Capsicum annum Hsp26.5 promotes defense responses against RNA viruses via ATAF2 but is hijacked as a chaperone for tobamovirus movement protein.

The expression of Capsicum annuum HEAT SHOCK PROTEIN 26.5 (CaHsp26.5) was triggered by the inoculation of Tobacco mosaic virus pathotype P0 (TMV-P0) but its function in the defense response of plants is unknown. We used gene silencing and overexpression approaches to investigate the effect of CaHsp26.5 expression on different plant RNA viruses. Moreover, we performed protein-protein and protein-RNA interaction assays to study the mechanism of CaHsp26.5 function. CaHsp26.5 binding to a short poly-cytosine motif in the 3'-untranslated region of the genome of some viruses triggers the expression of several defense-related genes such as PATHOGENESIS-RELATED GENE 1 with the help of a transcription factor, NAC DOMAIN-CONTAINING PROTEIN 81 (ATAF2). Thus, an elevated CaHsp26.5 level was accompanied by increased plant resistance against plant viruses such as Cucumber mosaic virus strain Korea. However, the movement proteins of Pepper mild mottle virus pathotype P1,2,3 and TMV-P0 were shown to be able to interact with CaHsp26.5 to maintain the integrity of their proteins. Our work shows CaHsp26.5 as a positive player in the plant defense response against several plant RNA viruses. However, some tobamoviruses can hijack CaHsp26.5's chaperone activity for their own benefit.