Non-Destructive Early Detection and Quantitative Severity Stage Classification of Tomato Chlorosis Virus (ToCV) Infection in Young Tomato Plants Using Vis-NIR Spectroscopy

Tomato chlorosis virus (ToCV) is a serious, emerging tomato pathogen that has a significant impact on the quality and quantity of tomato production worldwide. Detecting ToCV via means of spectral measurements in an early pre-symptomatic stage offers an alternative to the existing laboratory methods, leading to better disease management in the field. In this study, leaf spectra from healthy and diseased leaves were measured with a spectrometer. The diseased leaves were subjected to RT-qPCR for the detection and quantification of the titer of ToCV. Neighborhood component analysis (NCA) algorithm was employed for the feature selection of the effective wavelengths and the most important vegetation indices out of the 24 that were tested. Two machine learning methods, namely XY-fusion network (XY-F) and multilayer perceptron with automated relevance determination (MLP–ARD), were employed for the estimation of the disease existence and viral load in the tomato leaves. The results showed that before outlier elimination, the MLP–ARD classifier generally outperformed the XY-F network with an overall accuracy of 92.1% against 88.3% for the XY-F. Outlier elimination contributed to the performance of the classifiers as the overall accuracy for both XY-F and MLP–ARD reached 100%.

[1]  Reza Ehsani,et al.  Detection of multi-tomato leaf diseases (late blight, target and bacterial spots) in different stages by using a spectral-based sensor , 2018, Scientific Reports.

[2]  Tarin Paz-Kagan,et al.  Spectral assessment of two-spotted spider mite damage levels in the leaves of greenhouse-grown pepper and bean , 2017 .

[3]  D. Moshou,et al.  The potential of optical canopy measurement for targeted control of field crop diseases. , 2003, Annual review of phytopathology.

[4]  N. Katis,et al.  Transmission of Tomato chlorosis virus (ToCV) by Bemisia tabaci Biotype Q and Evaluation of Four Weed Species as Viral Sources. , 2016, Plant disease.

[5]  G. Wisler,et al.  Tomato chlorosis virus: a new whitefly-transmitted, Phloem-limited, bipartite closterovirus of tomato. , 1998, Phytopathology.

[6]  Adam Chlus,et al.  Hyperspectral Measurements Enable Pre-Symptomatic Detection and Differentiation of Contrasting Physiological Effects of Late Blight and Early Blight in Potato , 2020, Remote. Sens..

[7]  J. Roujean,et al.  Estimating PAR absorbed by vegetation from bidirectional reflectance measurements , 1995 .

[8]  M. Kalacska,et al.  Baseline assessment for environmental services payments from satellite imagery: a case study from Costa Rica and Mexico. , 2008, Journal of environmental management.

[9]  L. Plümer,et al.  Development of spectral indices for detecting and identifying plant diseases , 2013 .

[10]  Paul Scheunders,et al.  Close range hyperspectral imaging of plants: A review , 2017 .

[11]  G. Carter Ratios of leaf reflectances in narrow wavebands as indicators of plant stress , 1994 .

[12]  E. Verdin,et al.  Serological and molecular detection of Tomato chlorosis virus and Tomato infectious chlorosis virus in tomato , 2009 .

[13]  N. Broge,et al.  Comparing prediction power and stability of broadband and hyperspectral vegetation indices for estimation of green leaf area index and canopy chlorophyll density , 2001 .

[14]  L. Papayiannis,et al.  Rapid discrimination of Tomato chlorosis virus, Tomato infectious chlorosis virus and co-amplification of plant internal control using real-time RT-PCR. , 2011, Journal of virological methods.

[15]  H. Ramon,et al.  Early Disease Detection in Wheat Fields using Spectral Reflectance , 2003 .

[16]  D. Sims,et al.  Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages , 2002 .

[17]  D. M. Moss,et al.  Red edge spectral measurements from sugar maple leaves , 1993 .

[18]  A. Huete,et al.  A review of vegetation indices , 1995 .

[19]  Patrizia Busato,et al.  Machine Learning in Agriculture: A Review , 2018, Sensors.

[20]  K. Kim,et al.  Nuclear changes associated with euphorbia mosaic virus transmitted by the whitefly , 1979 .

[21]  William D. Philpot,et al.  Yellowness index: An application of spectral second derivatives to estimate chlorosis of leaves in stressed vegetation , 1999 .

[22]  B. Datt Remote Sensing of Chlorophyll a, Chlorophyll b, Chlorophyll a+b, and Total Carotenoid Content in Eucalyptus Leaves , 1998 .

[23]  D. Lamb,et al.  Evaluating ten spectral vegetation indices for identifying rust infection in individual wheat leaves , 2008, Precision Agriculture.

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

[25]  G. A. Blackburn,et al.  Quantifying Chlorophylls and Caroteniods at Leaf and Canopy Scales: An Evaluation of Some Hyperspectral Approaches , 1998 .

[26]  N. Boonham,et al.  Host Range Studies for Tomato chlorosis virus, and Cucumber vein yellowing virus Transmitted by Bemisia  tabaci (Gennadius) , 2006, European Journal of Plant Pathology.

[27]  Roberto Oberti,et al.  Detection of biotic and abiotic stresses in crops by using hierarchical self organizing classifiers , 2017, Precision Agriculture.

[28]  Jang-Kyun Seo,et al.  Molecular dissection of distinct symptoms induced by tomato chlorosis virus and tomato yellow leaf curl virus based on comparative transcriptome analysis. , 2018, Virology.

[29]  Chu Zhang,et al.  Hyperspectral Imaging for Presymptomatic Detection of Tobacco Disease with Successive Projections Algorithm and Machine-learning Classifiers , 2017, Scientific Reports.

[30]  Guang-Zhong Yang,et al.  Spatio-spectral classification of hyperspectral images for brain cancer detection during surgical operations , 2018, PloS one.

[31]  Siva Kumar Balasundram,et al.  A review of neural networks in plant disease detection using hyperspectral data , 2018, Information Processing in Agriculture.

[32]  L. Papayiannis,et al.  Epidemiology and genetic diversity of criniviruses associated with tomato yellows disease in Greece. , 2014, Virus research.

[33]  Forrest W. Nutter,et al.  Relationships between defoliation, leaf area index, canopy reflectance, and forage yield in the alfalfa-leaf spot pathosystem , 2002 .

[34]  A. Gitelson,et al.  Remote estimation of chlorophyll content in higher plant leaves , 1997 .

[35]  Xanthoula Eirini Pantazi,et al.  Spectral Identification of Disease in Weeds Using Multilayer Perceptron with Automatic Relevance Determination , 2018, Sensors.

[36]  Anne-Katrin Mahlein,et al.  Benefits of hyperspectral imaging for plant disease detection and plant protection: a technical perspective , 2018 .

[37]  E. Hoque,et al.  Spectral blue-shift of red edge minitors damage class of beech trees , 1992 .

[38]  P. Curran,et al.  A new technique for interpolating the reflectance red edge position , 1998 .

[39]  H. Ramon,et al.  Automatic detection of ‘yellow rust’ in wheat using reflectance measurements and neural networks , 2004 .

[40]  Bisun Datt,et al.  A New Reflectance Index for Remote Sensing of Chlorophyll Content in Higher Plants: Tests using Eucalyptus Leaves , 1999 .

[41]  J. Navas-Castillo,et al.  Tomato chlorosis virus, an emergent plant virus still expanding its geographical and host ranges , 2019, Molecular plant pathology.

[42]  Xanthoula Eirini Pantazi,et al.  Evaluation of hierarchical self-organising maps for weed mapping using UAS multispectral imagery , 2017, Comput. Electron. Agric..

[43]  D. Mulla Twenty five years of remote sensing in precision agriculture: Key advances and remaining knowledge gaps , 2013 .

[44]  Wang Jihua,et al.  Detection of Internal Leaf Structure Deterioration Using a New Spectral Ratio Index in the Near-Infrared Shoulder Region , 2014 .

[45]  Yuri A. Gritz,et al.  Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves. , 2003, Journal of plant physiology.

[46]  Natarajan Sriraam,et al.  Classification of focal and non-focal EEG signals using neighborhood component analysis and machine learning algorithms , 2018, Expert Syst. Appl..

[47]  N. Katis,et al.  Multiplex Detection of Criniviruses Associated with Epidemics of a Yellowing Disease of Tomato in Greece. , 2002, Plant disease.

[48]  John R. Miller,et al.  Hyperspectral vegetation indices and novel algorithms for predicting green LAI of crop canopies: Modeling and validation in the context of precision agriculture , 2004 .

[49]  Chaoyang Wu,et al.  Estimating chlorophyll content from hyperspectral vegetation indices : Modeling and validation , 2008 .

[50]  Pablo J. Zarco-Tejada,et al.  Early Detection and Quantification of Almond Red Leaf Blotch Using High-Resolution Hyperspectral and Thermal Imagery , 2016, Remote. Sens..

[51]  G. Wisler,et al.  Tomato infectious chlorosis virus — a new clostero-like virus transmitted byTrialeurodes vaporariorum , 1996, European Journal of Plant Pathology.

[52]  Rebecca L. Whetton,et al.  Machine learning based prediction of soil total nitrogen, organic carbon and moisture content by using VIS-NIR spectroscopy , 2016 .

[53]  Dionysis Bochtis,et al.  Intelligent multi-sensor system for the detection and treatment of fungal diseases in arable crops , 2011 .

[54]  A. Gitelson,et al.  Non-destructive determination of chlorophyll content of leaves of a green and an aurea mutant of tobacco by reflectance measurements , 1996 .

[55]  Anne-Katrin Mahlein,et al.  Sensors and imaging techniques for the assessment of the delay of wheat senescence induced by fungicides. , 2013, Functional plant biology : FPB.

[56]  Y. Zhu,et al.  Detecting leaf nitrogen content in wheat with canopy hyperspectrum under different soil backgrounds , 2014, Int. J. Appl. Earth Obs. Geoinformation.

[57]  Anne-Katrin Mahlein,et al.  Recent advances in sensing plant diseases for precision crop protection , 2012, European Journal of Plant Pathology.

[58]  G. Poppy,et al.  A simple, light clip‐cage for experiments with aphids , 2018 .

[59]  Wei Yang,et al.  Neighborhood Component Feature Selection for High-Dimensional Data , 2012, J. Comput..

[60]  Brigitte Leblon,et al.  Potato Late Blight Detection at the Leaf and Canopy Levels Based in the Red and Red-Edge Spectral Regions , 2020, Remote. Sens..

[61]  Georg Noga,et al.  Presymptomatic Detection of Powdery Mildew Infection in Winter Wheat Cultivars by Laser-Induced Fluorescence , 2012, Applied spectroscopy.

[62]  Shie Mannor,et al.  Outlier-Robust PCA: The High-Dimensional Case , 2013, IEEE Transactions on Information Theory.

[63]  V. K. Gupta,et al.  Spectral reflectance pattern in soybean for assessing yellow mosaic disease , 2013, Indian Journal of Virology.

[64]  Mahdi Vasighi,et al.  Genetic Algorithms for architecture optimisation of Counter-Propagation Artificial Neural Networks , 2011 .

[65]  Svetlana M. Kochubey,et al.  Derivative vegetation indices as a new approach in remote sensing of vegetation , 2012, Frontiers of Earth Science.

[66]  G. Wisler,et al.  Vector Specificity, Host Range, and Genetic Diversity of Tomato chlorosis virus. , 2006, Plant disease.

[67]  P. Zimba,et al.  Detecting Sugarcane yellow leaf virus infection in asymptomatic leaves with hyperspectral remote sensing and associated leaf pigment changes. , 2010, Journal of virological methods.

[68]  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..

[69]  L. Buydens,et al.  Supervised Kohonen networks for classification problems , 2006 .

[70]  Avital Bechar,et al.  Robotic Disease Detection in Greenhouses: Combined Detection of Powdery Mildew and Tomato Spotted Wilt Virus , 2016, IEEE Robotics and Automation Letters.

[71]  Roberto Oberti,et al.  Plant disease detection based on data fusion of hyper-spectral and multi-spectral fluorescence imaging using Kohonen maps , 2005, Real Time Imaging.