Abstract
Weeds are invasive species that grow along with cultivated plants due to their high phenotypic plasticity. They serve as reservoirs of geminiviruses during off-season for main crops and provide the source of virus inoculum during their plantation. Geminiviruses are single-stranded DNA viruses enclosed in icosahedral geminate particles. These viruses can be either monopartite or bipartite, depending upon the number of genomic circles present. The members of genus Begomovirus are responsible for huge economic crop losses and are transmitted through insect vector Bemisia tabaci. The majority of the weed-infecting monopartite begomoviruses are associated with Betasatellite genus of Tolecusatellitidae family and alphasatellites. Geminiviruses are reported to infect a variety of weeds in South-east Asia, Mediterranean region, Western Europe (mainly Spain and France), Africa, Latin America, Central America, Caribbean region, and Australia. Weeds harbor the mixed infection of viruses; therefore, these plants serve as melting pots for recombination and evolution of begomoviruses. This chapter presents the geminivirus infection on weeds, their recombination, and their spread to newer hosts.
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1 Introduction
The plant viruses of Geminiviridae family consist of circular single-stranded DNA as genetic material enclosed in icosahedral geminate capsid (Lazarowitz 1992). The family is classified into nine different genera: Mastrevirus, Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Topocuvirus, and Turncurtovirus on the basis of genome organization, insect vector, and host range. The members are transmitted by leafhoppers (Mastrevirus, Becurtovirus, and Curtovirus), treehoppers (Curtovirus, Grablovirus, and Topocuvirus), whitefly (Begomovirus), and aphid (Capulavirus) (Zerbini et al. 2017). Geminiviruses are able to infect both monocots and dicots; therefore, they are responsible for worldwide crop losses (Moffat 1999). The genome of these viruses can be monopartite or bipartite, based on the number of genomic components (Harrison and Robinson 1999). Monopartite geminiviruses possess single genomic component which encodes the proteins required for replication, encapsulation, movement, transcription, and suppression of gene silencing. Bipartite begomoviruses consist of two genomic components: DNA-A and DNA-B. DNA-A is homologous to DNA-A of monopartite geminiviruses and encodes proteins required for encapsulation, replication, transcription, and suppression of gene silencing. DNA-B encodes only two proteins, essential for intra- and intercellular movement (Hanley-Bowdoin et al. 2000). The viral genome replicates via rolling circle replication (RCR) mechanism that is initiated at stem-loop structure containing nonanucleotide sequence (TAATATT/AC). The Begomovirus is the largest genus of Geminiviridae family that infects dicots and is transmitted by whitefly (Bemisia tabaci) vector (Brown et al. 2015). Begomoviruses are distributed into two groups on the globe: old world (OW) and new world (NW) (Paximadis et al. 1999). The majority of monopartite begomoviruses are associated with members of Betasatellite genus and alphasatellite molecules which form disease complex in plants (Kulshreshtha et al. 2017; Sharma et al. 2019a; Zhou 2013).
Weeds are unwanted plants which grow along with cultivated crops and decrease their yield. They are responsible for 43% loss in crop yield and destroy the native habitats (Oerke 2006). Due to high environmental plasticity, weeds are widely distributed and are able to adapt in different ecological habitats (Holm et al. 1979). Weeds serve as reservoir host for the viruses and play important role in their persistence and spread (Hallan et al. 1998). During off-season of crops, they become main host for the virus population. The earliest record of geminivirus symptoms on a weed was described in a Japanese poem written 1265 years ago (Saunders et al. 2003). In this chapter, we described various geminiviruses-infecting weeds, their symptoms, and emergence.
2 Global Status of Weed-Infecting Geminiviruses
Begomovirus infection causes devastating disease and huge crop losses worldwide (Varma and Malathi 2003). The monopartite begomoviruses and some bipartite begomoviruses are present in OW. The majority of bipartite begomoviruses are present in the NW, which suggested their origin from OW begomoviruses (Rybicki 1994). The only exception is tomato leaf deformation virus (ToLDeV), a monopartite begomovirus present in NW (Melgarejo et al. 2013). The agricultural practices, trafficking of infected plant material by humans, and invasive polyphagous vectors are responsible for the global spread and diversification of geminiviruses. The best example is the spread of tomato yellow leaf curl virus (TYLCV) through infected seedlings from Israel to tomato-growing regions of NW during the early 1990s (Duffy and Holmes 2007). Similarly, the introduction of NW cotton to the Indian subcontinent resulted in incidence of leaf curl disease of cotton in Pakistan (Briddon and Markham 2000). The invasive polyphagous whitefly vector also (Bemisia tabaci) resulted in the transmission of native begomovirus to the new hosts and emergence of novel viruses. The yellow leaf curl-like symptoms were observed on tomato in the 1940s due to outbreaks of sweetpotato whitefly population and the infection was due to the presence of a geminivirus TYLCV (Cohen and Antignus 1994). Later on, TYLCV infection was reported on weeds such as Euphorbia sp., Lamium amplexicaule, Malva parviflora, and Ageratum conyzoides (Papayiannis et al. 2011; Kil et al. 2014). The weed species belonging to family Euphorbiaceae, Asteraceae, Fabaceae, Malvaceae, Solanaceae, Amaranthaceae, and Lamiaceae harbor virus inoculum in NW as well as OW. The weeds growing in South-east Asia are infected with both monopartite–satellite complex and bipartite begomoviruses. Therefore, South-east Asian region can be regarded as diversification center for weed-infecting begomoviruses (Fig. 1). Most of the weed species display chlorosis, yellow mosaic, vein yellowing symptoms, and stunting upon geminivirus infection (Fig. 2).
Ageratum conyzoides is a member of Asteraceae family and native of Central America. It is an annual invasive weed in tropical subtropical regions of the world and reported as natural host for ageratum yellow vein virus (Tan and Wong 1993; Saunders and Stanley 1999; Saunders et al. 2004), ageratum enation virus (Tahir et al. 2015), ageratum leaf curl virus (Huang and Zhou 2006a), chilli leaf curl virus (Iqbal et al. 2016), cotton leaf curl Rajasthan virus (Mubin et al. 2009), and malvastrum yellow vein virus (Jiang and Zhou 2004) in South-east Asia. A. conyzoides also serve as reservoir host for TYLCV in Tanzania and Mediterranean region as this weed grows along with tomato plantations (Papayiannis et al. 2011).
Datura stramonium commonly known as devil’s snare and jimson weed is a member of Solanaceae family. It is a native of America and is now distributed to tropical and subtropical regions and parts of Europe. A novel begomovirus datura leaf distortion virus was found to infect this weed in Venezuela (Fiallo-Olive et al. 2013). Leaf curl disease of jimson weed was found to be associated with tomato yellow leaf curl China virus (TYLCChV) and a betasatellite (Ding et al. 2007). In France and Spain, this weed was infected with monopartite TYLCV (Bedford et al. 1998).
Croton bonplandianum is an annual weed found in Asia and is infected with croton yellow vein virus, croton yellow vein mosaic virus, and tomato leaf curl New Delhi virus (Hussain et al. 2011; Pramesh et al. 2013; Chowda-Reddy et al. 2005). Malvastrum coromandelianum is an annual weed native to North America and now distributed in Africa, Asia, and South America. It acts as alternative host for monopartite begomoviruses such as malvastrum yellow mosaic virus, malvastrum leaf curl virus, malvastrum leaf curl Guangdong virus, and TYLCChV (Guo et al. 2007; Wu et al. 2007; Liu et al. 2011). In NW, it is reservoir host for sida golden yellow vein virus, sida golden mosaic Florida virus, and malvastrum yellow mosaic Jamaica virus (Fiallo-Olive et al. 2010, 2012; Graham et al. 2010).
Sida sp. is an invasive perennial weed found in tropical and subtropical areas of the world. S. acuta has been reported as natural host of sida golden mosaic virus and sida yellow mosaic China virus (Wong et al. 1993; Xiong et al. 2005). S. micrantha has been reported as reservoir host of abutilon mosaic virus, abutilon mosaic Bolivia virus, sida mosaic Bolivia virus 1, and sida golden mosaic buckup virus (Wyant et al. 2011; Stewart et al. 2014). In Brazil, Sida sp. served as reservoir host for sida micrantha virus and tomato mild mosaic virus which were found to infect tomatoes and beans (Castillo-Urquiza et al. 2010). The detailed information of geminivirus members infecting various weeds is given in Table 1.
3 Weeds as Mixing Vessels for Recombination and Assortment of Viruses
Recombination, mutation, and pseudo-recombination between variants, species, and genera of the virus significantly contribute to genetic diversity, local adaptation, and emergence of new viruses (Pita et al. 2001; Martin et al. 2005; Graham et al. 2010). It has been demonstrated that recombination in geminiviruses is dependent on parental virus strain, host plant, and inoculum (Padidam et al. 1999). Weeds harbor mixed infections of geminiviruses which result in the evolution and emergence of new virus species or strains. The mixed infections result in the association of betasatellites with helper begomoviruses which led to emergence of more virulent strains or species. These satellite molecules are known to enhance the symptom severity and disease epidemics in new environments (Sharma et al. 2019b; Saunders et al. 2001; Briddon et al. 2004). The evolution of sida micrantha mosaic-associated viruses and alternanthera yellow vein virus is a result of recombination in the weed hosts (Jovel et al. 2007; Mubin et al. 2010). The recombinants of begomoviruses associated with cassava mosaic disease in Africa showed increased virulence in comparison to parental strains (Zhou et al. 1997). In Brazil, multiple recombination events among cleome leaf crumple virus isolates were reported in a single weed Cleome affinis (Da Silva et al. 2011). Furthermore, sida mottle virus and sida micrantha mosaic virus were originally characterized from weed species that were transmitted to crops by insect vector (Castillo-Urquiza et al. 2007, 2010). Weeds belonging to Euphorbiaceae and Fabaceae family are reported as reservoir host for cassava-infecting begomoviruses in Africa (Alabi et al. 2008). Therefore, weeds are designated as “mixing vessels” for genetic recombination between begomoviruses. Ageratum enation virus is a monopartite begomovirus associated with betasatellite and alphasatellite, is widely distributed in South-east Asia, and infects non-cultivated plants such as Sonchus oleraceus and A. conyzoides (Tahir et al. 2015). Two weeds Chrozophora hierosolymitana and Herniaria sp. were reported to harbor the TYLCV inoculums in Iran (Fazeli et al. 2009).
4 Relationship Between Weed, Virus Disease Complex, and Insect Vector
Weeds act as alternate host for both virus and insect vector during off-season of the main crops. As a result, these plants prevent the extinction of virus populations in the absence of annual crops (Seal et al. 2006). In such conditions, a dramatic increase in the whitefly-transmitted geminiviruses (WTG) population has been reported. The virus-infected plants have a greater tendency to attract the insect vector in comparison to healthy plants. Furthermore, virus infection alters the morphology and defense system which increases the infestation and fitness of the insect vector (Awmack and Leather 2002; Chen et al. 2013). The invasive polyphagous B-biotype B. tabaci is found to be responsible for the TYLCV disease epidemic in the Mediterranean region. The invasive whitefly species is reported to transmit about 200 species of the begomoviruses in both cultivated and non-cultivated plants (Delatte et al. 2005; Hogenhout et al. 2008). The mobile and polyphagous nature of this insect allows the dissemination of viral diversity into new crops (Lefeuvre et al. 2007). The association of betasatellites and alphasatellite with helper begomovirus offers a selective advantage for helper begomovirus to produce symptoms on the weed. The yellow vein disease of A. conyzoides was due to infection of ageratum yellow vein virus and a betasatellite. In the absence of betasatellite, the weed failed to develop the typical symptoms (Saunders et al. 2001). Similarly, the yellow vein disease of C. bonplandianum was associated with infection of a monopartite begomovirus and a betasatellite (Hussain et al. 2011). In case of tomato leaf curl virus infection on Parthenium hysterophorus, the betasatellite and alphasatellite complex developed typical leaf curling symptoms (Kumar et al. 2016). The begomovirus disease complex including multiple and recombinant betasatellites was reported from a common weed, Digera arvensis, in Pakistan (Mubin et al. 2009). The widespread distribution of weeds and polyphagous invasive whitefly vector in the warmer regions provides favorable platform for virus proliferation. The whitefly population prefers high temperature for reproduction, but is adversely affected by prolonged winters. Under such circumstances, weed species serve as reservoir inoculums for viral diversity and global warming in temperate areas offers great advantage for the virus spread.
5 Conclusion
The increasing incidence of geminivirus infection on economic important crops has become a major concern, and it has been found that weeds or non-cultivated hosts serve as source of virus infection. The presence of mixed infection renders the weeds as melting pots for begomovirus recombination and led to emergence of more fit variants of the virus. Additionally, the increasing population insect vector contributed to the spread of begomoviruses in new hosts. Therefore, reservoir host, insect vector, and virus constitute a cycle which seems to be the main reason for the outbreak and emergence of begomovirus disease complex in newer hosts. However, it is unclear whether weeds act as indigenous host of viruses or they get infected from the infected crop host? To address this question, further studies are required to demonstrate the role of weeds in primary source of virus inoculum and evolution of novel viruses. The outcome of such studies will reveal a potential way to combat the geminivirus infection in cultivated crops.
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Acknowledgements
Authors acknowledge Director CSIR-IHBT for providing the research facilities. PR is thankful to Council of Scientific and Innovative Research for providing Junior and Senior Research Fellowship. AK thanks the University Grants Commission (UGC) for providing Junior and Senior Research Fellowship. PR and AK duly acknowledge Academy of Scientific and Innovative Research (AcSIR), New Delhi, India.
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Roshan, P., Kulshreshtha, A., Hallan, V. (2019). Global Weed-Infecting Geminiviruses. In: Kumar, R. (eds) Geminiviruses. Springer, Cham. https://doi.org/10.1007/978-3-030-18248-9_6
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