Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant Cuscuta campestris.

Cuscuta spp. are obligate parasites that connect to host vascular tissue using a haustorium. In addition to water, nutrients, and metabolites, a large number of mRNAs are bidirectionally exchanged between Cuscuta spp. and their hosts. This trans-specific movement of mRNAs raises questions about whether these molecules function in the recipient species. To address the possibility that mobile mRNAs are ultimately translated, we built upon recent studies that demonstrate a role for transfer RNA (tRNA)-like structures (TLSs) in enhancing mRNA systemic movement. C. campestris was grown on Arabidopsis that expressed a ß-glucuronidase (GUS) reporter transgene either alone or in GUS-tRNA fusions. Histochemical staining revealed localization in tissue of C. campestris grown on Arabidopsis with GUS-tRNA fusions, but not in C. campestris grown on Arabidopsis with GUS alone. This corresponded with detection of GUS transcripts in Cuscuta on Arabidopsis with GUS-tRNA, but not in C. campestris on Arabidopsis with GUS alone. Similar results were obtained with Arabidopsis host plants expressing the same constructs containing an endoplasmic reticulum localization signal. In C. campestris, GUS activity was localized in the companion cells or phloem parenchyma cells adjacent to sieve tubes. We conclude that host-derived GUS mRNAs are translated in C. campestris and that the TLS fusion enhances RNA mobility in the host-parasite interactions.

Development of Parasitic Organs of a Stem Holoparasitic Plant in Genus Cuscuta.

Parasitic plants infect a broad range of plant species including economically important crops. They survive by absorbing water, minerals, and photosynthates from their hosts. To support their way of life, parasitic plants generally establish parasitic organs that allow them to attach to their hosts and to efficiently absorb substances from the vascular system of the host. Here, we summarize the recent progress in understanding the mechanisms underlying the formation of these parasitic organs, focusing on the process depicted in the stem holoparasitic genus, Cuscuta. An attachment structure called "holdfast" on the stem surface is induced by the light and contact stimuli. Concomitantly with holdfast formation, development of an intrusive structure called haustorium initiates in the inner cortex of the Cuscuta stem, and it elongates through apoplastic space of the host tissue. When haustoria reaches to host vascular tissues, they begin to form vascular conductive elements to connect vascular tissue of Cuscuta stem to those of host. Recent studies have shown parasite-host interaction in the interfacial cell wall, and regulation of development of these parasitic structures in molecular level. We also briefly summarize the role of host receptor in the control of compatibility between Cuscuta and hosts, on which occurrence of attachment structure depends, and the role of plant-to-plant transfer of long-distance signals after the establishment of conductive structure.

Differentiation of vascular elements in haustoria of Cuscuta japonica.

Parasitic plants establish vascular-conducting cells in an intrusive organ called haustorium. In haustoria of a stem parasitic plant, Cuscuta japonica, the presence of cells expressing cell-type-specific genes of phloem companion cell, phloem sieve element, procambial cell and xylem vessel has recently been demonstrated. Differentiation of these vascular cells is regulated in a manner similar to that in conventional vascular tissues. However, the initiation of procambial cells occurs concomitantly with the differentiation of vascular-conducting cells. The differentiation process of phloem also differed from that of conventional vascular tissues because enucleation of sieve elements appeared to be impeded. These results collectively imply that the vascular differentiation process in haustoria of parasitic plants may be different from that in conventional vascular tissues.

Organization of Vascular Cells in the Haustorium of the Parasitic Flowering Plant Cuscuta japonica.

The stem parasite dodder, Cuscuta japonica, has evolved a specialized root-like organ, the haustorium, which is differentiated from the stem. In order to take up water and nutrients, C. japonica reprograms haustorial cells to vascular cells, connecting the host's vascular system to its own. However, little is known about vascular differentiation in haustoria. In this study, we first confirmed the temporal and spatial expression profiles of vascular cell type-specific genes, CjAPL, CjSEOR1, CjWOX4 and CjTED7, to examine whether phloem companion cells, developing sieve elements, procambial cells and differentiating xylem cells, respectively, are present in the haustoria. CjAPL and CjSEOR1 decreased, and CjWOX4 showed a transient increase before the onset of xylem vessel formation, and then decreased. CjTED7 increased coincidentally with xylem vessel formation. In situ hybridization demonstrated that CjWOX4-expressing cells and phloem-conducting cells are in close proximity, and occupied a domain distinguishable from xylem vessels, suggesting differentiation of a phloem/procambial domain and a xylem domain in the haustorium. Secondly, expression of regulatory genes that are involved in determination of the fate of procambial cells was investigated. Expression patterns of CjCLE41, CjGSK3 and CjBES1suggested that TDIF-TDR-GSK3-mediated signaling is activated in haustoria. The natural antisense transcript of CjCLE41 was detected in haustoria, implying the sense regulation of CjCLE41. Expression profiles of the regulatory genes, combined with those of cell type-specific marker genes, suggest that reprogramming of haustorial cells to vascular cells is regulated in a way that allows the immediate formation of xylem vessels by alleviating inhibition of xylem differentiation.