Transcriptomics of long-term, low oxygen storage coupled with ethylene signaling interference suggests neofunctionalization of hypoxia response pathways in apple (Malus domestica)

Authors: HADISH, JOHN - Washington State University; Hargarten, Heidi; ZHANG, HUITING - Washington State University; MATTHEIS, JAMES - Retired ARS Employee; FICKLIN, STEPHEN - Washington State University; Honaas, Loren

Submitted to: Plant Direct
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/29/2024
Publication Date: 12/20/2024
Citation: Hadish, J.A., Hargarten, H.L., Zhang, H., Mattheis, J.P., Ficklin, S.P., Honaas, L.A. 2024. Transcriptomics of long-term, low oxygen storage coupled with ethylene signaling interference suggests neofunctionalization of hypoxia response pathways in apple (Malus domestica). Plant Direct. 8(12). Article e70025. https://doi.org/10.1002/pld3.70025.
DOI: https://doi.org/10.1002/pld3.70025

Interpretive Summary: Postharvest management of apple fruits is important for reducing crop loss and ensuring that consumers receive high-quality produce at the grocery store. An important aspect of this management is making sure that batches of apples go to market prior to them going bad. Unfortunately, our understanding of how apples respond to multiple stresses during storage is very limited, which translates into an incomplete understanding of the root causes of apple spoilage. The work reported in this paper revealed that some of the apple fruit stress responses are potentially influenced by crop protectants that aim to help maintain fruit quality during storage. Further, we identified some genes that may play an important role in this process. This work is the culmination of years of effort that provided us with the tools to use results from other plant experiments to identify the apple genes that play an important role. This work advances the field of genomics in specialty crops. It also gives us new information that helps us understand how living apple fruit deals with stress during storage, which may lead to improved fruit storage protocols.

Technical Abstract: Research on how plants respond to hypoxia has concentrated on model organisms where tissues can only survive hypoxic conditions for a few hours to a few days. In contrast, hypoxic conditions are used commercially as a method to prolong the life of Malus domestica (apple) fruit for up to a year of storage without tissue death. This ability of apples to remain alive in hypoxic conditions is an interesting adaptation that has had limited molecular investigation despite its economic importance. Here we investigate the long-term apple hypoxia response using a time-course RNA-seq dataset collected for several post-harvest storage conditions. We use comparative phylogenies, differential expression, and regulatory networks to identify genes that regulate and are regulated by the hypoxia response. We identify potential neo-functionalizations of core-hypoxia response genes in apples, including novel regulation of sub-group VII Ethylene Response Factor (ERFVII) and plant cysteine oxidases (PCO) family members.