Grafting alters tomato transcriptome and enhances tolerance to an airborne virus infection

Abstract

Grafting of commercial tomato varieties and hybrids on the tomato ecotype Manduria resulted in high levels of tolerance to the infection of Sw5 resistance-breaking strains of tomato spotted wilt virus and of severe cucumber mosaic virus strains supporting hypervirulent satellite RNAs that co-determine stunting and necrotic phenotypes in tomato. To decipher the basis of such tolerance, here we used a RNAseq analysis to study the transcriptome profiles of the Manduria ecotype and of the susceptible variety UC82, and of their graft combinations, exposed or not to infection of the potato virus Y recombinant strain PVY c-to. The analysis identified graft-and virus-responsive mRNAs differentially expressed in UC82 and Manduria, which led to an overall suitable level of tolerance to viral infection confirmed by the appearance of a recovery phenotype in Manduria and in all graft combinations. The transcriptome analysis suggested that graft wounding and viral infection had diverging effects on tomato transcriptome and that the Manduria ecotype was less responsive than the UC82 to both graft wounding and potyviral infection. We propose that the differential response to the two types of stress could account for the tolerance to viral infection observed in the Manduria ecotype as well as in the susceptible tomato variety UC82 self-grafted or grafted on the Manduria ecotype.

The Role of Grafting in the Resistance of Tomato to Viruses

“…This review gives a brief account of the results and proposes mechanisms probably involved in the resistance/tolerance observed in grafted plants of the three cases-study carried out in our laboratory to manage one Sw5-RB strain of TSWV [ 62 ], two CMV strains supporting stunting and necrogenic satRNAs [ 63 ], and one recombinant PVY strain necrogenic to tomato [ 64 ].…”

“…Molfettese (Mo), and commercial tomato hybrids, Faino (Fa), Messapico (Me), Taylor (Ta) or not Pullrex (Pu), carrying the Sw5-resistance gene to TSWV and the tomato variety UC82 (UC) as highly susceptible control. Tests were carried out with cleft-grafted and non-grafted plants rub-inoculated on the first leaf above the graft junction with sap extracted from infected plants and grown under glasshouse [ 62 , 63 , 64 ] or exposed to field inoculum (this review). According to Kumar et al [ 38 ], complete repair of graft wound would be achieved between 7 and 10 days after grafting, thus we were confident that by the time of inoculation, continuous cambial connections between scion and rootstock had been restored.…”

“…Chemiluminescent hybridization signals were used to detect and quantify the accumulation of viral RNA by using Glyceraldehyde 3-phosphate dehydrogenase ( GAPDH ) as housekeeping gene for normalization [ 65 ]. Viral genomic RNAs and virus-specific small interfering RNAs were separated on agarose or polyacrylamide gels, respectively, and detected by northern blot hybridization with specific radiolabeled or DIG-labeled probes [ 62 , 63 ] or by NGS sequencing [ 64 ].…”

“…Results provided unique information on gene differentially expressed (DEGs) in the two tomato genotypes in response to graft wound and virus infection. Genes were considered significantly differentially expressed only when log2 of their fold change (FC) expression (log2FC) was ≥1 with a false discovery rate (FDR) ≤ 0.05 [ 64 ]. Beyond the use of resistant rootstocks to manage specific soil-borne pathogens of tomato such as fungi, oomycetes, bacteria, and viruses [ 27 , 86 ], it has been suggested that grafting per se activates systemic defense mechanisms in response to the graft wound [ 87 , 88 ].…”

“…This percentage was close to the 8% DEGs of the total genes annotated in A. thaliana involved in plant wound healing process [ 89 , 90 ]. Most of the graft wound responsive DEGs encoded signal molecules that overlapped their role also in response to abiotic stress and pathogen attack [ 64 , 87 , 90 , 91 ]. Table 5 show a selection of such graft wound-responsive genes detected in mock-inoculated and infected tomato plants.…”