Parasitic plants of the genus Cuscuta (dodders) can bidirectionally exchange proteins, mRNAs and viruses with their hosts through their feeding structures, the haustoria. A new study in Nature now provides evidence for the transfer of microRNAs (miRNAs) from Cuscuta campestris to infected Arabidopsis thaliana hosts, which may increase the virulence of the parasite.
To study the movement of miRNAs between host plant and parasitic plant, Shahid et al. performed small RNA sequencing of three tissues — the host stem, the interface (that is, the C. campestris haustorium and the A. thaliana stem) and the parasite stem — and compared the small non-coding RNA profiles. Despite the expression of the majority of C. campestris small RNAs being decreased at the interface when compared with the parasite stem, the expression of 76 small RNAs was upregulated; 42 of these were miRNAs.
A total of 26 miRNAs were 22 nucleotides in length, which is an unusual miRNA class in plants that is known to induce secondary small interfering RNA (siRNA) production from target mRNAs, followed by an increase in miRNA-mediated silencing of target gene expression. Indeed, six A. thaliana mRNAs were identified as plausible targets for the C. campestris miRNAs, and siRNAs sharing complementary sequences were found at the interface, suggesting secondary siRNA induction in the host. Accordingly, five of the six transcripts showed reduced expression in stems infected by the parasite compared with uninfected controls. These mRNAs had previously been associated with pathogen-induced signalling (AFB2, AFB3, BIK1 and TIR1) and sugar content in detached leaves (SEOR1).
A. thaliana mutants of seor1 and afb3-4 showed increased parasite biomass, indicating a growth advantage for the parasite when the host was deficient in either gene product. Considering that the haustorium is used for nutrient acquisition, this suggests a role for seor1 suppression as a means to increase sugar intake and, therefore, growth of the parasite.
Given that orthologues of the A. thaliana target mRNAs are found across a range of plants belonging to the eudicot clade, and some of them were predicted to also be targeted by C. campestris miRNAs, the authors repeated the small-RNA-sequencing screen with parasite-infected Nicotiana benthamiana and obtained similar results.
“a mechanism of trans-species regulation of mRNA expression”
Together, the data presented in this study implicate C. campestris miRNA induction as a mechanism of trans-species regulation of mRNA expression in multiple hosts that might offer a virulence advantage to the parasite.
Shahid, S. et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553, 82–85 (2018)