Messenger RNA exchange between scions and rootstocks in grafted grapevines

Yingzhen Yang, Linyong Mao, Yingyos Jittayasothorn, Youngmin Kang, Chen Jiao, Zhangjun Fei, Gan-Yuan Zhong

Grafting has been widely practiced for centuries in the propagation and production of many vegetable and fruit species. However, the underlying molecular and genetic mechanisms for how the graft partners interact with each other to produce a successful graft remain largely unknown. We hypothesized that genome-wide mRNA exchanges, which were recently documented in grafted model plant species, are a general phenomenon widely present in grafted plants, including those in vegetable and fruit species, and have specific genotype- and environment-dependent characteristics modulating plant performance. Using diagnostic SNPs derived from high throughput genome sequencing, we identified and characterized the patterns of genome-wide mRNA exchanges across graft junctions in grafted grapevines grown in the in vitro and field conditions. We identified more than 3000 genes transporting mRNAs across graft junctions. These genes were involved in diverse biological processes and those involved in basic cellular, biosynthetic, catabolic, and metabolic activities, as well as responses to stress and signal transduction, were highly enriched. Field-grown mature grafts had much fewer genes transmitting mRNAs than the in vitro young grafts (987 vs. 2679). These mobile mRNAs could move directionally or bi-directionally between scions and rootstocks. The mRNA transmission rates of these genes were generally low, with 65 % or more having transmission rates lower than 0.01. Furthermore, genotypes, graft combinations and growth environments had impact on the directions of mRNA movement as well as the numbers and species of mRNAs being exchanged. Moreover, we found evidence for the presences of both passive and selective mechanisms underlying long distance mRNA trafficking in grafted grapevines. We extended the studies of mRNA exchanges in model species to grapevines and demonstrated that genomic-scale mRNA exchange across graft junctions occurred in grapevines in a passive or genotype and environment-dependent manner.