Transcriptomic Interpretation on Explainable AI-Guided Intuition Uncovers Premonitory Reactions of Disordering Fate in Persimmon Fruit

Deep neural network (DNN) techniques, as an advanced machine learning framework, have allowed various image diagnoses in plants, which often achieve better prediction performance than human experts in each specific field. Notwithstanding, in plant biology, the application of DNNs is still mostly limited to rapid and effective phenotyping. The recent development of explainable CNN frameworks has allowed visualization of the features in the prediction by a convolutional neural network (CNN), which potentially contributes to the understanding of physiological mechanisms in objective phenotypes. In this study, we propose an integration of explainable CNN and transcriptomic approach to make a physiological interpretation of a fruit internal disorder in persimmon, rapid over-softening. We constructed CNN models to accurately predict the fate to be rapid softening in persimmon cv. Soshu, only with photo images. The explainable CNNs, such as Gradient-weighted Class Activation Mapping (Grad-Class Activation Mapping (CAM)) and guided Grad-CAM, visualized specific featured regions relevant to the prediction of rapid softening, which would correspond to the premonitory symptoms in a fruit. Transcriptomic analyses to compare the featured regions of the predicted rapid-softening and control fruits suggested that rapid softening is triggered by precocious ethylene signal–dependent cell wall modification, despite exhibiting no direct phenotypic changes. Further transcriptomic comparison between the featured and non-featured regions in the predicted rapid-softening fruit suggested that premonitory symptoms reflected hypoxia and the related stress signals finally to induce ethylene signals. These results would provide a good example for the collaboration of image analysis and omics approaches in plant physiology, which uncovered a novel aspect of fruit premonitory reactions in the rapid-softening fate.