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Article|11 Sep 2024|OPEN
Graft incompatibility between pepper and tomato elicits an immune response and triggers localized cell death 
Hannah Rae Thomas1,2 , , Alice Gevorgyan1,3 , Alexandra Hermanson1 , Samantha Yanders1 , Lindsay Erndwein4,5 , Matthew Norman-Ariztía1 , Erin E. Sparks4 , Margaret H. Frank,1 ,
1School of Integrative Plant Science, Cornell University, Ithaca, NY 14850, USA
2Department of Cell and Developmental Biology, John Innes Centre, Norwich NR2 2DT, UK
3Department of Biology, Stanford University, Stanford, CA 94305, USA
4Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19713, USA
5Genetic Improvement for Fruits and Vegetables Laboratory, USDA-ARS, Chatsworth, NJ 08019, USA
*Corresponding author. E-mail: Hannah.Thomas@jic.ac.uk,mhf47@cornell.edu

Horticulture Research 12,
Article number: uhae255 (2025)
doi: https://doi.org/10.1093/hr/uhae255
Views: 2150

Received: 13 May 2024
Accepted: 02 Sep 2024
Published online: 11 Sep 2024

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.