Hyperspectral Measurements Enable Pre-Symptomatic Detection and Differentiation of Contrasting Physiological Effects of Late Blight and Early Blight in Potato

In-vivo foliar spectroscopy, also known as contact hyperspectral reflectance, enables rapid and non-destructive characterization of plant physiological status. This can be used to assess pathogen impact on plant condition both prior to and after visual symptoms appear. Challenging this capacity is the fact that dead tissue yields relatively consistent changes in leaf optical properties, negatively impacting our ability to distinguish causal pathogen identity. Here, we used in-situ spectroscopy to detect and differentiate Phytophthora infestans (late blight) and Alternaria solani (early blight) on potato foliage over the course of disease development and explored non-destructive characterization of contrasting disease physiology. Phytophthora infestans, a hemibiotrophic pathogen, undergoes an obligate latent period of two–seven days before disease symptoms appear. In contrast, A. solani, a necrotrophic pathogen, causes symptoms to appear almost immediately when environmental conditions are conducive. We found that respective patterns of spectral change can be related to these differences in underlying disease physiology and their contrasting pathogen lifestyles. Hyperspectral measurements could distinguish both P. infestans-infected and A. solani-infected plants with greater than 80% accuracy two–four days before visible symptoms appeared. Individual disease development stages for each pathogen could be differentiated from respective controls with 89–95% accuracy. Notably, we could distinguish latent P. infestans infection from both latent and symptomatic A. solani infection with greater than 75% accuracy. Spectral features important for late blight detection shifted over the course of infection, whereas spectral features important for early blight detection remained consistent, reflecting their different respective pathogen biologies. Shortwave infrared wavelengths were important for differentiation between healthy and diseased, and between pathogen infections, both pre- and post-symptomatically. This proof-of-concept work supports the use of spectroscopic systems as precision agriculture tools for rapid and early disease detection and differentiation tools, and highlights the importance of careful consideration of underlying pathogen biology and disease physiology for crop disease remote sensing.

[1]  Erich-Christian Oerke,et al.  Sensory assessment of Cercospora beticola sporulation for phenotyping the partial disease resistance of sugar beet genotypes , 2019, Plant Methods.

[2]  Roberta E. Martin,et al.  Quantifying forest canopy traits: Imaging spectroscopy versus field survey , 2015 .

[3]  Aditya Singh,et al.  Leaf and Canopy Level Detection of Fusarium Virguliforme (Sudden Death Syndrome) in Soybean , 2018, Remote. Sens..

[4]  P. J. Pinter,et al.  Remote sensing for crop protection , 1993 .

[5]  Philip A. Townsend,et al.  Spectroscopic Determination of Leaf Nitrogen Concentration and Mass Per Area in Sweet Corn and Snap Bean , 2016 .

[6]  Roberta E. Martin,et al.  Spectral and chemical analysis of tropical forests: Scaling from leaf to canopy levels , 2008 .

[7]  Robert Powers,et al.  Multivariate Analysis in Metabolomics. , 2012, Current Metabolomics.

[8]  Max Kuhn,et al.  caret: Classification and Regression Training , 2015 .

[9]  M. Eberlin,et al.  Metabolomics of Solanum lycopersicum Infected with Phytophthora infestans Leads to Early Detection of Late Blight in Asymptomatic Plants , 2018, Molecules.

[10]  W. Fry,et al.  Phytophthora infestans: the plant (and R gene) destroyer. , 2008, Molecular plant pathology.

[11]  K. Lamour,et al.  The Spatiotemporal Genetic Structure of Phytophthora capsici in Michigan and Implications for Disease Management. , 2002, Phytopathology.

[12]  Matt J. Aitkenhead,et al.  Detection and differentiation between potato (Solanum tuberosum) diseases using calibration models trained with non-imaging spectrometry data , 2019, Comput. Electron. Agric..

[13]  N. Gudmestad,et al.  Effect of the F129L Mutation in Alternaria solani on Fungicides Affecting Mitochondrial Respiration. , 2005, Plant disease.

[14]  M. Hirafuji,et al.  Field phenotyping system for the assessment of potato late blight resistance using RGB imagery from an unmanned aerial vehicle , 2016 .

[15]  Raymond F. Kokaly,et al.  Plant phenolics and absorption features in vegetation reflectance spectra near 1.66 μm , 2015, Int. J. Appl. Earth Obs. Geoinformation.

[16]  Shawn P. Serbin Spectroscopic determination of leaf nutritional, morphological, and metabolic traits , 2012 .

[17]  Wenxiu Gao,et al.  Estimation of nitrogen, phosphorus, and potassium contents in the leaves of different plants using laboratory-based visible and near-infrared reflectance spectroscopy: comparison of partial least-square regression and support vector machine regression methods , 2013 .

[18]  Clayton C. Kingdon,et al.  Spectroscopic determination of leaf morphological and biochemical traits for northern temperate and boreal tree species. , 2014, Ecological applications : a publication of the Ecological Society of America.

[19]  R. Kokaly,et al.  Characterizing canopy biochemistry from imaging spectroscopy and its application to ecosystem studies , 2009 .

[20]  Kaitlin M. Gold,et al.  Investigating potato late blight physiological differences across potato cultivars with spectroscopy and machine learning. , 2020, Plant science : an international journal of experimental plant biology.

[21]  H. Lindqvist-Kreuze,et al.  Conserved RXLR Effector Genes of Phytophthora infestans Expressed at the Early Stage of Potato Infection Are Suppressive to Host Defense , 2017, Front. Plant Sci..

[22]  Julio Martin Duarte-Carvajalino,et al.  Evaluating Late Blight Severity in Potato Crops Using Unmanned Aerial Vehicles and Machine Learning Algorithms , 2018, Remote. Sens..

[23]  H. Nilsson Remote sensing and image analysis in plant pathology. , 1995, Annual review of phytopathology.

[24]  Kristian Kersting,et al.  Hyperspectral phenotyping on the microscopic scale: towards automated characterization of plant-pathogen interactions , 2015, Plant Methods.

[25]  W. Fry The Canon of Potato Science: 10. Late Blight and Early Blight , 2007, Potato Research.

[26]  Shawn P Serbin,et al.  Spectroscopic sensitivity of real-time, rapidly induced phytochemical change in response to damage. , 2013, The New phytologist.

[27]  Minghua Zhang,et al.  Spectral prediction of Phytophthora infestans infection on tomatoes using artificial neural network (ANN) , 2008, International Journal of Remote Sensing.

[28]  Jg Horsfall,et al.  An improved grading system for measuring plant diseases , 1945 .

[29]  L. Plümer,et al.  Original paper: Early detection and classification of plant diseases with Support Vector Machines based on hyperspectral reflectance , 2010 .

[30]  Philip A. Townsend,et al.  Mapping foliar functional traits and their uncertainties across three years in a grassland experiment , 2019, Remote Sensing of Environment.

[31]  Chu Zhang,et al.  Early Detection of Botrytis cinerea on Eggplant Leaves Based on Visible and Near-Infrared Spectroscopy , 2008 .

[32]  J. G. Horskfall An Improved Grading System For Measuring Plant Diseases Vol-36 , 1945 .

[33]  P. Townsend,et al.  Integrating Spectroscopy with Potato Disease Management. , 2018, Plant disease.

[34]  R. Jackson Remote sensing of biotic and abiotic plant stress , 1986 .

[35]  I. Herrmann,et al.  Contact reflectance spectroscopy for rapid, accurate, and non-destructive Phytophthora infestans clonal lineage discrimination. , 2019, Phytopathology.

[36]  Anne-Katrin Mahlein Plant Disease Detection by Imaging Sensors - Parallels and Specific Demands for Precision Agriculture and Plant Phenotyping. , 2016, Plant disease.

[37]  P. Zarco-Tejada,et al.  Previsual symptoms of Xylella fastidiosa infection revealed in spectral plant-trait alterations , 2018, Nature Plants.

[38]  Aditya Singh,et al.  Associations of Leaf Spectra with Genetic and Phylogenetic Variation in Oaks: Prospects for Remote Detection of Biodiversity , 2016, Remote. Sens..

[39]  P. Townsend,et al.  Spectroscopic determination of ecologically relevant plant secondary metabolites , 2016 .

[40]  Clayton C. Kingdon,et al.  Imaging spectroscopy algorithms for mapping canopy foliar chemical and morphological traits and their uncertainties. , 2015, Ecological applications : a publication of the Ecological Society of America.

[41]  Marston Héracles Domingues Franceschini,et al.  Feasibility of Unmanned Aerial Vehicle Optical Imagery for Early Detection and Severity Assessment of Late Blight in Potato , 2019, Remote. Sens..

[42]  Yong He,et al.  Hyperspectral imaging for classification of healthy and gray mold diseased tomato leaves with different infection severities , 2017, Comput. Electron. Agric..

[43]  A. J. Haverkort,et al.  Societal Costs of Late Blight in Potato and Prospects of Durable Resistance Through Cisgenic Modification , 2008, Potato Research.

[44]  Hans-Peter Mock,et al.  Non-invasive Presymptomatic Detection of Cercospora beticola Infection and Identification of Early Metabolic Responses in Sugar Beet , 2016, Front. Plant Sci..

[45]  Minghua Zhang,et al.  Remote Sensed Spectral Imagery to Detect Late Blight in Field Tomatoes , 2005, Precision Agriculture.

[46]  K. Kohmoto,et al.  Host-specific toxins and chemical structures from alternaria species. , 1983, Annual review of phytopathology.

[47]  Steven B. Johnson,et al.  Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen. , 2015, Phytopathology.

[48]  Joanna Kaczmarek,et al.  Hyperspectral and Thermal Imaging of Oilseed Rape (Brassica napus) Response to Fungal Species of the Genus Alternaria , 2015, PloS one.

[49]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[50]  G. N. Agrios Plant Pathogens and Disease: General Introduction , 2009 .

[51]  J. Simon,et al.  An improved clearing and mounting solution to replace chloral hydrate in microscopic applications1 , 2013, Applications in plant sciences.

[52]  Yong He,et al.  Detection of early blight and late blight diseases on tomato leaves using hyperspectral imaging , 2015, Scientific Reports.

[53]  B. Adolf,et al.  Occurrence of the F129L mutation in Alternaria solani populations in Germany in response to QoI application, and its effect on sensitivity , 2014 .

[54]  P. Reich The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto , 2014 .

[55]  L. Adam,et al.  Alteration of secondary metabolites' profiles in potato leaves in response to weakly and highly aggressive isolates of Phytophthora infestans. , 2012, Plant physiology and biochemistry : PPB.

[56]  B. Gao NDWI—A normalized difference water index for remote sensing of vegetation liquid water from space , 1996 .

[57]  P. Curran Remote sensing of foliar chemistry , 1989 .

[58]  Daniel S. Falster,et al.  Detecting myrtle rust (Austropuccinia psidii) on lemon myrtle trees using spectral signatures and machine learning , 2018 .

[59]  Anne-Katrin Mahlein,et al.  Hyperspectral Sensors and Imaging Technologies in Phytopathology: State of the Art. , 2018, Annual review of phytopathology.

[60]  G. Carter,et al.  Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. , 2001, American journal of botany.

[61]  L. Ponnala,et al.  Transcriptional dynamics of Phytophthora infestans during sequential stages of hemibiotrophic infection of tomato. , 2016, Molecular plant pathology.