4.8 Article

Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

Journal

PLANT CELL
Volume 34, Issue 1, Pages 535-556

Publisher

OXFORD UNIV PRESS INC
DOI: 10.1093/plcell/koab246

Keywords

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Funding

  1. Frank Lab startup funds from Cornell University College of Agriculture and Life Sciences
  2. National Science Foundation (NSF) [CAREER IOS-1942437, CAREER MCB-1453130]
  3. United States Department of Agriculture National institute of Food and Agriculture (USDA-NIFA) [2020-67011-31882]
  4. Foundation for Food and Agriculture Research [FFAR CA18-SS-0000000026]
  5. NIH [S10OD018516]

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This study investigated the phenomenon of incompatibility in grafting, identifying the cellular basis and key anatomical events of delayed incompatibility through a model system. Core regulatory factors for grafting were inferred based on these findings, with SlWOX4 identified as a potential regulator of graft compatibility through functional analysis.
Grafting has been adopted for a wide range of crops to enhance productivity and resilience; for example, grafting of Solanaceous crops couples disease-resistant rootstocks with scions that produce high-quality fruit. However, incompatibility severely limits the application of grafting and graft incompatibility remains poorly understood. In grafts, immediate incompatibility results in rapid death, but delayed incompatibility can take months or even years to manifest, creating a significant economic burden for perennial crop production. To gain insight into the genetic mechanisms underlying this phenomenon, we developed a model system using heterografting of tomato (Solanum lycopersicum) and pepper (Capsicum annuum). These grafted plants express signs of anatomical junction failure within the first week of grafting. By generating a detailed timeline for junction formation, we were able to pinpoint the cellular basis for this delayed incompatibility. Furthermore, we inferred gene regulatory networks for compatible self-grafts and incompatible heterografts based on these key anatomical events, which predict core regulators for grafting. Finally, we examined the role of vascular development in graft formation and uncovered SlWOX4 as a potential regulator of graft compatibility. Following this predicted regulator up with functional analysis, we show that Slwox4 homografts fail to form xylem bridges across the junction, demonstrating that indeed, SlWOX4 is essential for vascular reconnection during grafting, and may function as an early indicator of graft failure.

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