Reassessing the mechanism of genome packaging in plant viruses with lessons from ATPase fold

Abstract

Plant viruses cause various disease in crops and are responsible for huge economic losses. Understanding their mode of infection and spread is crucial for developing control strategies. Genome packaging is an important step in the process of viral maturation. Three systems of viral genome packaging are known till date. The type I packaging system, found in most of the small plant viruses, involves co-condensation of nucleic acid with viral capsid proteins (CPs) leading to the assembly of virion particles without utilizing ATP. The type II and III packaging systems, present in phages and nucleo-cytoplasmic large DNA viruses, exhibit genome translocation inside the prohead by utilizing ATP. Discovery of the ATPase fold in the CPs of many small plant viruses and the requirement of other ATPases during genome encapsidation have changed the perception about genome packaging in the type I system. Based on recent studies, it seems that the genome packaging mechanisms of plant viruses such as potexvirus have nothing in common with those of other well-characterized passive, energy-independent type I systems. Moreover, these studies have suggested that in these plant viruses, the genome encapsidation process is more intricately coupled with energy utilization than in other systems. In this comprehensive review, we present a novel, expanded sub-classification system for the type I system on the basis of ATP employed.

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Acknowledgements

This work was supported by grants from the Science and Engineering Research Board (SERB), Govt. of India, New Delhi (India) (File No. SRG/2019/002223) to TR. We thank Dr. Vihang Ghalsasi for the critical review of the manuscript and for helpful comments.

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Figure S1

Evolutionary relationship of capsid proteins in type IA, IB, and IC. Type IA sequences are shown in green, type IB in red, and type IC in purple. Detailed phylogenetic trees of CPs of the type I system of only plant viruses (a) and after inclusion of CPs of animal viruses and bacteriophage (b). [Acession number: ATU47240.1: Opuntia virus X, CUI25751.1: Potato virus Y, YP233104.1: Cassia yellow blotch virus, ATZ35297.1 CP: Potato leafroll virus, AVE14114.1: Cauliflower mosaic virus, AAB30891.1: Beet necrotic yellow vein virus, ABN48519.1: Cucurbit aphid-borne yellows virus, spP09509.2: BWYVG, QBG64852.1: Turnip yellows virus, QKE30561.1: Ginger chlorotic fleck-associated tombusvirus, 1VB2A Sesbania Mosaic Virus, QED42774.1: Soybean geminivirus, P14984.2: BCTVC, Q88886.1: TPCTV, ACM68957.1: Wheat dwarf virus, QLJ85111.1: Sesame curly top virus, YP_006590004.1: French bean severe leaf curl virus, QKE53473.1: Beet curly top Iran virus, AER29006.1: Chikungunya virus, AVN97691.1: Sacbrood virus, QIP75690.1: Tobacco mosaic virus, ANY93291.1: Plantago asiatica mosaic virus, ACM50753.1: Pepino mosaic virus, BAV91506.1: Adonis mosaic virus, QJX44289.1: Human immunodeficiency virus 1, spP12870.1: FHV, S46345: Simian immunodeficiency virus, AYM47481.1: Bovine leukemia virus, AWQ64531.1: Rabies lyssavirus] (PPTX 258 kb)

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Ranjan, T., Pal, A.K., Prasad, B.D. et al. Reassessing the mechanism of genome packaging in plant viruses with lessons from ATPase fold. Australasian Plant Pathol. (2021). https://doi.org/10.1007/s13313-020-00772-y

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Keywords

  • Plant virus genome packaging
  • Classification
  • Passive packaging system
  • Capsid protein (CP)
  • ATPase domain