Abstract

AbstractPlants are exposed to infection and predation by organisms from most kingdoms of life, including their own. Layers of molecular defence mechanisms have evolved to limit damage and disease from microbial and insect pathogens, and plants can also defend themselves against attack by members of their own kingdom. These so‐called parasitic plants attach to and take up nutrients from a host plant. It is not yet known whether parasites belonging to the plant kingdom can elicit a systemic defence response in their hosts, to which they have much more in common molecularly than viruses and fungi. To gain insight as to whether previous infection reduces the susceptibility of a host, we used two successive rounds of infection of the same host plants with the holoparasitic plant Phelipanche ramosa (‘broomrape,’ Orobanchaceae). We tested seven cultivars of tomato, and found that the ‘Moneymaker’ cultivar was re‐infested at a lower rate than its naïve counterpart and, if pre‐infested, supported fewer parasites than other cultivars. We collected tissue for RNA sequencing at the host–parasite interface of two cultivars, ‘Moneymaker’ and ‘Zuckertraube’, the latter of which showed no difference in susceptibility upon reinfection. These data revealed tomato cultivar‐specific transcriptional profiles in the parasite, including the upregulation of several peroxidase genes in parasites infecting ‘Moneymaker’, compared to ‘Zuckertraube’. Furthermore, we detected the upregulation of lignin biosynthesis genes in ‘Moneymaker’ tomato plants when they were pre‐infected with the holoparasitic plant. Together, our data suggest that some tomato cultivars may be naturally able to build up defences against parasitic plant infection. This could be relevant for agriculture, in that cuttings or other forms of vegetative propagation of pre‐infected tomato plants can prime crops to withstand field infestations more effectively.

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