Skip to main content
Top
Published in: Virology Journal 1/2021

Open Access 01-12-2021 | Research

Roles of two distinct alphasatellites modulating geminivirus pathogenesis

Authors: Manish Kumar, Fauzia Zarreen, Supriya Chakraborty

Published in: Virology Journal | Issue 1/2021

Login to get access

Abstract

Background

Alphasatellites are small coding DNA satellites frequently associated with a begomovirus/betasatellite complex, where they are known to modulate virulence and symptom development. Two distinct alphasatellites, namely, Cotton leaf curl Multan alphasatellite (CLCuMuA), and Gossypium darwinii symptomless alphasatellite (GDarSLA) associated with Cotton leaf curl Multan virus-India (CLCuMuV-IN) and Ludwigia leaf distortion betasatellite (LuLDB) were found to be associated with yellow mosaic disease of hollyhock (Alcea rosea) plants. In this study, we show that alphasatellites CLCuMuA and GDarSLA attenuate and delay symptom development in Nicotiana benthamiana. The presence of either alphasatellites reduce the accumulation of the helper virus CLCuMuV-IN. However, the levels of the associated betasatellite, LuLDB, remains unchanged. These results suggest that the alphasatellites could contribute to the host defence and understanding their role in disease development is important for developing resistance strategies.

Methods

Tandem repeat constructs of two distinct alphasatellites, namely, CLCuMuA and GDarSLA associated with CLCuMuV-IN and LuLDB were generated. N. benthamiana plants were co-agroinoculated with CLCuMuV and its associated alphasatellites and betasatellite molecules and samples were collected at 7, 14 and 21 days post inoculation (dpi). The viral DNA molecules were quantified in N. benthamiana plants by qPCR. The sequences were analysed using the MEGA-X tool, and a phylogenetic tree was generated. Genetic diversity among the CLCuMuA and GDarSLA was analysed using the DnaSP tool.

Results

We observed a reduction in symptom severity and accumulation of helper virus in the presence of two alphasatellites isolated from naturally infected hollyhock plants. However, no reduction in the accumulation of betasatellite was observed. The phylogenetic and genetic variability study revealed the evolutionary dynamics of these distinct alphasatellites , which could explain the role of hollyhock-associated alphasatellites in plants.

Conclusions

This study provides evidence that alphasatellites have a role in symptom modulation and suppress helper virus replication without any discernible effect on the replication of the associated betasatellite.
Appendix
Available only for authorised users
Literature
1.
go back to reference Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, et al. ICTV virus taxonomy profile: geminiviridae. J Gen Virol. 2017;98:131–3.CrossRef Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, et al. ICTV virus taxonomy profile: geminiviridae. J Gen Virol. 2017;98:131–3.CrossRef
2.
go back to reference Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, et al. Diversity of DNA β, a satellite molecule associated with some monopartite begomoviruses. Virology. 2003;312:106–21.CrossRef Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, et al. Diversity of DNA β, a satellite molecule associated with some monopartite begomoviruses. Virology. 2003;312:106–21.CrossRef
3.
go back to reference Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, et al. Diversity of DNA 1: a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology. 2004;324:462–74.CrossRef Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, et al. Diversity of DNA 1: a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology. 2004;324:462–74.CrossRef
4.
go back to reference Lozano G, Trenado HP, Fiallo-Olivé E, Chirinos D, Geraud-Pouey F, Briddon RW, et al. Characterization of non-coding DNA satellites associated with sweepoviruses (Genus Begomovirus, Geminiviridae): definition of a distinct class of begomovirus-associated satellites. Front Microbiol. 2016;7:1–13.CrossRef Lozano G, Trenado HP, Fiallo-Olivé E, Chirinos D, Geraud-Pouey F, Briddon RW, et al. Characterization of non-coding DNA satellites associated with sweepoviruses (Genus Begomovirus, Geminiviridae): definition of a distinct class of begomovirus-associated satellites. Front Microbiol. 2016;7:1–13.CrossRef
5.
go back to reference Fiallo-Olivé E, Martínez-Zubiaur Y, Moriones E, Navas-Castillo J. A novel class of DNA satellites associated with New World begomoviruses. Virology. 2012;426:1–6.CrossRef Fiallo-Olivé E, Martínez-Zubiaur Y, Moriones E, Navas-Castillo J. A novel class of DNA satellites associated with New World begomoviruses. Virology. 2012;426:1–6.CrossRef
6.
go back to reference Briddon RW, Mansoor S, Bedford ID, Pinner MS, Saunders K, Stanley J, et al. Identification of DNA components required for induction of cotton leaf curl disease. Virology. 2001;285:234–43.CrossRef Briddon RW, Mansoor S, Bedford ID, Pinner MS, Saunders K, Stanley J, et al. Identification of DNA components required for induction of cotton leaf curl disease. Virology. 2001;285:234–43.CrossRef
7.
go back to reference Cui X, Li G, Wang D, Hu D, Zhou X. A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol. 2005;79:10764–75.CrossRef Cui X, Li G, Wang D, Hu D, Zhou X. A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol. 2005;79:10764–75.CrossRef
8.
go back to reference Saunders K, Norman A, Gucciardo S, Stanley J. The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1). Virology. 2004;324:37–47.CrossRef Saunders K, Norman A, Gucciardo S, Stanley J. The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1). Virology. 2004;324:37–47.CrossRef
9.
go back to reference Gopal P, Pravin Kumar P, Sinilal B, Jose J, Kasin Yadunandam A, Usha R. Differential roles of C4 and βC1 in mediating suppression of post-transcriptional gene silencing: evidence for transactivation by the C2 of Bhendi yellow vein mosaic virus, a monopartite begomovirus. Virus Res. 2007;123:9–18.CrossRef Gopal P, Pravin Kumar P, Sinilal B, Jose J, Kasin Yadunandam A, Usha R. Differential roles of C4 and βC1 in mediating suppression of post-transcriptional gene silencing: evidence for transactivation by the C2 of Bhendi yellow vein mosaic virus, a monopartite begomovirus. Virus Res. 2007;123:9–18.CrossRef
10.
go back to reference Amin I, Hussain K, Akbergenov R, Yadav JS, Qazi J, Mansoor S, et al. Suppressors of RNA silencing encoded by the components of the cotton leaf curl begomovirus-betasatellite complex. Mol Plant-Microbe Interact. 2011;24:973–83.CrossRef Amin I, Hussain K, Akbergenov R, Yadav JS, Qazi J, Mansoor S, et al. Suppressors of RNA silencing encoded by the components of the cotton leaf curl begomovirus-betasatellite complex. Mol Plant-Microbe Interact. 2011;24:973–83.CrossRef
11.
go back to reference Mansoor S, Khan SH, Bashir A, Saeed M, Zafar Y, Malik KA, et al. Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology [Internet]. 1999;259:190–9.CrossRef Mansoor S, Khan SH, Bashir A, Saeed M, Zafar Y, Malik KA, et al. Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology [Internet]. 1999;259:190–9.CrossRef
12.
go back to reference Saunders K, Stanley J. A nanovirus-like DNA component associated with yellow vein disease of Ageratum conyzoides: evidence for interfamilial recombination between plant DNA viruses. Virology. 1999;264:142–52.CrossRef Saunders K, Stanley J. A nanovirus-like DNA component associated with yellow vein disease of Ageratum conyzoides: evidence for interfamilial recombination between plant DNA viruses. Virology. 1999;264:142–52.CrossRef
14.
15.
go back to reference Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu JK, Brown JK. An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol. 2011;92:706–17.CrossRef Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu JK, Brown JK. An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol. 2011;92:706–17.CrossRef
16.
go back to reference Luo C, Wang ZQ, Liu X, Zhao L, Zhou X, Xie Y. Identification and analysis of potential genes regulated by an alphasatellite (TYLCCNA) that contribute to host resistance against tomato yellow leaf curl China virus and its betasatellite (TYLCCNV/TYLCCNB) infection in Nicotiana benthamiana. Viruses. 2019;11:442.CrossRef Luo C, Wang ZQ, Liu X, Zhao L, Zhou X, Xie Y. Identification and analysis of potential genes regulated by an alphasatellite (TYLCCNA) that contribute to host resistance against tomato yellow leaf curl China virus and its betasatellite (TYLCCNV/TYLCCNB) infection in Nicotiana benthamiana. Viruses. 2019;11:442.CrossRef
17.
go back to reference Kumar J, Kumar J, Singh SP, Tuli R. Association of satellites with a mastrevirus in natural infection: complexity of wheat Dwarf India virus disease. J Virol. 2014;88:7093–104.CrossRef Kumar J, Kumar J, Singh SP, Tuli R. Association of satellites with a mastrevirus in natural infection: complexity of wheat Dwarf India virus disease. J Virol. 2014;88:7093–104.CrossRef
18.
go back to reference Kumar M, Kumar RV, Chakraborty S. Association of a begomovirus-satellite complex with yellow vein.pdf. Arch Virol. 2020;165:2099–103.CrossRef Kumar M, Kumar RV, Chakraborty S. Association of a begomovirus-satellite complex with yellow vein.pdf. Arch Virol. 2020;165:2099–103.CrossRef
19.
go back to reference Sangeeta, Ranjan P, Kumar RV, Bhatt BS, Chahwala FD, Yadav BK, et al. Two distinct monopartite begomovirus-betasatellite complexes in western India cause tomato leaf curl disease. Virus Res [Internet]. 2021;295:198319.CrossRef Sangeeta, Ranjan P, Kumar RV, Bhatt BS, Chahwala FD, Yadav BK, et al. Two distinct monopartite begomovirus-betasatellite complexes in western India cause tomato leaf curl disease. Virus Res [Internet]. 2021;295:198319.CrossRef
21.
22.
go back to reference Chakraborty S, Vanitharani R, Chattopadhyay B, Fauquet CM. Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J Gen Virol [Internet]. 2008;89:818–28. https://doi.org/10.1099/vir.0.82873-0.CrossRef Chakraborty S, Vanitharani R, Chattopadhyay B, Fauquet CM. Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J Gen Virol [Internet]. 2008;89:818–28. https://​doi.​org/​10.​1099/​vir.​0.​82873-0.CrossRef
23.
go back to reference Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olivé E, Moriones E, et al. Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch Virol [Internet]. 2018;163:2587–600. https://doi.org/10.1007/s00705-018-3854-2.CrossRef Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olivé E, Moriones E, et al. Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch Virol [Internet]. 2018;163:2587–600. https://​doi.​org/​10.​1007/​s00705-018-3854-2.CrossRef
24.
go back to reference Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.CrossRef Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.CrossRef
26.
go back to reference Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.CrossRef Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.CrossRef
29.
go back to reference Basu S, Kumar Kushwaha N, Kumar Singh A, Pankaj Sahu P, Vinoth Kumar R, Chakraborty S. Dynamics of a geminivirus-encoded pre-coat protein and host RNA-dependent RNA polymerase 1 in regulating symptom recovery in tobacco. J Exp Bot. 2018;69:2085–102.CrossRef Basu S, Kumar Kushwaha N, Kumar Singh A, Pankaj Sahu P, Vinoth Kumar R, Chakraborty S. Dynamics of a geminivirus-encoded pre-coat protein and host RNA-dependent RNA polymerase 1 in regulating symptom recovery in tobacco. J Exp Bot. 2018;69:2085–102.CrossRef
30.
go back to reference Malathi VG, Renukadevi P, Chakraborty S, Biswas KK, Roy A, Sivalingam PN, et al. Begomoviruses and their satellites occurring in India: distribution, diversity and pathogenesis. Singapore: Springer; 2017. Malathi VG, Renukadevi P, Chakraborty S, Biswas KK, Roy A, Sivalingam PN, et al. Begomoviruses and their satellites occurring in India: distribution, diversity and pathogenesis. Singapore: Springer; 2017.
33.
go back to reference Siddiqui K, Mansoor S, Briddon RW, Amin I. Diversity of alphasatellites associated with cotton leaf curl disease in Pakistan. Virol Rep [Internet]. 2016;6:41–52.CrossRef Siddiqui K, Mansoor S, Briddon RW, Amin I. Diversity of alphasatellites associated with cotton leaf curl disease in Pakistan. Virol Rep [Internet]. 2016;6:41–52.CrossRef
34.
go back to reference Shakir S, Zaidi SS-A, Atiq-ur-Rehman, Farooq M, Amin I, Scheffler J, et al. Non-cultivated cotton species (Gossypium spp.) act as a reservoir for cotton leaf curl begomoviruses and associated satellites. Plants [Internet]. 2019;8:127.CrossRef Shakir S, Zaidi SS-A, Atiq-ur-Rehman, Farooq M, Amin I, Scheffler J, et al. Non-cultivated cotton species (Gossypium spp.) act as a reservoir for cotton leaf curl begomoviruses and associated satellites. Plants [Internet]. 2019;8:127.CrossRef
35.
go back to reference Deng Y, Liu T, Xie Y, Wei Y, Xie Z, Shi Y, et al. High genetic diversity and low differentiation in Michelia shiluensis, an endangered Magnolia species in south China. Forests. 2020;11:1–15. Deng Y, Liu T, Xie Y, Wei Y, Xie Z, Shi Y, et al. High genetic diversity and low differentiation in Michelia shiluensis, an endangered Magnolia species in south China. Forests. 2020;11:1–15.
37.
go back to reference Vinoth Kumar R, Singh AK, Singh AK, Yadav T, Singh AK, Kushwaha N, et al. Complexity of begomovirus and betasatellite populations associated with chilli leaf curl disease in India. J Gen Virol. 2015;96:3143–58.CrossRef Vinoth Kumar R, Singh AK, Singh AK, Yadav T, Singh AK, Kushwaha N, et al. Complexity of begomovirus and betasatellite populations associated with chilli leaf curl disease in India. J Gen Virol. 2015;96:3143–58.CrossRef
39.
43.
go back to reference Patil BL, Fauquet CM. Differential interaction between cassava mosaic geminiviruses and geminivirus satellites. J Gen Virol. 2010;91:1871–82.CrossRef Patil BL, Fauquet CM. Differential interaction between cassava mosaic geminiviruses and geminivirus satellites. J Gen Virol. 2010;91:1871–82.CrossRef
44.
go back to reference Mar TB, Mendes IR, Lau D, Fiallo-Olivé E, Navas-Castillo J, Alves MS, et al. Interaction between the New World begomovirus Euphorbia yellow mosaic virus and its associated alphasatellite: effects on infection and transmission by the whitefly Bemisia tabaci. J Gen Virol [Internet]. 2017;98:1552–62. https://doi.org/10.1099/jgv.0.000814.CrossRef Mar TB, Mendes IR, Lau D, Fiallo-Olivé E, Navas-Castillo J, Alves MS, et al. Interaction between the New World begomovirus Euphorbia yellow mosaic virus and its associated alphasatellite: effects on infection and transmission by the whitefly Bemisia tabaci. J Gen Virol [Internet]. 2017;98:1552–62. https://​doi.​org/​10.​1099/​jgv.​0.​000814.CrossRef
45.
go back to reference Briddon RW, Stanley J. Subviral agents associated with plant single-stranded DNA viruses. Virology. 2006;344:198–210.CrossRef Briddon RW, Stanley J. Subviral agents associated with plant single-stranded DNA viruses. Virology. 2006;344:198–210.CrossRef
46.
go back to reference Orozco BM, Miller AB, Settlage SB, Hanley-Bowdoin L. Functional domains of a geminivirus replication protein. J Biol Chem. 1997;272:9840–6.CrossRef Orozco BM, Miller AB, Settlage SB, Hanley-Bowdoin L. Functional domains of a geminivirus replication protein. J Biol Chem. 1997;272:9840–6.CrossRef
Metadata
Title
Roles of two distinct alphasatellites modulating geminivirus pathogenesis
Authors
Manish Kumar
Fauzia Zarreen
Supriya Chakraborty
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2021
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-021-01718-6

Other articles of this Issue 1/2021

Virology Journal 1/2021 Go to the issue