Manipulation of the Plant Host by the Geminivirus AC2/C2 Protein, a Central Player in the Infection Cycle

Abstract

Geminiviruses are a significant group of emergent plant DNA viruses causing devastating diseases in food crops worldwide, including the Southern United States, Central America and the Caribbean. Crop failure due to geminivirus-related disease can be as high as 100%. Improved global transportation has enhanced the spread of geminiviruses and their vectors, supporting the emergence of new, more virulent recombinant strains. With limited coding capacity, geminiviruses encode multifunctional proteins, including the AC2/C2 gene that plays a central role in the viral replication-cycle through suppression of host defenses and transcriptional regulation of the late viral genes. The AC2/C2 proteins encoded by mono-and bipartite geminiviruses and the curtovirus C2 can be considered virulence factors, and are known to interact with both basal and inducible systems. This review highlights the role of AC2/C2 in affecting the jasmonic acid and salicylic acid (JA and SA) pathways, the ubiquitin/proteasome system (UPS), and RNA silencing pathways. In addition to suppressing host defenses, AC2/C2 play a critical role in regulating expression of the coat protein during the viral life cycle. It is important that the timing of CP expression is regulated to ensure that ssDNA is converted to dsDNA early during an infection and is sequestered late in the infection. How AC2 interacts with host transcription factors to regulate CP expression is discussed along with how computational approaches can help identify critical host networks targeted by geminivirus AC2 proteins. Thus, the role of AC2/C2 in the viral life-cycle is to prevent the host from mounting an efficient defense response to geminivirus infection and to ensure maximal amplification and encapsidation of the viral genome.

Targets and Mechanisms of Geminivirus Silencing Suppressor Protein AC2

“…A phosphomimic mutation of the S 109 reduced viral DNA accumulation and delayed symptom appearance in Arabidopsis, thus revealing phosphorylation of viral protein as a host defense mechanism against an invading virus (Shen et al, 2014). Guerrero et al (2020) report that AC2 of all old world begomoviruses and cutoviruses C2 lack the S 109 residue. While majority of the new world begomovirus AC2s possess the conserved SnRK1 phosphorylation site, some new world begomoviruses including TGMV AC2 lack the S 109 residue and hence are not phosphorylated.…”

“…The arms race between silencing and silencing suppression results in resistance or susceptibility to the pathogen. Geminiviruses encode several proteins namely AC2/C2, AC4/C4, AV2/V2, βC1, and Rep that suppress RNA silencing by targeting various components of the post-transcriptional gene silencing (PTGS) machinery, transcriptional gene silencing (TGS) machinery, and cellular regulatory genes (reviewed in Hanley-Bowdoin et al, 2013;Kumar, 2019;Rishishwar and Dasgupta, 2019;Yang et al, 2019;Guerrero et al, 2020). Of all the known geminiviral suppressor proteins, AC2 is the most well-studied and is known to target multiple plant genes and proteins.…”

“…AC2 of begomoviruses and C2 of curtoviruses act as suppressors of silencing through two broadly classified mechanisms: (i) activation domain-dependent silencing suppression-begomovirus AC2 with a C-terminal acidic activation domain (Figure 2B) is involved in this mechanism and (ii) activation domainindependent silencing suppression, which is manifested by curtovirus C2 which lacks the activation domain (Figure 2D) and certain begomovirus AC2 proteins with deletions of the activation domain (Figure 2C). AC2/C2 also interacts with and inactivates many cellular regulatory proteins to circumvent the innate defense mechanism which is independent of siRNAmediated silencing (Guerrero et al, 2020).…”

Plant Virology Delivers Diverse Toolsets for Biotechnology

“…In this process, plant viruses must recruit and utilize the host’s translation apparatus [ 28 ] as well as the host’s energy resources [ 29 ]. Some plant viruses, particularly single-stranded DNA (ssDNA) geminiviruses, rely on host polymerases for genome replication [ 30 , 31 ]. In the third step, viral genome encapsidation occurs to form new virions [ 32 , 33 ].…”

The AC2 Protein of a Bipartite Geminivirus Stimulates the Transcription of the BV1 Gene Through Abscisic Acid Responsive Promoter Elements

“…Plant viruses of the family Geminiviridae are among the most important pathogens of crop plants worldwide [1][2][3][4]. Examples of agriculturally devastating geminiviruses include tomato yellow leaf curl virus (TYLCV) and its close relatives, maize streak virus (MSV), and numerous variants of African cassava mosaic virus [5,6].…”