Arbuscular Mycorrhizae and the Computer Vision Techniques for their Identification

Keywords: Morphometric Classification, Soil Decontamination, Arbuscular Mycorrhizal Fungi, Automatic Identification System, Computer Vision

Abstract

This article aims to analyze the leading computer vision techniques and strategies used in designed systems to automatically identify arbuscular mycorrhizal fungi, addressing general aspects of mycorrhizae and their taxonomic classification. Mycorrhizae are symbiotic associations between plants' roots and certain fungi groups. They are characterized by great benefits to the surrounding soil, the plants, and the derived productive processes. The work was developed with a specialized information collection methodology based on specific search criteria, selecting relevant publications, in a time range between 2014 and 2021, in the Scopus, Scielo, Dialnet, and Google Scholar databases. The study's results revealed that fuzzy mathematical morphology is an essential technique in the segmentation of fungal spores. In general, the studies developed are based on a binary identification of the spores, where the Hough transform, and artificial neural networks are the combined techniques that report better results. This study concludes that it is possible to assist the identification process of mycorrhizal fungi from artificial vision techniques. It contributes by indicating a lack of information regarding non-binary classification systems, which are important and must be considered to support advanced classification processes, according to the number of families and genera reported in the literature.

Author Biographies

Jimilgton Enrique Soto Sogamoso* , Universidad de la Amazonia, Colombia

Universidad de la Amazonia, Florencia-Colombia, ji.soto@udla.edu.co

Jesús Emilio Pinto Lopera, Universidad de la Amazonia, Colombia

Universidad de la Amazonia, Florencia-Colombia, jes.pinto@udla.edu.co

Edwin Eduardo Millán Rojas, Universidad de la Amazonia, Colombia

Universidad de la Amazonia, Florencia-Colombia, e.millan@udla.edu.co

References

A. Báez-Pérez; A. Limón-Ortega; C. E. Ramírez-Barrientos; I. A. Ortega-Villalobos; E. A. Olivares-Arreola, “Efecto de biofertilizantes y agricultura de conservación en la producción de trigo en un Vertisol”, Rev. TERRA Latinoam., vol. 38. No. 3, pp. 569–581, 2020. https://doi.org/10.28940/terra.v38i3.649

J. F. Sandoval-Pineda; U. A. Pérez-Moncada; A. Rodríguez; E. Torres-Rojas, “Alta presencia de cadmio resulta en baja diversidad de hongos formadores de micorrizas arbusculares asociados a cacao (Theobroma cacao L.)”, Acta Biológica Colombiana, vol. 25, no. 3, pp. 333–344, 2020. http://dx.doi.org/10.15446/abc.v25n3.78746

A. Díaz Franco; D. Gálvez López; F. E. Ortiz Cháirez, “Bioinoculación y fertilización química reducida asociadas con el crecimiento de planta y productividad de sorgo”, Revista Internacional de Contaminación Ambiental, vol. 31, no. 3, pp. 245–252, 2015. http://www.scielo.org.mx/pdf/rica/v31n3/v31n3a4.pdf

L. P. Garzón, “Importancia de las micorrizas arbusculares (ma) para un uso sostenible del suelo en la amazonia colombiana”, Rev. Luna Azul, no. 42, pp. 217–234, 2016. https://revistasojs.ucaldas.edu.co/index.php/lunazul/article/view/1616

A. Díaz-Franco; F. Alejandro-Allende; F. E. Ortiz-Cháirez, “Características de planta y productividad de sorgo con dosis de micorriza arbuscular en Tamaulipas”, Revista Chapingo Serie Zonas Áridas, vol. 16, no. 1, pp. 33–38, 2017. https://www.redalyc.org/pdf/4555/455552312003.pdf

Y. M. Quiñones Martínez et al., “Comunidades vegetales en suelo de ecosistema semiárido y su relación con hongos micorrízicos”, Terra Latinoamericana, vol. 36, no. 4, pp. 381–391, 2018. https://doi.org/10.28940/terra.v36i4.401

M. Agüero-Fernández; L. G. Hernández-Montiel; A. Nieto-Garibay; E. Troyo-Diéguez; R. Zulueta-Rodríguez; B. Murillo-Amador, “Hongos micorrízicos arbusculares como agentes mitigadores del estrés salino por NaCl en plántulas de albahaca”, Nova Scientia, vol. 8, no. 17, pp. 60–86, 2016. https://doi.org/10.21640/ns.v8i17.533

M. M. Gupta; L. K. Abbott, “Exploring economic assessment of the arbuscular mycorrhizal symbiosis”, Symbiosis, vol. 83, no. 2, pp. 143–152, 2021. https://doi.org/10.1007/s13199-020-00738-0

I. A. Salmerón-Santiago; M. E. Pedraza-Santos; L. S. Mendoza-Oviedo; A. T. Chávez-Bárcenas, “Cronología de la taxonomía y cladística de los glomeromicetos”, Revista Fitotecnia Mexicana, vol. 38, no. 2, pp. 153–163, 2015. http://www.scielo.org.mx/pdf/rfm/v38n2/v38n2a5.pdf

Y. Rodríguez; Y. Dalpé; S. Séguin, “Clasificación taxonómica de la cepa de hongo micorrizógeno arbuscular INCAM-2 como Funneliformis mosseae, syn. Glomus mosseae”, Cultivos tropicales, vol. 35, no. 2, pp. 27–33, 2014.http://scielo.sld.cu/pdf/ctr/v35n2/ctr04214.pdf

E. C. L. Yang; C. Khoo-Lattimore; C. Arcodia, “A systematic literature review of risk and gender research in tourism”, Tourism Management, vol. 58, pp. 89–100, Feb. 2017. https://doi.org/10.1016/j.tourman.2016.10.011

J. P. W. Young, “A molecular guide to the taxonomy of arbuscular mycorrhizal fungi”, New Phytologist, vol. 193, no. 4, pp. 823–826, Mar. 2012. https://doi.org/10.1111/j.1469-8137.2011.04029.x

D. Redecker; A. Schüßler; H. Stockinger; S. L. Stürmer; J. B. Morton; C. Walker, “An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota)”, Mycorrhiza, vol. 23, no. 7, pp. 515–531, 2013. https://doi.org/10.1007/s00572-013-0486-y

H. J. Monroy L.; C. R. Salamanca; C. Cano; L. M. Moreno-Conn; J. O. Orduz-Rodríguez, “Influencia de las coberturas en cultivos de cítricos sobre los hongos formadores de micorrizas arbusculares en Oxisoles del piedemonte llanero colombiano”, Ciencia y Tecnología Agropecuaria, vol. 14, no. 1, pp. 53–65, Jan. 2013. https://doi.org/10.21930/rcta.vol14_num1_art:343

F. Oehl; E. Sieverding; J. Palenzuela; K. Ineichen; G. Alves da Silva, “Advances in Glomeromycota taxonomy and classification”, IMA Fungus, vol. 2, no. 2, pp. 191–199, 2011. https://doi.org/10.5598/imafungus.2011.02.02.10

S. E. Smith; S. Dickson, “Quantification of Active Vesicular-Arbuscular Mycorrhizal Infection Using Image Analysis and Other Techniques”, Australian Journal of Plant Physiology, vol. 18, no. 6, pp. 637–648, 1991. https://doi.org/10.1071/PP9910637

D. C. Green; R. Newsam; P. Jeffries; J. C. Dodd; A. Vilariño, “Quantification of mycelial development of arbuscular mycorrhizal fungi using image analysis”, Mycorrhiza, vol. 5, no. 2, pp. 105–113, 1994. https://doi.org/10.1007/BF00202341

J. Schindelin et al., “Fiji: an open-source platform for biological-image analysis”, Nature Methods, vol. 9, no. 7, pp. 676–682, 2012. https://doi.org/10.1038/nmeth.2019

A. Schüßler; C. Walker, The Glomeromycota: A species list with new families and new genera, CreateSpace Independent Publishing Platform, 2011. https://www.cabdirect.org/cabdirect/abstract/20198647552

S. Guzmán-González; J. Farías-Larios, “Biología y regulación molecular de la micorriza arbuscular”, Avances en Investigación Agropecuaria, vol. 9, no. 2, pp. 17–31, 2005. https://www.redalyc.org/articulo.oa?id=83790202

A. Khalil Gardezi; S. R. Márquez Berber; A. V. Ayala Garay, “Los usos y beneficios de las micorrizas en la agricultura”, in Desarrollo y tecnología. Aportaciones a los problemas de la sociedad, Primera edición, México, Plaza y Valdés Editores, 2015, pp. 243–265. https://www.researchgate.net/profile/Elizabeth-Acosta-2/publication/280114658_Sistema_Agroforestal_establecido_en_suelos_del_Distrito_de_Riego_028_Tulancingo_Hidalgo/links/55aaf4e208ae815a04279460/Sistema-Agroforestal-establecido-en-suelos-del-Distrito-de-Riego-028-Tulancingo-Hidalgo.pdf#page=244%20%0D

F. A. Rivera Páez; V. González Salazar; J. G. González Acosta; P. A. Ossa López, “Caracterización molecular, análisis morfológico y colonización micorrízica en la rizósfera del aguacate (Persea americana Mill) en Caldas, Colombia”, Acta Agronómica, vol. 65, no. 4, pp. 398–405, Dec. 2016. http://dx.doi.org/10.15446/acag.v65n4.51714

A. Pérez C.; F. Espitia D.; A. Núñez O.; R. Jiménez Z., “Diversidad de géneros de hongos formadores de micorrizas arbusculares asociados a pasto colosuana (Bothriochloa pertusa (L) A. Camus) en suelos compactados y no compactados del municipio de San Marcos, Sucre-Colombia”, Rev Colombiana Cienc Anim. - RECIA, vol. 7, no. 2, pp. 185–190, 2015. https://doi.org/10.24188/recia.v7.n2.2015.267

A. Pérez; K. Cury; L. Oviedo, “Colonización de micorrizas arbusculares en tres especies de pasturas del departamento de Sucre”, Temas Agrarios, vol. 21, no. 2, pp. 65–75, 2016. https://doi.org/10.21897/rta.v21i2.902

E. Furrazola; Y. Torres-Arias, “Parte II. Las micorrizas”, in Ecotecnologías para la restauración ecológica: los tratamientos de semillas y las micorrizas, La Habana, Editorial Academia,2018, pp. 55–92.

Z. Li; N. Wu; S. Meng; F. Wu; T. Liu, “Arbuscular mycorrhizal fungi (AMF) enhance the tolerance of Euonymus maackii Rupr. At a moderate level of salinity”, PLoS ONE, vol. 15, no. 4, pp. 1–16, 2020. https://doi.org/10.1371/journal.pone.0231497

F. López-Botía; D. Y. Peña “Presencia de esporas de hongos micorrízico arbusculares en cinco estados sucesionales de bosque altoandino Colombiano”, Revista De Investigación Agraria y Ambiental, vol. 9, no. 2, pp. 135–148, 2018. https://doi.org/10.22490/21456453.2194

J. D. Lewis, “Mycorrhizal Fungi, Evolution and Diversification of”, Encyclopedia of Evolutionary Biology, vol. 3, pp. 94–99, 2016. https://doi.org/10.1016/B978-0-12-800049-6.00251-1

K. J. Restrepo Giraldo; M. I. Montoya Correa; P. Henao Jaramillo; L. A. Gutiérrez; L. P. Molina Guzmán, “Caracterización de hongos micorrízicos arbusculares de suelos ganaderos del trópico alto y trópico bajo en Antioquia, Colombia”, Idesia (Arica), vol. 37, no. 1, pp. 35–44, Mar. 2019. http://dx.doi.org/10.4067/S0718-34292019005000301

M. Chen; M. Arato; L. Borghi; E. Nouri; D. Reinhardt, “Beneficial Services of Arbuscular Mycorrhizal Fungi – From Ecology to Application”, Frontiers in Plant Science, vol. 9, p. 1270, 2018. https://doi.org/10.3389/fpls.2018.01270

M. Ruiz-Sánchez; Y. Santana Baños; A. Y. Muñoz Hernández; A. Y. Martínez Robaina; B. V. Bharat, “Simbiosis de micorrizas arbusculares en plantas de arroz (Oryza sativa L.) en condiciones de inundación y secano”, Acta Agronómica, vol. 64, no. 3, pp. 227–233, 2015. https://doi.org/10.15446/acag.v64n3.43087

S. W. Graham; V. K. Y. Lam; V. S. F. T. Merckx, “Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes”, New Phytologist, vol. 214, no. 1. pp. 48–55, Apr. 2017. https://doi.org/10.1111/nph.14398

X. Sun; W. Hu; M. Tang; H. Chen, “Characterizing and handling different kinds of AM fungal spores in the rhizosphere”, World Journal of Microbiology and Biotechnology, vol. 32, no. 6, p. 97, Abr. 2016. https://doi.org/10.1007/s11274-016-2053-0

M. Francis, Molecular Mycorrhizal Symbiosis. New Jersey: John Wiley & Sons, Inc., 2016.

H. K. Kehri; O. Akhtar; I. Zoomi; D. Pandey, “Arbuscular Mycorrhizal Fungi: Taxonomy and its Systematics”, Int. J. Life Sci. Res., vol. 6, no. 4, pp. 58–71, Oct. 2018. https://www.researchgate.net/publication/328289460_Arbuscular_Mycorrhizal_Fungi_Taxonomy_and_its_Systematics

W. Aguilar-Ulloa; P. Arce-Acuña; F. Galiano-Murillo; T. J. Torres-Cruz, “Aislamiento de esporas y evaluación de métodos de inoculación en la producción de micorrizas en cultivos trampa”, Tecnología en Marcha, vol. 29, no. 3, pp. 5–14, 2016. https://dx.doi.org/10.18845/tm.v29i7.2700

R. Akshaya; H. S. Kumar; D. Bhat, “A novel method to recognize object in Images using Convolution Neural Networks”. in 2019 IEEE International Conference on Intelligent Computing and Control Systems (ICCS), 2019, pp. 425-430. https://doi.org/10.1109/ICCS45141.2019.9065367

L. Jácome; L. Benavides; D. Jara; G. Riofrio; F. Alvarado; M. Pesantez, “A Survey on Intelligent Traffic Lights”, in 2018 IEEE International Conference on Automation/XXIII Congress of the Chilean Association of Automatic Control (ICA-ACCA), 2018, pp. 1–6. https://doi.org/10.1109/ICA-ACCA.2018.8609705

D. A. Heras Benavides, “Clasificador de imágenes de frutas basado en inteligencia artificial”, Killkana Técnica, vol. 1, no. 2, p. 21-30, Aug. 2017. https://doi.org/10.26871/killkana_tecnica.v1i2.79

R. Kotteswari; K. G. Sathiya, “Analysis of foreground detection in MRI images using region based segmentation”, in 2016 International Conference on Communication and Signal Processing (ICCSP), 2016, pp. 1062–1065. https://doi.org/10.1109/ICCSP.2016.7754312

D. Santos; L. Dallos; P. A. Gaona-García, “Algoritmos de rastreo de movimiento utilizando técnicas de inteligencia artificial y machine learning”, Información tecnológica, vol. 31, no. 3, pp. 23–38, Jun. 2020.

O. D. Velasco-Delgado; M. F. Pérez-Sandoval; J. F. Flórez-Marulanda, “Design and construction of automatic sorting station with machine vision”, TecnoLógicas, vol. 17, no. 32, pp. 97–109, Jan. 2014. https://doi.org/10.22430/22565337.200

Y. Zhao; F. Lin; S. Liu, Z. Hu; H. Li; Y. Bai, “Constrained-Focal-Loss Based Deep Learning for Segmentation of Spores”, in IEEE Access, vol. 7, pp. 165029–165038, 2019. https://doi.org/10.1109/ACCESS.2019.2953085

V. Stoian et al., “Sensitive approach and future perspectives in microscopic patterns of mycorrhizal roots”, Scientific Reports, vol. 9, no. 1, p. 10233, Jul. 2019. https://doi.org/10.1038/s41598-019-46743-2

G. Carotenuto; I. Sciascia; L. Oddi; V. Volpe; A. Genre, “Size matters: three methods for estimating nuclear size in mycorrhizal roots of Medicago truncatula by image analysis”, BMC Plant Biology, vol. 19, no. 1, p. 180, May. 2019. https://doi.org/10.1186/s12870-019-1791-1

J. Y. Tinevez et al., “TrackMate: An open and extensible platform for single-particle tracking”, Methods, vol. 115, pp. 80–90, Feb. 2017. https://doi.org/10.1016/j.ymeth.2016.09.016

A. Cardini; E. Pellegrino; E. del Dottore; H. A. Gamper; B. Mazzolai; L. Ercoli, “HyLength: a semi-automated digital image analysis tool for measuring the length of roots and fungal hyphae of dense mycelia,” Mycorrhiza, vol. 30, no. 2, pp. 229–242, Apr. 2020. https://doi.org/10.1007/s00572-020-00956-w

E. Evangelisti et al., “Deep learning-based quantification of arbuscular mycorrhizal fungi in plant roots”, New Phytologist, vol. 232, no. 5, pp. 2207–2219, Dec. 2021. https://doi.org/10.1111/nph.17697

C. A. O. Melo; J. G. Lopes; A. O. Andrade; R. M. P. Trindade; R. S. Magalhaes, “Semi-Automated Counting of Arbuscular Mycorrhizal Fungi Spores Using Artificial Neural Network”, in IEEE Latin America Transactions, vol. 15, no. 8, pp. 1566–1573, 2017. https://doi.org/10.1109/tla.2017.7994807

C. A. O. D. E. Melo; J. Lopes; A. Andrade; R. Trindade; R. Magalhães, “Semi-automated counting model for arbuscular mycorrhizal fungi spores using the Circle Hough Transform and an artificial neural network”, Anais da Academia Brasileira de Ciências, vol. 91, no. 4, pp. 1–15, 2019. https://doi.org/10.1590/0001-3765201920180165

A. O. Andrade et al., “Analysis of fuzzy morphology in spore counts of mycorrhizal fungi”, in 2015 Annual Conference of the North American Fuzzy Information Processing Society (NAFIPS) held jointly with 2015 5th World Conference on Soft Computing (WConSC), 2015, pp. 1–8. https://doi.org/10.1109/nafips-wconsc.2015.7284131

A. O. Andrade; R. M. P. Trindade; F. B. Bergamasch; A. Santos Barros; R. H. Nunes Santiago; A. M. Guimaraes Guerreiro, “Analyzing the R-Implications of Weber and Fodor in the Counting of Mycorrhizal Fungi Spores”, Journal of Communication and Computer, vol. 13, pp. 116–124, 2016. https://doi.org/10.17265/1548-7709/2016.03.002

Invam, “International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi”, http://fungi.invam.wvu.edu/

A. O. Andrade et al., “The counting of mycorrhizal fungi spores using fuzzy mathematical morphology”, in 2015 Annual Conference of the North American Fuzzy Information Processing Society (NAFIPS) held jointly with 2015 5th World Conference on Soft Computing (WConSC), 2015, pp. 1–6. https://doi.org/10.1109/nafips-wconsc.2015.7284167

A. S. Barros; A. O. Andrade; R. M. P. Trindade, “Utilização da morfologia fuzzy para quantificação de esporos de fungos micorrizicos”, Rev. Ciência da Comput, vol. 1, no. 1, pp. 1–7, Mar. 2019. https://doi.org/10.22481/recic.v1i1.4920

How to Cite
[1]
J. E. . Soto Sogamoso, J. E. Pinto Lopera, and E. E. Millán Rojas, “Arbuscular Mycorrhizae and the Computer Vision Techniques for their Identification”, TecnoL., vol. 25, no. 54, p. e2348, Aug. 2022.

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Published
2022-08-12
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Review Article

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