How do plants communicate, remember and evolve?
The Shahid lab investigates how regulatory RNAs, epigenetic processes, and genome plasticity shape intimate interactions between plants and other organisms, and how these interactions, in turn, influence genome evolution. Using parasitic plants as powerful models, we ask how small RNAs move between species, whether these encounters leave an epigenetic memory, and how genome plasticity enables the evolution of parasitism.
We combine comparative genomics and bioinformatics with molecular biology and genetics to uncover the mechanisms of interspecies communication and identify new routes to crop resilience. We also develop computational approaches for discovering and functionally annotating small RNA genes, including mobile small RNAs that regulate genes across species.
Our research is organised around three interconnected themes:
Interspecies RNA communication
Small RNAs are powerful regulators of gene expression across eukaryotes. Using the shoot parasitic plant Cuscuta, we demonstrated that parasite-derived small RNAs target host messenger RNAs, providing evidence for mobile small RNAs functioning in interspecies RNA interference (also known as trans-species RNAi) in plant–plant communication (Shahid et al., 2018, Nature, Yang et al., 2019, Nature Plants). We now investigate the mechanisms that determine which small RNAs become mobile, how they are trafficked between species, and how recipient cells recognise and respond to regulatory RNAs originating from another species. We are particularly interested in whether common principles govern small RNA exchange across antagonistic and beneficial interactions, from parasitic plants to symbiotic partners.
Understanding these processes allows us to address a broader question: how can one genome influence the activity of another without changing its DNA sequence?
Epigenetic memory
Plants can retain molecular traces of pathogen attack, sometimes across generations. But can a plant parasite remember its host? Parasitic plants offer an unusually powerful system for answering this question because they form long-lasting physiological connections with their hosts through haustoria, enabling sustained communication and bidirectional molecular exchange between two plant species. Unlike many acute microbial infections, these prolonged associations allow us to follow how interaction-induced chromatin states emerge, persist and change over much of the partners’ lifetimes.
We investigate the earliest signals that connect host–parasite recognition to chromatin reprogramming. We are particularly interested in which chromatin states are established by small RNAs through RNA-directed DNA methylation, which arise through small RNA-independent pathways, how long they persist and whether they alter the outcome of a subsequent encounter.
Previous host encounters may leave epigenetic states that retune parasite responsiveness or virulence towards future hosts. Determining whether these states are host-specific, persistent or reversible could help predict resistance breakdown and reveal how crop rotation influences parasite behaviour. On the host side, identifying persistent resistance states could uncover new targets for crop priming and breeding. Ultimately, this work could inform strategies that reinforce durable crop resistance and limit the emergence of increasingly virulent parasitic weeds.
Genome plasticity and the evolution of plant parasitism
The transition to parasitism represents one of the most dramatic lifestyle changes in plant evolution. A parasitic plant must recognise another species, establish a haustorial connection, and coordinate its development with a host. These intimate associations also create opportunities for horizontal gene transfer (HGT) between host and parasite genomes. But acquiring foreign DNA does not guarantee that it will become functional. Newly acquired sequences enter a genome equipped with small-RNA and chromatin-based surveillance systems that normally restrict foreign and mobile DNA, including transposable elements. Their epigenetic state may therefore determine whether they remain silent, are lost, or become available for evolutionary co-option.
Our previous work showed that horizontally acquired loci in Cuscuta are frequent sources of 24-nucleotide small RNAs and that at least one transferred locus overlaps an interspecies regulatory microRNA known to regulate host gene expression (Yang et al., 2019, Nature Plants). This raises the intriguing possibility that some of the foreign/invasive sequences initially subjected to genome surveillance can eventually be repurposed for interspecies regulation. Using some of the highly invasive parasitic weeds Cuscuta and Striga, we investigate how foreign DNA is recognised, epigenetically regulated and repurposed, and whether these processes contribute to epigenomic plasticity, adaptation and the evolution of parasitism. As part of this project, we are collaborating with the laboratories of Michael Timko (University of Virginia) and Claude dePamphilis (Penn State University) to sequence genomes and epigenomes from multiple Striga species.