533 Review Received: 4 July 2008 Revised: 23 October 2008 Accepted: 23 October 2008 Published online in Wiley Interscience: 02 March 2009 (www.interscience.wiley.com) DOI 10.1002/ps.1727 RNA translocation between parasitic plants and their hosts James H Westwood, * Jeannine K Roney, Piyum A Khatibi and Verlyn K Stromberg Abstract Recent research indicates that RNA translocation occurs between certain parasitic plant species and their hosts. The movement of at least 27 mRNAs has been demonstrated between hosts and Cuscuta pentagona Engelm., with the largest proportion of these being regulatory genes. Movement of RNAi signals has been documented from hosts to the parasites Triphysaria versicolor (Frisch & CA Mey) and Orobanche aegyptiaca (Pers.), demonstrating that the regulation of genes in one species can be influenced by transfer of RNA signals through a parasitic association. This review considers the implications of these findings in light of present understanding of host – parasite connections and the growing body of evidence that RNAs are able to act as signal molecules that convey regulatory information in a cell- and tissue-specific manner. Together, this suggests that parasitic plants can exchange RNAs with their hosts, and that this may be part of the coordinated growth and development that occurs during the process of parasitism. This phenomenon offers promise for new insights into parasitic plants, and new opportunities for the control of parasitic weeds. c  2009 Society of Chemical Industry Keywords: Cuscuta pentagona; Orobanche aegyptiaca; Triphysaria versicolor; RNA trafficking 1 INTRODUCTION Parasitic plants are some of the most intriguing of plant species, having evolved many adaptations for parasitism, such as reductions in root or leaf area and loss of photosynthetic capacity. However, the defining feature of parasitic plants is a specialized organ termed a haustorium, which functions to penetrate the host plant and form a physical and physiological bridge between the two species. 1 This union puts two different species in direct cellular contact with each other and defines the bulk of the interactions between them. The host–parasite interaction involves multiple levels of plant – plant communication, some of which are well characterized while others are almost unexplored. Well-studied signal exchanges include chemicals that stimulate germination of the seeds of parasitic species and other chemicals that initiate haustorium development in members of the Orobanchaceae. 2,3 For Cuscuta species, orientation toward volatile signals and thigmotropism has been described. 4,5 However, once the haustorium has penetrated the host tissue, little is known about the interchange between the two plants that leads the parasite to navigate correctly through the host tissues to make vascular contact and induce appropriate differentiation of cells. This is a vast unexplored territory of host–parasite interaction, and, while clues to host responses to parasitism have been gained from studies of host gene expression, 6–8 the mechanisms of plant-to-plant signaling have not been elucidated. Certainly, many factors can reasonably be postulated to play a role in this interaction, including mechanical pressure, osmotic potentials, hormone levels or sugar concentrations, and RNA can now be added to this list. With the recent reports that Cuscuta pentagona (Engelm.) takes up mRNAs from its hosts, 9,10 and that small interfering RNA (siRNA) expressed in the host can influence parasite gene expression in Triphysaria 11 and Orobanche, 12 it is appropriate to consider that RNA molecules may form a component of host–parasite communication. RNA molecules are increasingly being shown to function in regulating plant development, and the observation of RNA movement into three parasite species suggests that the phenomenon may widely occur in parasites. This review considers the potential mechanisms and implications of RNA as a signal molecule, and focuses on Cuscuta and species of the family Orobanchaceae. 2 HOST – PARASITE MOVEMENT OF RNA 2.1 Trafficking of mRNA The best-characterized incidence of host–parasite translocation of RNA is the movement of viruses through Cuscuta. The ability of Cuscuta to transmit viruses among infected and non-infected hosts through Cuscuta bridges has been known for over 60 years, 13 and at least 56 viruses have been documented as being transmitted by Cuscuta. 14 More recently, the transfer of a potato virus Y isolate N (PVY N ) between two tobacco (Nicotiana tabacum L.) plants across a Cuscuta bridge was quantitatively characterized. 15 Although the virus levels in both donor and recipient hosts were high, the levels in the Cuscuta bridge were nearly undetectable, suggesting that the virus passes through the parasite without significant multiplication inside the parasite. ∗ Correspondence to: James H Westwood, Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA 24061-0390, USA. E-mail: westwood@vt.edu Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA 24061-0390, USA Pest Manag Sci 2009; 65: 533–539 www.soci.org c  2009 Society of Chemical Industry