On-tree ripening block of avocado fruit involves changes in ethylene sensitivity linked to gibberellin and auxin pathways

Avocado (Persea americana Mill.) fruit hang on the tree in a physiologically mature but unripe state for many months. We hypothesised that this was due to an on-tree ripening block that prevents the development of ethylene sensitivity in the fruit. Physiologically mature fruit, determined by size and dry matter content, were categorised into ethylene sensitive or insensitive based on whether an ethylene treatment at harvest accelerated ripening. Using tissue biopsies taken from the fruit 2 d prior to their harvest, ethylene-insensitive mature fruit were found to have retained the transcriptome profile of very young immature fruit and were enriched in transcripts related to gibberellin biosynthesis and auxin signalling. Transcript abundance of GIBBERELLIN 20-OXIDASE, GIBBERELLIN METHYLTRANSFERASE and IAA13 in mesocarp biopsies taken 7 d before the fruit were harvested could predict the ethylene sensitivity status of the fruit. Upon harvest, the fruit with low transcript abundance of these genes responded to the ethylene challenge by producing ethylene and ripening earlier, whereas the fruit with high transcript abundance were unresponsive to ethylene and ripened with similar timing to fruit not exposed to ethylene. We conclude that avocado fruit on-tree have different strengths of ripening inhibition, which is caused by the differential retention of gibberellin and auxin-related biology that affects their sensitivity to ethylene. •Avocado fruit do not ripen on the tree.•Fruit detached from the tree initiated ripening at varying times.•The acquisition of ethylene sensitivity controlled when ripening began.•Ethylene insensitive fruit were linked to auxin and gibberellin transcripts.•GMT, GAO and IAA13 mRNA abundance could predict fruit ethylene-insensitivity.