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Abstract Graft compatibility is the capacity of two plants to form cohesive vascular connections. Tomato and pepper are incompatible graft partners; however, the underlying cause of graft rejection between these two species remains unknown. We diagnosed graft incompatibility between tomato and diverse pepper varieties based on weakened biophysical stability, decreased growth, and persistent cell death using viability stains. Transcriptomic analysis of the junction was performed using RNA sequencing, and molecular signatures for incompatible graft response were characterized based on meta-transcriptomic comparisons with other biotic processes. We show that tomato is broadly incompatible with diverse pepper cultivars. These incompatible graft partners activate prolonged transcriptional changes that are highly enriched for defense processes. Amongst these processes was broad nucleotide-binding and leucine-rich repeat receptors (NLR) upregulation and genetic signatures indicative of an immune response. Using transcriptomic datasets for a variety of biotic stress treatments, we identified a significant overlap in the genetic profile of incompatible grafting and plant parasitism. In addition, we found over 1000 genes that are uniquely upregulated in incompatible grafts. Based on NLR overactivity, DNA damage, and prolonged cell death, we hypothesize that tomato and pepper graft incompatibility is characterized by an immune response that triggers cell death which interferes with junction formation. 

Abstract Short-read RNA-seq studies of grafted plants have led to the proposal that thousands of messenger RNAs (mRNAs) move over long distances between plant tissues^1–7, potentially acting as signals^8–12. Transport of mRNAs between cells and tissues has been shown to play a role in several physiological and developmental processes in plants, such as tuberization¹³, leaf development¹⁴and meristem maintenance¹⁵; yet for most mobile mRNAs, the biological relevance of transport remains to be determined^16–19. Here we perform a meta-analysis of existing mobile mRNA datasets and examine the associated bioinformatic pipelines. Taking technological noise, biological variation, potential contamination and incomplete genome assemblies into account, we find that a high percentage of currently annotated graft-mobile transcripts are left without statistical support from available RNA-seq data. This meta-analysis challenges the findings of previous studies and current views on mRNA communication.