Long‐distance transport of mRNA via parenchyma cells and phloem across the host–parasite junction in Cuscuta

Abstract

Summary• It has been shown that the parasitic plant dodder (Cuscuta pentagona) establishes a continuous vascular system through which water and nutrients are drawn. Along with solutes, viruses and proteins, mRNA transcripts are transported from the host to the parasite. The path of the transcripts and their stability in the parasite have yet to be revealed.• To discover the route of mRNA transportation, the in situ reverse transcriptasepolymerase chain reaction (RT-PCR) technique was used to locally amplify host transcript within parasitic tissue. The stability of host mRNA molecules was also checked by monitoring specific transcripts along the growing dodder thread.• Four mRNAs, α and β subunits of PYROPHOSPHATE (PPi)-DEPENDENT PHOS-PHOFRUCTOKINASE (LePFP), the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), and GIBBERELLIC ACID INSENSITIVE (LeGAI), were found to move from host (tomato (Solanum lycopersicum)) to dodder. LePFP mRNA was localized to the dodder parenchyma cells and to the phloem. LePFP transcripts were found in the growing dodder stem up to 30 cm from the tomato-dodder connection.• These results suggest that mRNA molecules are transferred from host to parasite via symplastic connections between parenchyma cells, move towards the phloem, and are stable for a long distance in the parasite. This may allow developmental coordination between the parasite and its host.

Interspecific RNA Interference of SHOOT MERISTEMLESS-Like Disrupts Cuscuta pentagona Plant Parasitism

“…The RNA silencing signal in plants also moves across graft junctions (Palauqui et al, 1997;Voinnet and Baulcombe, 1997). RNAs have been shown to freely translocate between parasitic plants and their hosts (Roney et al, 2007;David-Schwartz et al, 2008). For example, a b-glucuronidase silencing signal generated by the host roots was translocated across the haustorium and was shown to be functional in the facultative root parasite Triphysaria (Tomilov et al, 2008).…”

“…Furthermore, RNAi offers the advantages of being applicable to silencing of multigene family members and homologs in polyploids (Lawrence and Pikaard, 2003). It has been demonstrated that RNAs freely translocate between parasitic plants and their hosts (Roney et al, 2007;David-Schwartz et al, 2008). Thus, expression of RNAs that debilitate parasite development upon uptake, or RNAi in the host of target gene sequences specific to the parasite, are both strategies that are being explored for parasite control (Tomilov et al, 2007).…”

“…Macromolecules are naturally transported into the parasite from the host plant, and earlier reports have implicated haustorial connections in protein and RNA translocation between host and parasite (Mower et al, 2004;Roney et al, 2007;David-Schwartz et al, 2008). RNA movement between host and parasite has even been implicated in horizontal gene transfer between the host and parasite genomes.…”

Phloem sap intricacy and interplay with aphid feeding

“…For example, in the host-parasite junction of Cuscuta pentágona with tomato, several mRNAs were found to move from host to the dodder [180,181]. Some of the genes with mobile transcripts have roles in mediating plant response to the environment [180], and were proposed to allow some coordination between the parasite and its host [181]. This observation provides the potential to use gene-silencing technologies to increase resistance of crop plants against parasites by exploiting the interspecific trafficking of small interfering RNAs to target vital functions in the parasite.…”

A Three-Dimensional RNA Motif inPotato spindle tuber viroidMediates Trafficking from Palisade Mesophyll to Spongy Mesophyll inNicotiana benthamiana

“…Gene silencing signals containing siRNAs also traffic within a plant to mediate systemic RNA silencing as a means of antiviral defense (Ding and Voinnet, 2007;Kalantidis et al, 2008). RNA trafficking also occurs between some parasitic plants and their hosts, with biological functions yet to be understood (Roney et al, 2007;David-Schwartz et al, 2008).…”