Role of alphasatellite in begomoviral disease complex.
Geminiviruses are an emerging group of plant viruses infecting most of economically important crops and ornamental plants throughout the world (Mansoor et al., 2003). Based on the host range, genome organisation and the vector, die Geminiviruses ate classified into seven genera: Becurtovirus, Eragrovirus, Turncutovirus Topocuvirus, Curtovirus, Mastrevirus and Begomovirus (Adam et al., 2013; Brown et al., 2012). However, majority of the members of this family belongs to the genus Begomovirus and are spread by the whitefly, Bemisia tabaci (Briddon and Stanley, 2006). Viruses of tins genus are distributed into two subgroups; bipartite begomoviruses with DNA-A?B genomes and monopardte begomoviruses that have a single DNA chain homologous to the DNA-A of bipartite begomovirus. DNA-A component of bipartite and die single component of monopartite begomoviruses (homologues to die DNA-A) encodes all viral functions required for virus replication, control of gene expression and insect transmission All begomoviruses have a potential stem-loop structure containing die nono-nucleotide sequence TAA/TATT/AC, necessary for replication.
In the last few years alphasatellite, the member of monopartite betasatellite/begomoviruses complexes, with a monomer of approximately 1375 nucleotide sequences, has attracted much attention and has become, probably, the most attentive scientific topic in the study of single stranded DNA (ssDNA) viruses. After the discovery of this satellite in 1999, more than 150 alphasatellite sequences have been deposited in database to date, however, very little is known about their function(s) during begomovirus-satellites infections. Examples of stability and maintaining of the alphasatellite component in natural infection with several begomoviruses complex have been shown several times since its first discovery, but without gaining further insights on their function (Shahid et al., 2014: Amrao et al., 2010; Mubin el al., 2010). Certainly, alphasatellites are nonessential for vims infection and appear to play no major role in the etiology of the infections with which they are associated (Mansoor et al., 1999). However, recent reports showed that some alphasatellites can attenuate disease symptoms caused by begomovirus-betasatellite complexes in the early stages of infection (Idris et al., 2011: Nawazul-Rehman et al., 2010). An overview of the origin and evolution of alphasatellites including the recent advances in understanding their molecular structure and their applications for reverse genetics are discussed.
General characteristics of alphasatellites. Despite that alphasatellites were discovered virtually 15 years ago, very little information is available up til now about its functions). Alphasatellite molecules are mostly associated with monopartite begomovirus-betasatellite complex and also monopartite begomovirus can contain this component frequently (Shahid et al., 2014; Harimalala et al., 2013; Zhou, 2013; Zia-Ur-Rehman et al., 2013; Mubin et al., 2010; Dry et al., 1997). On the contrary, a few bipartite begomoviruses have been reported to be associated with alphasatellite (Satya et al., 2014; Paprotka et al., 2010).
Initially, alphasatellites were found in association with the begomovirus-betasatellite complex from the old world (OW). Nevertheless, some distinctive alphasatellites were recently discovered to be associated with the new world (NW) begomovirus complex (Fiallo-Olive et al., 2012). Alphasatellites are believed to have evolved from satellite-like, Rep-encoding components associated with nanoviruses (Wyant et al., 2012; Briddon and Stanley 2006; Saunders and Stanley, 1999), another family of plant ssDNA viruses. Alphasatellite was also found in association with a yellow vein disease in Ageratum conyzoides (weeds) (Saunders and Stanley, 1999).
Genome, genomic organization and replication mechanism. The size of alphasatellite is between 1,300 bp to 1,400 bp nucleotides in length and has three conserved domains: a hairpin structure, a rolling circle replication initiator protein (Rep) and a rich region (A-rich) (Fig. 1). The hairpin structure has a loop that includes a unique nono-nucleotide sequence, which usually varies from rest of the begomovirus components. TAG/TAT/IAC and differs from the TAA/TAT/TAC sequence of geminiviruses by one nucleotide (G instead of A on a third nucleotide). In both begomoviruses and nanoviruses this sequence contains the origin of replication (ori) and is nicked by the rolling circle replication initiator protein to initiate viral DNA replication. The Rep of alphasatellite is the only single large open reading frame in the virion-sense which is predicted to encode a 315 amino acid product similar to the replication associated protein of nanoviruses. An adenine-rich region (approximately 200 bp with 45-52% adenine content) is also present, which is hypothesised to be a stuffer sequence that serves to fulfill the size constrain imposed by helper virus-mediated movement or encapsidation (Shahid et al., 2014; Zhou, 2013). Alphasatellite can replicate autonomously and its replication is specifically mediated by its Rep (Tao et al., 2004), while the replication of other components including betasatellite, is specifically mediated by the begomovirus Rep. This would suggest a difference in the begomovirus and alphasatellite replication origins. Recently, an alphasatellite associated with Okra leaf curl disease from West Africa (Kon et al., 2009) is highly divergent molecule from previously characterized alphasatellites (Fiallo-Olive et al., 2012; Saunders et al., 2002) indicating geographically isolated evolution of a West African lineage of these satellites. The geographical distribution and the genetic diversity of these satellites are consistent with a long term association with monopartite begomoviruses (Briddon and Stanley, 2006).
[FIGURE 1 OMITTED]
Genetic variability. Most of the monopartite begomovirus-betasatellite complex associated with alphasatellites have been characterised in the OW. Previous studies have shown that cotton leaf curl Multan virus (CLCuMV), cotton leaf curl Burewala virus (CLCuBV), tobacco leaf curl Pusa virus (TbLCuPuV), Ageratum yellow vein virus (AYVV), tobacco curly shoot virus (TbCSV), tomato yellow leaf curl virus (TYLCV), East African cassava mosaic Kenya virus (EACMKnV) and mungbean yellow mosaic virus (MYMV) are usually associated with alphasatellite (Satya et al., 2014; Shahid et al., 2014; Harimalala el al., 2013; Kumar et al., 2011; Singh et al., 2011; Mubin et al., 2010; Xie et al., 2010; Mansoor et al., 1999) (Fig. 2). Recently, different alphasatellites such as cassava mosaic (virus) alphasatellite, Gossvpium darwinii symptomless alphasatellite, Vernonia yellow vein Fijian alphasatellite associated with EACMKnV, and CLCuBV, MYMV were isolated from different hosts i.e., cassava, cucurbits and legumes (Satya et al., 2014; Harimalala et al., 2013; Zia-Ur-Rehman et al., 2013). Interestingly, a strain of TYLCV originating from Oman has been shown to be associated with an unusual alphasatellite (Ageratun yellow vein Singapore alphasatellite), the only alphasatellite that was previously reported from Singapore back in 1999 (Idris et al., 2011; Saunders and Stanley, 1999). Recently, Sida yellow vein China alphasatellite (SiYVCNA) has been identified in association with TYLCW from main land Japan. However, the low levels of sequence divergence between all isolates of SiYVCNA suggests that this has only recently spread into Japan (Shahid et al., 2014).
[FIGURE 2 OMITTED]
Potential alphasatellite functions. Alphasatellites have no obvious contribution to symptoms induced by begomovirus-betasatellite disease complexes and appear to affect betasatellite replication but do not affect helper virus replication. However, some alphasatellites can attenuate disease symptoms caused by begomovirus-betasatellite complex in the early stages of infection. For example, Nawaz-ul-Rehman et al. (2010) have shown the alphasatellite Rep proteins encoded by two non-pathogenic alphasatellites, Gossvpium darwinii symptomless alphasatellite (GDarSLA) and Gossvpium mustelinium symptomless alphasatellite (GMusSLA). They can interact with Cotton leaf curl Rajasthan vims (CLCuRaV) Rep proteins (Table 1). Betasatellites depend solely for replication on the Rep proteins encoded by their helper begomoviruses: binding between alphasatellite-Rep and helper virus Rep proteins may inhibit betasatellite replication and results in down regulated expression of [beta]C1 and correspondent symptom amelioration. Also GDarSLA and GMusSLA alphasatellite-Reps have strong gene silencing suppressor activities (Nawaz-ul-Rehman et al., 2010). Although further investigations are required to prove whether alphasatellite-Reps encoded by other alphasatellites also have silencing suppressor activities. Recently, alphasatellites have been found in association with bipartite begomoviruses in Venezuela and Brazil (Zia-Ur-Rehman et al., 2013; Romay et al., 2010), respectively. The DNA-2 type alphasatellite, a different alphasatellite (only two members) of this alphasatellite are found until now, one from. Ageratum in Singapore and the other from tomato from Oman (Idris et al., 2011; Saunders et al., 2002). Although all these members contain conserved alphasatellite genome features, the DNA-2 type molecules are less homogeneous and have less than 50% nucleotide sequence identity with each other. The DNA-2 type alphasatellite identified in Oman can attenuate begomovirus symptoms and reduce accumulations of betasatellites (Idris et al., 2011). Further studies are needed to confirm whether these satellite molecules are replicated by their helper virus (es) and whether they have role in pathogenesis similar to those of betasatellites and some alphasatellites. New technologies like vector-enabled metagenomics and the recent circular DNA genomics (Ng et al., 2011) are anticipated to soon provide additional information about the field distributions of these novel satellites and their associated begomoviruses. The promising study about the function of this satellite indicate that the alphasatellite is most likely a molecular parasite of the helper begomovirus (Kon et al., 2009).
Viral vectors based on alphasatellites. Many plant viruses have been adapted into expression and VIGS vectors for external protein expression (Gleba et al., 2007) and silencing (Purkayastha and Dasgupta. 2009) of target genes in main crop plants. Recently, tobacco curly shoot alphasatellite (TbCSA) was successfully used to silence [beta]-glucuronidase and the sulphur desatinase genes in different Nictoiana tabacum cultivare (Purkayastha and Dasgupta, 2009). Among that it can be used to investigate gene expression (or as an expression vector) on the entire host range of the begomoviruses/curtoviruses. Alphasatellite has some unique properties that make this component distinctive among other molecules. For example, it has Rep gene which makes the alphasatellite autonomous in replication, secondly it has a-rich region if deleted cannot effect on its replication, lastly this molecule is quiet small and easy to manipulate. Shahid et al. (2009) have shown by agroinoculation studies with a-rich deleted cotton leaf curl Multan alphasatellite (CLCuMA) that this sequence is not required for the infectivity or maintenance of CLCuMA. Also CLCuMA has a wider host range and can successfully be maintained by a large number of diverse Begomovirus species. The ability to amplify itself is useful in a vector since it will increase the copy number (and thus also expression) of inserted sequences, deletion of a-rich region to increase the insert size and wider host range makes it a potentially useful vector (Tao and Zhou, 2004). The a-rich deleted CLCuMA was maintained in plants in the presence of a begomovirus. Although little is yet known about the maintenance of alphasatellites by begomoviruses, it is likely that high-level replication of these molecules is required for their maintenance, which depends upon its own Rep. There is no evidence for a (strong) selection mechanism for maintenance of alphasatellites. Maintenance of alphasatellites can simply be a selection of numbers; plants containing high levels of the satellite allow cell-to-cell movement by the virus encoded movement proteins or infection to the next plant by the vector of the helper begomovirus. Tao and Zhou (2004) used modified CLCuMA for virus induced gene silencing vector in plants. The same vector was used to successfully silence the chelates gene (ChlI). One of the advantages of an alphasatellite vector, over many of the other vectors, is that it can, at least in theory, be used with different Begomovirus or even Curtovirus (Saunders et al. 2002).
Recent research advances. Recent progresses in research comprises of the construction of the alphasatellite-based vectors, the development of the first VIGS system for different agricultural crops, the description of new alphasatellites, improvement in diagnostics, and new information on the begomovirus-satellite complex.
The role that alphasatellites play in begomovirus-satellite disease complex is still generally unidentified. The recent advancement and emerging potential of Next Generation Sequencing approaches will undoubtedly contribute considerably to the elucidation of the aetiology of many of these alphasatellite associated diseases. The fairly recent discovery of alphasatellite in Japan (Shahid et al., 2014) and its presence in papaya gardens in Nepal (Shahid et al., 2013) suggest that its occurrence and possible role in disease in other agricultural-producing regions need to be investigated. What effect the presence of an alphasatellite and the defective allied component may have on future begomovirus-betasatellite complex is not clear.
Whereas outdated research focused on the detection and characterisation of prevailing and new begomovirus-satellite complexes, we believe research on (i) the elucidation of the etiology of these disease complexes (ii) the development of resistance using non-transgenic approaches, and (iii) studies on the molecular interaction of alphasatellites and their helper viruses with their original host. As efficient tools are being developed now, future research with begomoviruses, as well as with all other whitefly-vectoring viruses, has to move from typical (model) plants like Nicotiana benthamiana towards other host plants to allow the study of symptomology, pathogenicity, host-plant response and viral determinants of vector transmission in their natural host.
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Muhammad Shafiq Shahid (a) *, Mehmoona Ilyas (b), Abdul Waheed (a) and Rajarshi Kumar Gaur (c)
(a) Department of Biosciences, COMSATS Institute of Information Technology, Sahiwal 57000, Pakistan
(b) Department of Biotechnology, University of Sargodha, Sargodha, Pakistan
(c) Department of Science, Faculty of Arts, Science and Commerce, Mody Institute of Technology and Science, Lakshmangarh, Sikar-332311, Rajasthan, India
(received April 29, 2015; revised June 17, 2015; accepted August 19, 2015)
* Author for correspondence; E-mail: email@example.com.
Table 1. Alphasatellite associated with monopartite-betasatellite complex Alphasatellite Acc. no. Associated Virus Ageratum yellow vein AJ238493 Ageratum yellow vein alphasatellite virus (AYVV) Ageratum yellow vein JX570736 Tomato leaf curl India alphasatellite Karnataka virus Ageratum yellow vein AJ512960 Diversity of Kenya alphasatellite alphasatellite Ageratum yellow vein FR772085 Cotton leaf curl Pakistan Burewala virus alphasatellite Ageratum yellow vein AJ416153 AYVV Singapore alphasatellite Cassava mosaic HE984148 East African cassava Madagascar mosaic Kenya virus alphasatellite Cleome leaf crumple FN436007 Cleome leaf crumple alphasatellite virus Cotton leaf curl Dabwali AJ512957 Diversity of alphasatellite alphasatellite Cotton leaf curl Gezira FM164740 AYVV alphasatellite Croton yellow vein FN658711 Croton yellow vein mosaic alphasatellite mosaic virus Euphorbia yellow mosaic FN436008 Euphorbia yellow mosaic alphasatellite virus Gossypium darwinii EU384606 Cototn leaf curl symptomless Rajasthan virus alphasatellite Hibiscus leaf curl AJ512950 Diversity of alphasatellite alphasatellite Hollyhock yellow vein FR772086 Hollyhock yellow vein symptomless virus alphasatellite Lantana yellow vein KC206075 Lantana yellow vein alphasatellite virus Malvastrum yellow mosaic AM050734 Malvastrum yellow mosaic alphasatellite virus Malvastrum yellow mosaic FN675297 Tomato yellow leaf curl Cameroon China virus (ToLCCNV) alphasatellite Melon chlorotic mosaic FM163578 Melonchlorotic leaf curl virus alphasatellite virus Mesta yellow vein mosaic JX183090 Mesta yellow vein mosaic alphasatellite virus Okra leaf curl AJ512954 Diversity of alphasatellite alphasatellite Sida yellow vein Vietnam DQ641718 Sida yellow vein Vietnam alphasatellite virus Tobacco curly shoot AJ579361 Tomato yellow leaf curl alphasatellite China virus (ToLCCNV) Tomato yellow leaf curl AJ579358 ToLCCNV China alphasatellite Verbesina encelioides HQ631431 Hollyhock yellow vein leaf curl virus alphasatellite Vemonia yellow vein JF733780 Vemonia yellow vein Fujian alphasatellite Fujian virus Vinca yellow vein KC206076 Vinca yellow vein virus alphasatellite Alphasatellite Source Ageratum yellow vein Saunders etal, 1997 alphasatellite Ageratum yellow vein Chatchawankanphanich and India alphasatellite Maxwell, 2002 Ageratum yellow vein Briddon et al, 2004 Kenya alphasatellite Ageratum yellow vein Iqbal et al, 2013 Pakistan alphasatellite Ageratum yellow vein Saunders, 1999 Singapore alphasatellite Cassava mosaic Harimalala et al, 2013 Madagascar alphasatellite Cleome leaf crumple Paprotka et al, 2010 alphasatellite Cotton leaf curl Dabwali Briddon et al, 2004 alphasatellite Cotton leaf curl Gezira Leke et al, 2013 alphasatellite Croton yellow vein Zaffalon et al, 2011 mosaic alphasatellite Euphorbia yellow mosaic Fernanda et al, 2011 alphasatellite Gossypium darwinii Nawazul-Rehman et al, symptomless 2010 alphasatellite Hibiscus leaf curl Briddon et al, 2004 alphasatellite Hollyhock yellow vein Saunders et al, 2000 symptomless alphasatellite Lantana yellow vein Marwal et al, 2013a alphasatellite Malvastrum yellow mosaic Guo et al, 2006 alphasatellite Malvastrum yellow mosaic Leke et al, 2011 Cameroon alphasatellite Melon chlorotic mosaic Romay et al, 2010 virus alphasatellite Mesta yellow vein mosaic Chatterjee et al, 2005 alphasatellite Okra leaf curl Briddon et al, 2004 alphasatellite Sida yellow vein Vietnam Ha et al, 2006 alphasatellite Tobacco curly shoot Xie et al, 2010 alphasatellite Tomato yellow leaf curl Xie et al, 2010 China alphasatellite Verbesina encelioides Prajapat et al, 2011 leaf curl alphasatellite Vemonia yellow vein Zulfiqar et al, 2012 Fujian alphasatellite Vinca yellow vein Marwal et al, 2013b alphasatellite