Alfalfa leaf curl virus is transmitted by Aphis craccivora in a highly specific circulative manner

Abstract

Two members of the genus Capulavirus (Geminiviridae) are transmitted by aphids including Alfalfa leaf curl virus (ALCV) transmitted by Aphis craccivora. The capulavirus Euphorbia caput-medusae latent virus was shown here to be transmitted also by A. craccivora, using the population EuphorbiaSA. ALCV was transmissible by several A. craccivora populations including Robinia, but not EuphorbiaSA, reflecting a high transmission specificity. ALCV accumulation and localization were analyzed in whole insects, midguts, hemolymphs, and heads of aphids from both populations and from the non-vector species Acyrthosiphon pisum.A 6-day persistence was observed in A. craccivora populations but not in A. pisum. Vector and non-vector A. craccivora populations could be distinguished by contrasted virus accumulations and midgut intracellular localization. Results confirm that ALCV is transmitted according to a circulative-persistent mode, and are consistent with a gut barrier to the transmission of ALCV in A. pisum and a primary salivary gland barrier in A. craccivora.

Alfalfa leaf curl virus is efficiently acquired by its aphid vector Aphis craccivora but inefficiently transmitted

“…The construct for the Agrobacterium -mediated inoculation of ALCV was reported by Roumagnac et al [ 9 ]. Agrobacterium cultures were prepared and inoculated on broad bean plants as described by Ryckebusch et al [ 10 ].…”

“…Whiteflies (Aleyrodidae) transmit geminiviruses of the genus Begomovirus [4], leafhoppers (Cicadellidae) transmit those of the genera Mastrevirus , Curtovirus , Becurtovirus , Turncurtovirus and probably Eragrovirus [5–7], and treehoppers (Membracidae) transmit those of the genera Topocuvirus and Grablovirus [8]. Finally, aphids were found to be vectors of genetically distinct geminiviruses recently detected by metagenomic analyses and for which a new genus was defined, named Capulavirus [9–11]. Although taxonomically very distinct, aphids transmit geminiviruses by a circulative, non-propagative (CNP) mechanism [1, 10] similar to that of the aphid-transmitted viruses of the family Luteoviridae [2] and Nanoviridae [3].…”

“…Finally, aphids were found to be vectors of genetically distinct geminiviruses recently detected by metagenomic analyses and for which a new genus was defined, named Capulavirus [9–11]. Although taxonomically very distinct, aphids transmit geminiviruses by a circulative, non-propagative (CNP) mechanism [1, 10] similar to that of the aphid-transmitted viruses of the family Luteoviridae [2] and Nanoviridae [3]. Circulative non-propagatively transmitted viruses require circulation through insect bodies before transmission [12].…”

“…ALCV was also tested for a possible impact on the fitness of the aphid vector and for vertical transmission. Particular attention was given to transmission efficiency because previous results showed that it was relatively low compared to other CNP viruses [10, 40].…”

“…While CNP transmission in aphids has long been reported only in the families Nanoviridae and Luteoviridae , an aphid vector, Aphis craccivora Koch, 1854, was recently identified for the geminivirus alfalfa leaf curl virus (ALCV) [ 9 ]. A CNP transmission mechanism was identified based on the retention of viral DNA in gut, haemolymph and salivary gland compartments, as well as persistence of infectivity over time through insect moults [ 10 ]. The transmission of ALCV is highly specific.…”