Role of the Sw5 Gene Cluster in the Fight against Plant Viruses

Abstract

The Sw5 gene cluster furnishes robust resistance to Tomato spotted wilt virus in tomato, which has led to its widespread applicability in agriculture. Among the five orthologs, Sw5b functions as a resistance gene against a broad-spectrum tospovirus and is linked with tospovirus resistance. However, its paralog Sw5a has been recently implicated in providing resistance against Tomato leaf curl New Delhi virus, broadening the relevance of the Sw5 gene cluster in promoting defense against plant viruses. We propose that plants have established modifications within the homologs of R genes that permit identification of different effector proteins and provide broad and robust resistance against different pathogens through activation of the hypersensitive response and cell death.

Keywords: R gene-mediated resistance; Sw5 gene; Tomato leaf curl virus; Tomato spotted wilt virus; hypersensitive response.

FIG 1

Sw5b-mediated resistance against TSWV. TSWV is transmitted by thrips (Frankliniella occidentalis), and its multiplication occurs in the cytoplasm via RNA-dependent RNA polymerase (RdRP). Sw5b confers resistance against tospoviruses by recognizing virus-encoded NSm. When NSm is present at lower concentrations, SD of Sw5b interacts with it and releases the inhibition on the LRR domain by the CC domain. Further, LRR interacts with NSm, and the activated Sw5b leads to HR-mediated defense against tospoviruses. The translocation of the activated form of Sw5b into the nucleus is facilitated by importins α and β. In the nucleus, Sw5b activates defense-related genes through an unknown mechanism and inhibits long-distance movement of virus, thus inhibiting the systemic spread of virus.

FIG 2

Schematic representation of Sw5a-mediated resistance against ToLCNDV. ToLCNDV is spread by whitefly (Bemisia tabaci). It enters the cell and, after uncoating, circular viral ssDNA enters the nucleus of the plant cell (step 1) and complementary strand synthesis by host DNA polymerase leads to the synthesis of double-stranded DNA (dsDNA). This dsDNA serves as the template for transcription, and viral proteins are synthesized in the cytoplasm (step 2). AC4 is a pathogenesis determinant that suppresses antiviral RNA silencing machinery (step 3). Upon ToLCNDV infection, expression of sly-miR159 is reduced (step a), thus inhibiting the miR159-mediated cleavage of SlMyb33 (step b) and increasing the level of SlMyb33. SlMyb33 is translocated into the nucleus (step c), where it binds to the upstream promoter region of SlSw5a and enhances its expression. Furthermore, interaction between SlSw5a and AC4 triggers the HR and limits viral spread (step d).

FIG 3

Fluorescent and bright-field images of Nicotiana leaves infiltrated with a SlSw5a-green fluorescent protein (GFP) fusion protein. Localization analysis of SlSw5a confirmed that it is localized in both the nucleus and the membrane.