Long distance signalling and epigenetic changes in crop grafting

Abstract

Humans have used grafting for more than 4000 years to improve plant production, through physically joining two different plants, which can continue to grow as a single organism. Today, grafting is becoming increasingly more popular as a technique to increase the production of herbaceous horticultural crops, where rootstocks can introduce traits such as resistance to several pathogens and/or improving the plant vigour. Research in model plants have documented how long-distance signalling mechanisms across the graft junction, together with epigenetic regulation, can produce molecular and phenotypic changes in grafted plants. Yet, most of the studied examples rely on proof-of-concept experiments or on limited specific cases. This review explores the link between research findings in model plants and crop species. We analyse studies investigating the movement of signalling molecules across the graft junction and their implications on epigenetic regulation. The improvement of genomics analyses and the increased availability of genetic resources has allowed to collect more information on potential benefits of grafting in horticultural crop models. Ultimately, further research into this topic will enhance our ability to use the grafting technique to exploit genetic and epigenetic variation in crops, as an alternative to traditional breeding.

Keywords: DNA methylation; cucurbitaceous; epigenetic; graft junction; grafting; mobile siRNA; signaling molecules; solanaceous.

Figure 1

Four classes of mobile RNA molecules in plants. Potential mobile RNA molecules include messenger RNA (mRNA) molecules which encode proteins; transfer RNA (tRNA) -like structures which are associated to movement of RNA molecules; micro RNA (miRNA) which regulate gene expression by guiding gene silencing mechanisms such as Post Transcriptional Gene Silencing (PTGS) and small interfering RNAs (siRNA) which mediate the silencing of gene expression through PTGS and/or through Transcriptional Gene Silencing (TGS) via the RNA-directed DNA methylation pathway (RdDM). Figure created with BioRender.com.

Figure 2

The movement of small RNA (siRNA) between root and shoot drive epigenetic modifications and lead to phenotypical changes in the plant. The siRNAs can move both from root-to-shoot and shoot-to-roots directions, via the phloem through the sieve tubes. Once at the destination tissue, the siRNAs can alter DNA methylation at specific loci via the RNA-directed DNA Methylation (RdDM) pathway, or prevent the translation of a gene product via the Post-Transcriptional Gene Silencing (PTGS) pathway. Messenger RNAs (mRNA) can move across a systemically (and across a graft junction) into cells where they are translated into transcription factors (TFs) to control gene expression. Although not yet demonstrated in grafting experiment, siRNAs can introduce histone modifications. Alterations to these epigenetic marks can result in changes to the plant phenotype including resistance to abiotic and biotic stress, as well as alteration in the plant architecture and vigour. Figure created with BioRender.com.