In contrast to most autotrophic plants, which produce carbohydrates from carbon dioxide using photosynthesis, parasitic plants obtain water and nutrients by parasitizing host plants. Many important crop plants are infested by these heterotrophic plants, leading to severe agricultural loss and reduced food security. Understanding how host plants perceive and resist parasitic plants provides insight into underlying defense mechanisms and the potential for agricultural applications. In this review, we offer a comprehensive overview of the current understanding of host perception of parasitic plants and the pre-attachment and post-attachment defense responses mounted by the host. Since most current research overlooks the role of organ specificity in resistance responses, we also summarize the current understanding and cases of cross-organ parasitism, which indicates nonconventional haustorial connections on other host organs, for example, when stem parasitic plants form haustoria on their host roots. Understanding how different tissue types respond to parasitic plants could provide the potential for developing a universal resistance mechanism in crops against both root and stem parasitic plants. Expected final online publication date for the Annual Review of Plant Biology, Volume 73 is May 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Cuscuta species (dodders) are agriculturally destructive, parasitic angiosperms. These parasitic plants use haustoria as physiological bridges to extract nutrients and water from hosts. Cuscuta campestris has a broad host range and wide geographical distribution. While some wild tomato relatives are resistant, cultivated tomatoes are generally susceptible to C. campestris infestations. However, some specific Heinz tomato (Solanum lycopersicum) hybrid cultivars exhibit resistance to dodders in the field, but their defense mechanism was previously unknown. Here, we discovered that the stem cortex in these resistant lines responds with local lignification upon C. campestris attachment, preventing parasite entry into the host. LIF1 (Lignin Induction Factor 1, an AP2-like transcription factor), SlMYB55, and CuRLR1 (Cuscuta R-gene for Lignin-based Resistance 1, a CC-NBS-LRR) are identified as factors that confer host resistance by regulating lignification. SlWRKY16 is upregulated upon C. campestris infestation and potentially negatively regulates LIF1 function. Intriguingly, CuRLR1 may play a role in signaling or function as an intracellular receptor for receiving Cuscuta signals or effectors, thereby regulating lignification-based resistance. In summary, these four regulators control the lignin-based resistance response in specific Heinz tomato cultivars, preventing C. campestris from parasitizing resistant tomatoes. This discovery provides a foundation for investigating multilayer resistance against Cuscuta species and has potential for application in other essential crops attacked by parasitic plants.

Repression of miR408 activates the expression of three miR408 target genes, IbKCS, IbPCL, and IbGAUT, leading to activation of defense response against wounding in sweet potato.