Recombination Among Begomoviruses on Malvaceous Plants Leads to the Evolution of Okra Enation Leaf Curl Virus in Pakistan

Saad Serfraz; Imran Amin; Khalid P. Akhtar; Shahid Mansoor

doi:10.1111/jph.12373

ORIGINAL ARTICLE

Recombination Among Begomoviruses on Malvaceous Plants

Leads to the Evolution of Okra Enation Leaf Curl Virus in Pakistan

Saad Serfraz

1

, Imran Amin

1

, Khalid P. Akhtar

2

and Shahid Mansoor

1

1 Agricultural Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan

2 Plant Protection Division, Nuclear Institute for Agriculture and Biology, Faisalab ad, Pakistan

Keywords

begomoviruses, malvaceous host, new

species, Okra enation leaf curl virus

Correspondence

S. Mansoor, National Institute for

Biotechnology and Genetic Engineering,

Faisalabad, Pakistan.

E-mail: Shahidmansoor7@gmail.com

Received: August 10, 2014; accepted:

December 29, 2014.

doi: 10.1111/jph.12373

Abstract

Whiteﬂy transmitted begomoviruses (family Geminiviridae) are the major

reason for signiﬁcant yield losses of dicotyledonous crops in tropics and

subtropics. Okra (Abelmoschus esculentus) is one of the important vegetable

crops, and leaf curl disease caused by geminiviruses is the most important

limiting factor for its production in Pakistan. Here, we report a new species

of okra-infecting begomovirus in south-eastern region of Pakistan and the

name Okra enation leaf curl virus (OELCuV) complex is proposed. This okra

enation leaf curl disease complex (OELCuD) in Pakistan is found to be

associated with Ageratum conyzoides symptomless alphasatellite (ACon-

SLA). All efforts to clone the betasatellite were unsuccessful. Comprehen-

sive sequence analyses suggest that intermalvaceous recombination

between okra and cotton-infecting begomoviruses resulted in the evolu-

tion of the new species. Surprisingly, Bhendi yellow vein mosaic virus (BY-

VMV) which has not been reported previously from Pakistan is the major

parent while Cotton leaf curl Multan virus (CLCuMV) acts as a distant parent

of the virus. Comparative recombination analysis also reveals that okra-

infecting begomoviruses from south and north-western India is causing

OELCuD in the Pakistan by recombining with CLCuMV at the Rep (1964–

1513 nts). Recombination is common among geminiviruses and recom-

bining of BYVMV and CLCuMV resulted in a new species: OELCuV. To

the best of our knowledge, this evolution of a new species of okra-infect-

ing begomovirus is the ﬁrst report of intermalvaceous recombination

where Rep acts as the target region.

Introduction

Plant viruses belonging to the family Geminiviridae are

with single-stranded (ss) DNA genomes, encapsidated

within two incomplete icosahedral particles inter-

twined to form a unique type of morphology of viral

coat protein with a diameter ~18 nm and length

~30 nm (Fauquet et al. 2008). According to recent

classiﬁcation, the family Geminivirdae is divided into

seven different genera (Mastrevirus, Topocuvirus, Curto-

virus, Becurtovirus, Turncurtovirus, Eragovirus and

Begomovirus) based on the genome organization, insect

vector and host range (Adams et al. 2013). Begomovi-

rus is the largest and economically the most important

genus within the family. Begomoviruses have a wide

host range which includes economically important

crops from diverse families such as Malvaceae, Solana-

ceae, Rosaseaece and Fabaceae and is transmitted by

whiteﬂy Bemisia tabaci (Gennadius; Varma and Mala-

thi 2003; Akhtar et al. 2014; Ullah et al. 2014, 2015).

Begomoviruses genome organization differs according

to geographical location. The genome of viruses native

to the New World (NW) comprises two components,

DNA-A and DNA-B. With few exceptions, most of the

Old World (OW) begomoviruses are monopartite and

show a synergistic association with a helper compo-

nent (betasatellite, alphasatellites; Mansoor et al.

2000; Briddon et al. 2004; Briddon and Stanley 2006).

J Phytopathol 163 (2015) 764–776 Ó 2015 Blackwell Verlag GmbH764

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Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses

Identification of a disease complex involving a novel monopartite begomovirus with beta- and alphasatellites associated with okra leaf curl disease in Oman

China rose (Hibiscus rosa-sinensis): a new natural host of Cotton leaf curl Burewala virus in Pakistan

Suppressors of RNA silencing encoded by the components of the cotton leaf curl begomovirus-betasatellite complex

An iteron-related domain is associated to motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach

Sub-viral agents associated with plant single-stranded DNA viruses

Clones of cotton leaf curl geminivirus induce symptoms atypical of cotton leaf curl disease

Identification of DNA components required for induction of cotton leaf curl disease

Diversity of DNA 1; a satellite-like molecule associated with monopartite begomovirus-DNA β complexes

Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses

Universal primers for the PCR-mediated amplification of DNA 1: a satellite-like molecule associated with begomovirus-DNA β complexes

First report of an alphasatellite associated with Okra enation leaf curl virus

A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus

Isolation of plant DNA from fresh tissue

Rates of evolutionary change in viruses: patterns and determinants

Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus

Geminivirus strain demarcation and nomenclature

Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses

Genetic structure and population variability of Tomato yellow leaf curl China virus

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

A simple method for cloning the complete begomovirus genome using the bacteriophage ϕ29 DNA polymerase

Horizontal gene transfer accelerates genome innovation and evolution

Bhendi yellow vein mosaic disease in India is caused by association of a DNA β satellite with a begomovirus

Suppressor of RNA silencing encoded by the monopartite tomato leaf curl Java begomovirus

Avoidance of protein fold disruption in natural virus recombinants

Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination

Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan

Association of a begomovirus and nanovirus-like molecule with Ageratum yellow vein disease in Pakistan

Geminivirus disease complexes: an emerging threat

The evolutionary value of recombination is constrained by genome modularity

RDP2: recombination detection and analysis from sequence alignments

Xanthium strumarium: a weed host of components of begomovirus–betasatellite complexes affecting crops

Post-transcriptional gene silencing suppressor activity of the alpha-Rep of non-pathogenic alphasatellites associated with begomoviruses

Possible emergence of new geminiviruses by frequent recombination

Contribution of the satellite encoded gene βC1 to cotton leaf curl disease symptoms

Dominance of resistance-breaking cotton leaf curl Burewala virus (CLCuBuV) in northwestern India

Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses

A single complementary-sense transcript of a geminiviral DNA β satellite is determinant of pathogenicity

Using a residue clash map to functionally characterize protein recombination hybrids

A unique virus complex causes Ageratum yellow vein disease

Replication promiscuity of DNA-β satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-β satellite localises sequences involved in replication

Complete nucleotide sequences of cotton leaf curl Rajasthan virus and its associated DNA β molecule infecting tomato

Suppressors of RNA silencing encoded by tomato leaf curl betasatellites

Infectivity of the cloned geminivirus genome requires sequences from both DNAs

The Clustal_X windows interface; flexible strategies for multiple sequence alignment aided by quality analysis tools

An analysis of the non-host resistance of Gossypium arboreum to cotton leaf curl disease by grafting

Evidence of Cotton leaf curl Burewala virus variant and its associate betasatellite with yellow mosaic of eggplant (Solanum melongena) in Pakistan

Emerging geminivirus problems: a serious threat to crop production

Molecular evidence for association of Cotton leaf curl Alabad virus with yellow vein mosaic disease of okra in North India

Association of a recombinant Cotton leaf curl Bangalore virus with yellow vein and leaf curl disease of okra in India

Molecular characterization of a new species of begomovirus associated with yellow vein mosaic of bhendi (Okra) in Bhubhaneswar, India

Protein building blocks preserved by recombination

Rapid host adaptation by extensive recombination

Interaction between a nanovirus-like component and the Tobacco curly shoot virus/satellite complex

Four DNA-A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA-A of geminivirus isolates from okra

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