Advances in automated and high-throughput imaging technologies have resulted in a deluge of high-resolution images and sensor data of plants. However, extracting patterns and features from this large corpus of data requires the use of machine learning (ML) tools to enable data assimilation and feature identification for stress phenotyping. Four stages of the decision cycle in plant stress phenotyping and plant breeding activities where different ML approaches can be deployed are (i) identification, (ii) classification, (iii) quantification, and (iv) prediction (ICQP). We provide here a comprehensive overview and user-friendly taxonomy of ML tools to enable the plant community to correctly and easily apply the appropriate ML tools and best-practice guidelines for various biotic and abiotic stress traits.

Deep learning (DL), a subset of machine learning approaches, has emerged as a versatile tool to assimilate large amounts of heterogeneous data and provide reliable predictions of complex and uncertain phenomena. These tools are increasingly being used by the plant science community to make sense of the large datasets now regularly collected via high-throughput phenotyping and genotyping. We review recent work where DL principles have been utilized for digital image-based plant stress phenotyping. We provide a comparative assessment of DL tools against other existing techniques, with respect to decision accuracy, data size requirement, and applicability in various scenarios. Finally, we outline several avenues of research leveraging current and future DL tools in plant science.

Current approaches for accurate identification, classification, and quantification of biotic and abiotic stresses in crop research and production are predominantly visual and require specialized training. However, such techniques are hindered by subjectivity resulting from inter- and intrarater cognitive variability. This translates to erroneous decisions and a significant waste of resources. Here, we demonstrate a machine learning framework’s ability to identify and classify a diverse set of foliar stresses in soybean [Glycine max (L.) Merr.] with remarkable accuracy. We also present an explanation mechanism, using the top-K high-resolution feature maps that isolate the visual symptoms used to make predictions. This unsupervised identification of visual symptoms provides a quantitative measure of stress severity, allowing for identification (type of foliar stress), classification (low, medium, or high stress), and quantification (stress severity) in a single framework without detailed symptom annotation by experts. We reliably identified and classified several biotic (bacterial and fungal diseases) and abiotic (chemical injury and nutrient deficiency) stresses by learning from over 25,000 images. The learned model is robust to input image perturbations, demonstrating viability for high-throughput deployment. We also noticed that the learned model appears to be agnostic to species, seemingly demonstrating an ability of transfer learning. The availability of an explainable model that can consistently, rapidly, and accurately identify and quantify foliar stresses would have significant implications in scientific research, plant breeding, and crop production. The trained model could be deployed in mobile platforms (e.g., unmanned air vehicles and automated ground scouts) for rapid, large-scale scouting or as a mobile application for real-time detection of stress by farmers and researchers. Significance Plant stress identification based on visual symptoms has predominately remained a manual exercise performed by trained pathologists, primarily due to the occurrence of confounding symptoms. However, the manual rating process is tedious, is time-consuming, and suffers from inter- and intrarater variabilities. Our work resolves such issues via the concept of explainable deep machine learning to automate the process of plant stress identification, classification, and quantification. We construct a very accurate model that can not only deliver trained pathologist-level performance but can also explain which visual symptoms are used to make predictions. We demonstrate that our method is applicable to a large variety of biotic and abiotic stresses and is transferable to other imaging conditions and plants.

Hyperspectral imaging is emerging as a promising approach for plant disease identification. The large and possibly redundant information contained in hyperspectral data cubes makes deep learning based identification of plant diseases a natural fit. Here, we deploy a novel 3D deep convolutional neural network (DCNN) that directly assimilates the hyperspectral data. Furthermore, we interrogate the learnt model to produce physiologically meaningful explanations. We focus on an economically important disease, charcoal rot, which is a soil borne fungal disease that affects the yield of soybean crops worldwide. Based on hyperspectral imaging of inoculated and mock-inoculated stem images, our 3D DCNN has a classification accuracy of 95.73% and an infected class F1 score of 0.87. Using the concept of a saliency map, we visualize the most sensitive pixel locations, and show that the spatial regions with visible disease symptoms are overwhelmingly chosen by the model for classification. We also find that the most sensitive wavelengths used by the model for classification are in the near infrared region (NIR), which is also the commonly used spectral range for determining the vegetative health of a plant. The use of an explainable deep learning model not only provides high accuracy, but also provides physiological insight into model predictions, thus generating confidence in model predictions. These explained predictions lend themselves for eventual use in precision agriculture and research application using automated phenotyping platforms.

Plant stress phenotyping is essential to select stress-resistant varieties and develop better stress-management strategies. Standardization of visual assessments and deployment of imaging techniques have improved the accuracy and reliability of stress assessment in comparison with unaided visual measurement. The growing capabilities of machine learning (ML) methods in conjunction with image-based phenotyping can extract new insights from curated, annotated, and high-dimensional datasets across varied crops and stresses. We propose an overarching strategy for utilizing ML techniques that methodically enables the application of plant stress phenotyping at multiple scales across different types of stresses, program goals, and environments.

Phenotyping is a critical component of plant research. Accurate and precise trait collection, when integrated with genetic tools, can greatly accelerate the rate of genetic gain in crop improvement. However, efficient and automatic phenotyping of traits across large populations is a challenge; which is further exacerbated by the necessity of sampling multiple environments and growing replicated trials. A promising approach is to leverage current advances in imaging technology, data analytics and machine learning to enable automated and fast phenotyping and subsequent decision support. In this context, the workflow for phenotyping (image capture → data storage and curation → trait extraction → machine learning/classification → models/apps for decision support) has to be carefully designed and efficiently executed to minimize resource usage and maximize utility. We illustrate such an end-to-end phenotyping workflow for the case of plant stress severity phenotyping in soybean, with a specific focus on the rapid and automatic assessment of iron deficiency chlorosis (IDC) severity on thousands of field plots. We showcase this analytics framework by extracting IDC features from a set of ~4500 unique canopies representing a diverse germplasm base that have different levels of IDC, and subsequently training a variety of classification models to predict plant stress severity. The best classifier is then deployed as a smartphone app for rapid and real time severity rating in the field. We investigated 10 different classification approaches, with the best classifier being a hierarchical classifier with a mean per-class accuracy of ~96%. We construct a phenotypically meaningful ‘population canopy graph’, connecting the automatically extracted canopy trait features with plant stress severity rating. We incorporated this image capture → image processing → classification workflow into a smartphone app that enables automated real-time evaluation of IDC scores using digital images of the canopy. We expect this high-throughput framework to help increase the rate of genetic gain by providing a robust extendable framework for other abiotic and biotic stresses. We further envision this workflow embedded onto a high throughput phenotyping ground vehicle and unmanned aerial system that will allow real-time, automated stress trait detection and quantification for plant research, breeding and stress scouting applications.