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In Plant Physiology IN PLANT PHYSIOLOGY Did Silencing Suppression Counter-Defensive Strategy Contribute To Origin And Evolution Of The Triple Gene Block Coding For Plant Virus Movement Proteins? Sergey Y. Morozov and Andrey G. Solovyev Journal Name: Frontiers in Plant Science ISSN: 1664-462X Article type: Opinion Article Received on: 30 May 2012 Accepted on: 05 Jun 2012 Provisional PDF published on: 05 Jun 2012 Frontiers website link: www.frontiersin.org Citation: Morozov SY and Solovyev AG(2012) Did Silencing Suppression Counter-Defensive Strategy Contribute To Origin And Evolution Of The Triple Gene Block Coding For Plant Virus Movement Proteins?. Front. Physio. 3:136. doi:10.3389/fpls.2012.00136 Article URL: http://www.frontiersin.org/Journal/FullText.aspx?s=907& name=plant%20physiology&ART_DOI=10.3389/fpls.2012.00136 (If clicking on the link doesn't work, try copying and pasting it into your browser.) Copyright statement: © 2012 Morozov and Solovyev. This is an open‐access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited. This Provisional PDF corresponds to the article as it appeared upon acceptance, after rigorous peer-review. Fully formatted PDF and full text (HTML) versions will be made available soon. 1 OPINION ARTICLE 2 3 Did Silencing Suppression Counter-Defensive Strategy 4 Contribute To Origin And Evolution Of The Triple Gene Block 5 Coding For Plant Virus Movement Proteins? 6 7 Sergey Y. Morozov*, Andrey G. Solovyev 8 9 Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 10 Russia 11 12 Correspondence: 13 Sergey Y. Morozov, 14 Belozersky Institute of Physico-Chemical Biology, 15 Moscow State University, 16 Moscow119992, 17 Russia 18 [email protected] 19 20 Running title: silencing and evolution of TGB 21 22 Keywords: plant viruses, silencing suppressors, movement proteins, evolution 23 24 25 1 1 Comparison of gene silencing in tissues and whole organisms shows intriguing similarities 2 between plants and animals (Melnik et al., 2011; Molnar et al., 2011; Hyun et al., 2011; 3 Cohen and Xiong, 2011; Jose et al., 2011) despite that they are very different from each other 4 in many aspects related to the cell-to-cell communications (Ritzenthaler, 2011). Interestingly, 5 one of the shared mechanisms is the reprogramming of intracellular silencing pathways and 6 intercellular communications during development of virus infections. As a part of their 7 counter-defensive strategy, viruses encode silencing suppressors to inhibit various stages of 8 the silencing process. These suppressors are diverse in sequence and structure and act via 9 different molecular mechanisms including, particularly, blockage of intercellular and 10 systemic spread of mobile small interfering RNAs (siRNAs) (Li and Ding, 2006; Song et al., 11 2011; Bivalkar-Mehla et al., 2011; Burgyan and Havelda, 2011; Shimura and Pantaleo, 12 2011). Importantly, plant, insect and animal virus suppressors can substitute for each other in 13 different eukaryotic model systems (Schnettler et al., 2008; Jing et al., 2011; Maliogka et al., 14 2012; Zhu et al., 2012). Many viral proteins that in the past were characterized as proteins 15 involved in systemic plant invasion are now known to be suppressors of gene silencing. For 16 example, tombusvirus P19 blocks the local movement of the silencing signal by binding 17 DCL4-dependent 21-nt siRNA. Cucumovirus 2b protein inhibits the systemic movement of 18 RNA silencing by either binding dsRNA/siRNA or inhibiting the slicer activity of AGO1. 19 Potato virus X P25 protein also inhibits the systemic movement of RNA silencing (see Li and 20 Ding, 2006; Burgyan and Havelda, 2011; Shimura and Pantaleo, 2011). Direct link between 21 the viral suppressor activity and the ability of virus to move from cell to cell and long- 22 distance is further strengthened by the discovery of plant movement proteins (MPs) acting 23 also as silencing suppressors (Voinnet et al., 1999; Bayne et al., 2005; Yaegashi et al., 2007; 24 Powers et al., 2008; Lim et al., 2010; Wu et al., 2010; Senshu et al., 2011; Renovell et al., 25 2012). On the other hand, it has been shown that the MPs of certain viruses act as viral 26 enhancers of RNA silencing by promoting the propagation of RNA silencing from cell to cell 27 (Vogler et al., 2008; Lacombe et al., 2010; Amari et al., 2012). 28 29 Unlike Tobacco mosaic virus and many other viruses having a single MP gene, the genomes 30 of a number plant virus genera encode a ‘triple gene block’ (TGB), a specialized 31 evolutionarily conserved gene module involved in the movement of viruses. The TGB-based 32 transport system exploits the co-ordinated action of three polypeptides to deliver viral 33 genomes to plasmodesmata and to accomplish virus entry into neighbouring cells. TGB- 34 encoded proteins are referred to as TGB1, TGB2 and TGB3 (Morozov and Solovyev, 2003; 35 Verchot-Lubicz et al., 2010). We present here a hypothetical model of how interaction of 36 plant viruses with the silencing machinery may contribute to the TGB origin and evolution 37 during adaptation of viruses to land plant hosts. The hypothesis was stimulated by the 38 previous evidence indicating that the suppression of silencing by TGB1 protein encoded by 39 potex- and carlaviruses is not sufficient to allow virus movement between cells, and there 40 must be another function of this protein independent of silencing but required for cell-to-cell 41 movement (Bayne et al., 2005; Lim et al., 2010; Senshu et al., 2011). 42 43 In principle, there are three distinct scenarios for the evolution of viruses: first, evolution 44 from a common ancestral virus accompanying the divergence of host taxonomic groups; 45 second, horizontal transfer of viruses and their genomic elements; third, parallel origin from 46 related genetic elements (Dolja and Koonin, 2011). If we take first principle as the main 47 evolutionary flow for plant plus-RNA viruses, algae (especially those included into the 48 kingdom Viridiplantae) should be considered as hosts for precursors of land plant viruses. It 49 is currently well documented that green algae possess many components that are assumed to 50 be involved in RNA silencing mechanisms in other better studied eukaryotes (Ahn et al., 2 1 2010; Cerutti et al., 2011). Correspondingly, algal viruses should have evolved to acquire 2 silencing suppressors making possible establishing successful infection. However, most green 3 algae-infecting viruses sequenced so far (classified in the virus family Phycodnaviridae) are 4 among the largest known DNA viruses (Weynberg et al., 2011; Van Etten and Dunigan, 5 2012). We are still in the ‘lag phase’ of understanding in algal RNA virology and, as new 6 genomic technologies become more widely used in this field, we will see an exponential rise 7 in number of sequenced plus-RNA algal virus genomes. Metagenomics provide a way to 8 bypass the difficulty of obtaining genomic information about viruses that are hard to retrieve 9 in pure culture. There are large datasets of metaviriomes, and they often can be assembled 10 into nearly complete genomic RNAs to study the enormous diversity of the genes of viruses 11 and to help in the annotation of viral ORFs (Kristensen et al., 2010). 12 13 Until now we have only single example of well-characterized plus-RNA virus from algae 14 closely related to land plants. This is Chara australis virus (CAV) (Gibbs et al., 2011), the 15 largest encoded protein of which shows the relationship with RNA polymerases of 16 benyviruses, while the coat protein - with the coat protein of tobamoviruses, thus reflecting 17 the ancient sister relationship between hosts of these viruses, charophytes and land plants. 18 Two additional CAV ORFs code for non-replicative RNA helicase and a protein of unknown 19 function. Importantly, this CAV helicase is related to CI helicase (SF-II) of ipomoviruses 20 (family Potyviridae) (Fig. 1), which is involved in cell-to-cell movement in addition to 21 replication (Wei et al., 2010). Emergence by CAV genome a second SF-II helicase in 22 addition to unrelated replicative SF-I helicase is intriguing assuming the newly discovered 23 role of cell SF-II helicases in the RNA interference and antiviral host defence (Ulvila et al., 24 2010). Organization of multicellular charophytes is rather close to land plants and they 25 contain plasmodesmata (PD) which are morphologically similar to higher plant PD 26 (Brecknock et al., 2011). Thus we can propose that plus-RNA viruses of unicellular algae in 27 the course of transition of hosts to multicellularity may evolve additional RNA helicase genes 28 (either by shuffling with distantly related viruses or by duplication of helicase domain in own 29 replicase) required for virus genome spread over the plant organism (Fig. 1). 30 31 It is known that plant virus RNA replicases may significantly contribute to virus silencing 32 suppressor activity (Ding et al., 2004; Mine et al., 2010), and RNA helicase domain (Koonin 33 and Dolja, 1993) may play important separate role in this activity (Wang et al., 2012). 34 Similarly, replicative DNA helicases of single-stranded plant DNA viruses may be involved 35 in silencing suppression (Nawaz-Ul-Rehman et al., 2010). The TGB is found in viruses of the 36 ‘alpha-like’ supergroup only (families Virgaviridae, Alphaflexiviridae, Betaflexiviridae and 37 genus Benyvirus) (Koonin and Dolja, 1993; Adams et al., 2009; Verchot-Lubicz et al., 2010), 38 suggesting a specific co-adaptation between replication and movement genes. TGBp1 39 contains an NTPase/helicase sequence domain that is related to the replicative helicases of 40 alpha-like viruses and belongs to helicases of superfamily I (SF-I) (Koonin and Dolja, 1993).
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