along with NSP) plays a crucial role in the transfer of viral genomes to the PD via endosomes by interacting with SYTA (CabLCV) or ER-tubules (SLCuV). The interaction of histone H3 with the NSP and MP (BDMV) also possibly facilitates this cell-to-cell transport.
FIGURE 3
FIGURE 3
Multiple roles of C4 protein in regulating the cell cycle and cell division. The C4 protein reprograms the cell cycle either by preventing SKη-mediated degradation of CYCD or by probably degrading cell cycle inhibitors (ICK/KRP). The C4 protein also indirectly regulates cell division by interfering with CLV1-mediated expression of the WUS gene. Further, the expression of WUS gene is reported to inhibit cell division. Thus, by regulating the cell cycle/cell division, the C4 protein provides a favorable environment for virus replication in infected plant cells.
FIGURE 4
FIGURE 4
Consequence of post-translational modification of viral and host proteins during geminiviral pathogenesis. Virus-encoded TrAP inhibits plant defense responses either by modulating the derubylation of CUL1 (removal of RUB, a ubiquitin-like protein, from CULLIN in the active E3 ubiquitin ligase complex inactivates its E3 ligase activity) or by attenuating the degradation of the SAMDC1 enzyme. However, the βC1 protein impairs the ubiquitin degradation pathway and hormonal (jasmonic acid and giberellic acid) signaling by interacting with the E2 conjugating enzyme (UBC3) and SKP1, respectively. Also by inhibiting the kinase activity of MPK4 and MKK2, βC1 protein can possibly prevent the phosphorylation of the target proteins. Furthermore, the NSP is phosphorylated by PERK, which potentiates virus infection by an unknown mechanism. The C1 protein probably helps with virus replication by modulating the SUMOylation of PCNA. Additionally, the C1 protein interacts with histone mono-ubiquitination machinery (UBC2 and HUB1) to facilitate the transcription of viral genes.
FIGURE 5
FIGURE 5
Implication of various approaches employed by host-mediated resistance factors in defense against geminiviruses. Plants implicate protein kinases (GRIK1 and SnRK1) and an autophagy pathway in several stages of the geminivirus infection cycle. Moreover, plant nuclear-bound RPT4 and EML1 inhibit viral transcription by preventing the binding of RNA polymerase II to viral chromatin. Plant kinases also prevent the nucleo-cytoplasmic trafficking of viral genomes through the sequestering of NIG (by WWP) from the cytoplasm to nuclear immune bodies. The NIK-mediated antiviral strategy involves the formation of a phosphorylated L10-LIMYB complex resulting in global translational suppression and prevention of polysome binding to viral transcripts. Membrane-localized BAMs are also employed by plants to assist with the cell-to-cell spread of RNA silencing.
FIGURE 6
FIGURE 6
Insect vector-mediated transmission of geminiviruses. (A) List of different genera of the Geminiviridae family and its associated insect vectors. (B) Interference of MYC2-regulated gene expression by geminiviral proteins to modulate insect transmission. Begomovirus-encoded TrAP binds to ubiquitin and impedes the degradation of JAZ1, whereas the βC1 protein prevents MYC2 from binding to the G-box in the promoter of downstream target genes. As a consequence, the expression of defense-related genes is inhibited, resulting in the improved performance of the vector in virus transmission.
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