Pigeonpea sterility mosaic virus: a legume-infecting Emaravirus from South Asia.

Pigeonpea sterility mosaic virus (PPSMV), a species of the genus Emaravirus, is the causal agent of sterility mosaic disease (SMD) of pigeonpea [Cajanus cajan (L.) Millsp]. This disease, dubbed the 'green plague', as the infected plants remain in the vegetative state without flower production, has been reported from India and a few other South-East Asian countries. SMD is estimated to result in an annual yield loss of over US$300 million in India alone. The aetiology of SMD, which remained a mystery for over 70 years, was resolved with the discovery of PPSMV in 2000 and its complete genome sequence in 2014.

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SMD is characterized by stunted and bushy plants, leaves of reduced size with chlorotic rings or mosaic symptoms, and partial or complete cessation of flower production (i.e. sterility). The causal agent of the disease is PPSMV, a virus with a segmented, negative-sense, single-stranded RNA genome, transmitted in a semi-persistent manner by an eriophyid mite Aceria cajani Channabassavanna (Acari: Arthropoda). Both the virus and vector are highly specific to pigeonpea and a few of its wild relatives, such as C. scarabaeoides and C. cajanifolius. Under experimental conditions, PPSMV was transmitted to Nicotiana benthamiana by sap inoculation using fresh extract of SMD-infected leaves (but not to pigeonpea); however, purified nucleoprotein preparations are not infectious. The virus was also transmitted to French bean (Phaseolus vulgaris L.) using viruliferous eriophyid mites. PPSMV is not seed transmitted in pigeonpea or other hosts known to be infected by this virus. On the basis of the differential host reactions in different geographical locations, the occurrence of diverse PPSMV strains was suspected.

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PPSMV can infect several genotypes of cultivated and wild relatives of pigeonpea. Experimental hosts include N. benthamiana, N. clevelandii, P. vulgaris and Chrozophora rottleri. However, pigeonpea alone and a few wild species of Cajanus were found to support the vector A. cajani. SMD is endemic in most of the pigeonpea-growing regions of India, but the incidence varies widely between regions and years. In nature, A. cajani populations were almost exclusively observed on SMD-infected pigeonpea, but not on healthy plants, indicating a strong communalistic relationship between the virus-infected plants and the vector. The epidemiology of SMD involves the virus, mite vector, cultivar and environmental conditions. Infected perennial and volunteer plants serve as a source for both the virus and its vector mites, and play an important role in the disease cycle.

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The PPSMV genome contains five segments of single-stranded RNA that are predicted to encode proteins in negative sense. The ribonucleoprotein complex is encased in quasi-spherical, membrane-bound virus particles of 100-150 nm. The largest segment, RNA-1, is 7022 nucleotides in length and codes for RNA-dependent RNA polymerase (2295 amino acids); RNA-2, with a sequence length of 2223 nucleotides, codes for glycoproteins (649 amino acids); RNA-3, with a sequence length of 1442 nucleotides, codes for nucleocapsid protein (309 amino acids); RNA-4, with a sequence length of 1563 nucleotides, codes for a putative movement protein p4 (362 amino acids); and RNA-5, with a sequence length of 1689 nucleotides, codes for p5 (474 amino acids), a protein with unknown function. PPSMV was recently classified as a species in the genus Emaravirus, a genus whose members show features resembling those of members of the genera Tospovirus (Family: Bunyaviridae) and Tenuivirus, both of which comprise single-stranded RNA viruses that encode proteins by an ambisense strategy.

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The disease is mainly controlled using SMD-resistant cultivars. However, the occurrence of distinct strains/isolates of PPSMV in different locations makes it difficult to incorporate broad-spectrum resistance. Studies on the inheritance of SMD resistance in different cultivars against different isolates of PPSMV indicate that the resistance is mostly governed by recessive genes, although there are contrasting interpretations of the data. Genetic engineering through RNA-interference (RNAi) and resistant gene-based strategies are some of the potential approaches for the transgenic control of SMD. Seed treatment or soil and foliar application of a number of organophosphorus-based insecticides or acaricides, which are recommended for the management of the vector mites, are seldom practised because of prohibitive costs and also their risks to human health and the environment.