The Role of Grafting in the Resistance of Tomato to Viruses

Abstract

Grafting is routinely implemented in modern agriculture to manage soilborne pathogens such as fungi, oomycetes, bacteria, and viruses of solanaceous crops in a sustainable and environmentally friendly approach. Some rootstock/scion combinations use specific genetic resistance mechanisms to impact also some foliar and airborne pathogens, including arthropod or contact-transmitted viruses. These approaches resulted in poor efficiency in the management of plant viruses with superior virulence such as the strains of tomato spotted wilt virus breaking the Sw5 resistance, strains of cucumber mosaic virus carrying necrogenic satellite RNAs, and necrogenic strains of potato virus Y. Three different studies from our lab documented that suitable levels of resistance/tolerance can be obtained by grafting commercial tomato varieties onto the tomato ecotype Manduria (Ma) rescued in the framework of an Apulian (southern Italy) regional program on biodiversity. Here we review the main approaches, methods, and results of the three case studies and propose some mechanisms leading to the tolerance/resistance observed in susceptible tomato varieties grafted onto Ma as well as in self-grafted plants. The proposed mechanisms include virus movement in plants, RNA interference, genes involved in graft wound response, resilience, and tolerance to virus infection.

Keywords: RNAi; disease tolerance/resistance; plant viruses; tomato ecotype; vegetable grafting; wound and pathogen response.

Figure 1

Severe symptoms of a Sw5-RB strain of TSWV on tomato cv Regina (A) compared to the same variety grafted onto Manduria (B) during 2016 field tests.

Figure 2

Detection of TSWV in sections of self-grafted (G) and non-grafted (WT) N. benthamiana plants at 5, 8, and 13 dpi with TSWV-CiPz. (A). Cross sections were prepared from apex, inoculated leaf, above and below graft junction, and from main and lateral roots. Virus was detected by using an antiserum against the NSs protein. (B). Detection of TSWV-CiPz RNA in UC, Ma, UC/UC, Ma/Ma, and UC/Ma at 19 dpi. Viral RNA was detected by tissue print hybridization with a DIG-labelled RNA probe for TSWV M RNA. Cross sections were prepared from apex, stem junction of the inoculated leaf, above, at and below the graft junction and from principal root. M = mock-inoculated UC plant.

Figure 3

Proposed flow diagram of an airborne virus infection in grafted and non-grafted tomato plants. By the time of virus infection, a general graft wound-response is already active only in grafted plants (pink oval in the background). After cell-to-cell movement in epidermal cells, the virus enters the abaxial phloem, bypasses graft union (circled in red), and accumulates in roots following the source-to-sink phloem sap movement. In rootstock tissues, heavy loads of replicating viral RNA trigger RNAi, probably induces changes in defense gene expression, and signals molecules via interactions with specific transcription factors. Reduced virus loads move from roots into the scion bypassing the graft union and old leaves and spreads into young leaves where it may induce symptoms. Virus load is still sufficient to trigger RNAi and changes in defense gene expression. Between 14-21 days post infection (dpi), virus replication and load are very low, a tolerant state is activated and plant recovers from disease symptoms. In roots of non-grafted plants, the virus replicates actively and accumulates in root tissues by suppressing RNAi via the expression of its VSRs. Then, the virus spreads upward to infect systemically tomato leaves. Active virus replication and expression of its VSRs induce disease symptoms and hinders recovery.