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Leaf spectral reflectance of Hevea brasiliensis in response to Pseudocercospora ulei

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Abstract

South American Leaf Blight (SALB) is a fungal disease caused by the pathogen Pseudocercospora ulei. It is the main disease affecting rubber trees in Latin America. This study was designed to investigate the changes in the spectral reflectance of rubber leaflets inoculated with P. ulei under controlled conditions. Young leaflets of two clones of Hevea brasiliensis with different degrees of resistance to SALB were tested. The results demonstrated that SALB severity affected the spectral properties of the rubber leaflets, increasing the spectral reflectance in the visible range, decreasing the near-infrared range, and causing variating in the spectral vegetation indices. The changes were more obvious in the most susceptible clone (FX 3864) than in the most resistant one (FX 4098). The SALB severity classes were correlated with the relative chlorophyll content, the leaflet phenology, and the appearance of disease symptoms after the pathogen inoculation. New mathematical models for predicting the SALB severity in the leaflets B (10–18 days old) and C (22–30 days old) in the two rubber tree clones were designed.

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References

  • Alisaac, E., Behmann, J., Kuska, M. T., Dehne, H-W., & Mahlein, A-K. (2018). Hyperspectral quantification of wheat resistance to Fusarium head blight: Comparison of two Fusarium species. European Journal of Plant Pathology, 152, 869–884. https://doi.org/10.1007/s10658-018-1505-9.

  • Ashourloo, D., Mobasheri, M., & Huete, A. (2014). Evaluating the effect of different wheat rust disease symptoms on vegetation indices using Hyperspectral measurements. Remote Sensing, 6(6), 5107–5123. https://doi.org/10.3390/rs6065107.

    Article  Google Scholar 

  • Campbell, C. L., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: Wiley-Interscience, John Wiley & Sons.

    Google Scholar 

  • Cardoso, S. E. A., Freitas, T. A., da Silva, D. C., Gouvêa, L. R. L., de Gonçalves, P. S., Mattos, C. R. R., & Garcia, D. (2014). Comparison of growth, yield and related traits of resistant Hevea genotypes under high south American leaf blight pressure. Industrial Crops and Products, 53, 337–349. https://doi.org/10.1016/J.INDCROP.2013.12.033.

    Article  CAS  Google Scholar 

  • Datt, B. (1999). A new reflectance index for remote sensing of chlorophyll content in higher plants: Tests using Eucalyptus leaves. Journal of Plant Physiology, 154(1), 30–36. https://doi.org/10.1016/S0176-1617(99)80314-9.

    Article  CAS  Google Scholar 

  • Delalieux, S., Somers, B., Verstraeten, W. W., van Aardt, J. A. N., Keulemans, W., & Coppin, P. (2009). Hyperspectral indices to diagnose leaf biotic stress of apple plants, considering leaf phenology. International Journal of Remote Sensing, 30(8), 1887–1912. https://doi.org/10.1080/01431160802541556.

    Article  Google Scholar 

  • Delalieux, S., van Aardt, J., Keulemans, W., Schrevens, E., & Coppin, P. (2007). Detection of biotic stress (Venturia inaequalis) in apple trees using hyperspectral data: Non-parametric statistical approaches and physiological implications. European Journal of Agronomy, 27(1), 130–143. https://doi.org/10.1016/j.eja.2007.02.005.

    Article  Google Scholar 

  • Demmig-Adams, B., & Adams, W. W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science, 1(1), 21–26. https://doi.org/10.1016/S1360-1385(96)80019-7.

    Article  Google Scholar 

  • Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2017). InfoStat versión (2017). Córdoba, Ar.: Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

  • Gamon, J. A., Field, C. B., Bilger, W., Björkman, O., Fredeen, A. L., & Peñuelas, J. (1990). Remote sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies. Oecologia, 85(1), 1–7. https://doi.org/10.1007/BF00317336.

    Article  CAS  PubMed  Google Scholar 

  • Gamon, J. A., Peñuelas, J., & Field, C. B. (1992). A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment, 41(1), 35–44. https://doi.org/10.1016/0034-4257(92)90059-S.

    Article  Google Scholar 

  • Garcia, D., Troispoux, V., Grange, N., Rivano, F., & D’Auzac, J. (1999). Evaluation of the resistance of 36 Hevea clones to Microcyclus ulei and relation to their capacity to accumulate scopoletin and lignins. European Journal of Forest Pathology, 29, 323–338.

  • Gasparotto, L., Ferreira, F. A., Dos Santo, A. F., Rezende, P. J., & Furtado, E. L. (2012). Capítulo 3: Doenças das folhas. In L. Gasparotto & R. J. C. Pereira (Eds.), Doenças da seringueira no Brasil (pp. 39–176). Brasília, DF: EMBRAPA Amazônia Occidental.

    Google Scholar 

  • Gitelson, A. A., Merzlyak, M. N., & Chivkunova, O. B. (2001). Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochemistry and Photobiology, 74(1), 38–45. https://doi.org/10.1562/0031-8655(2001)074<0038:OPANEO>2.0.CO;2.

    Article  CAS  PubMed  Google Scholar 

  • Hallé, F., Oldeman, R., & Tomlinson, P. B. (1978). Tropical trees and forest. Berlin, DE: Springer.

    Book  Google Scholar 

  • Heim, R. H. J., Wright, I. J., Chang, H. C., Carnegie, A. J., Pegg, G. S., Lancaster, E. K., et al. (2018). Detecting myrtle rust (Austropuccinia psidii) on lemon myrtle trees using spectral signatures and machine learning. Plant Pathology, 67(5), 1–8. https://doi.org/10.1111/ppa.12830.

    Article  CAS  Google Scholar 

  • Hora Júnior, B. T., De Macedo, D. M., Barreto, R. W., Evans, H. C., Mattos, C. R. R., et al. (2014). Erasing the past: A new identity for the Damoclean pathogen causing south American leaf blight of rubber. PLoS One, 9(8), e104750. https://doi.org/10.1371/journal.pone.0104750.

  • Instituto Geográfico Agustin Codazzi (IGAC). (2010). Caquetá, características geográficas. Bogotá, DC: Imprenta nacional de Colombia.

    Google Scholar 

  • Jaimes, Y., Rojas, J., Cilas, C., & Furtado, E. L. (2016). Suitable climate for rubber trees affected by the south American leaf blight (SALB): Example for identification of escape zones in the Colombian middle Magdalena. Crop Protection, 81, 99–114. https://doi.org/10.1016/j.cropro.2015.12.016.

    Article  Google Scholar 

  • Jing, L., Jinbao, J., Yunhao, C., Yuanyuan, W., Wei, S., & Wenjiang, H. (2007). Using hyperspectral indices to estimate foliar chlorophyll a concentrations of winter wheat under yellow rust stress. New Zealand Journal of Agricultural Research, 50(5), 1031–1036. https://doi.org/10.1080/00288230709510382.

    Article  Google Scholar 

  • Junqueira, N. T. V., Chaves, G. M., Zambolim, L., Gasparotto, L., & Alfenas, A. C. (1986). Variabilidade fisiologica de Microcyclus ulei. Fitopatologia Brasileira, 11, 823–833.

    Google Scholar 

  • Karadağ, K., Tenekeci, M. E., Taşaltın, R., & Bilgili, A. (2019). Detection of pepper fusarium disease using machine learning algorithms based on spectral reflectance. Sustainable Computing: Informatics and Systems. https://doi.org/10.1016/j.suscom.2019.01.001.

    Book  Google Scholar 

  • Khaled, A. Y., Aziz, S. A., Bejo, S. K., Nawi, N. M., Seman, I. A., & Onwude, D. I. (2018). Early detection of diseases in plant tissue using spectroscopy – Applications and limitations. Applied Spectroscopy Reviews, 53(1), 36–64. https://doi.org/10.1080/05704928.2017.1352510.

    Article  Google Scholar 

  • Kobayashi, T., Kanda, E., Naito, S., Nakajima, T., Arakawa, I., Nemoto, K., Honma, M., Toujyou, H., Ishiguro, K., Kitada, K., & Torigoe, Y. (2003). Ratio of rice reflectance for estimating leaf blast severity with a multispectral radiometer. Journal of General Plant Pathology, 69(1), 17–22. https://doi.org/10.1007/s10327-002-0006-y.

    Article  Google Scholar 

  • Koop, D. M., Rio, M., Sabau, X., Almeida Cardoso, S. E., Cazevieille, C., Leclercq, J., & Garcia, D. (2016). Expression analysis of ROS producing and scavenging enzyme-encoding genes in rubber tree infected by Pseudocercospora ulei. Plant Physiology and Biochemistry, 104, 188–199. https://doi.org/10.1016/j.plaphy.2016.03.022.

    Article  CAS  PubMed  Google Scholar 

  • Kuska, M. T., & Mahlein, A. K. (2018). Aiming at decision making in plant disease protection and phenotyping by the use of optical sensors. European Journal of Plant Pathology, 152, 1–6. https://doi.org/10.1007/s10658-018-1464-1.

    Article  Google Scholar 

  • Kuska, M. T., Brugger, A., Thomas, S., Wahabzada, M., Kersting, K., Oerke, E.-C., Steiner, U., & Mahlein, A. K. (2017). Spectral patterns reveal early resistance reactions of barley against Blumeria graminis f. sp. hordei. Phytopathology, 107(11), 1388–1398. https://doi.org/10.1094/PHYTO-04-17-0128-R.

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler, H. K., Gitelson, A., & Lang, M. (1996). Non-destructive determination of chlorophyll content of leaves of a green and an Aurea mutant of tobacco by reflectance measurements. Journal of Plant Physiology, 148(3–4), 483–493. https://doi.org/10.1016/S0176-1617(96)80283-5.

    Article  CAS  Google Scholar 

  • Lieberei, R. (2007). South American leaf blight of the rubber tree (Hevea spp.): New steps in plant domestication using physiological features and molecular markers. Annals of Botany, 100(6), 1125–1142. https://doi.org/10.1093/aob/mcm133.

  • Mahlein, A.-K., Rumpf, T., Welke, P., Dehne, H.-W., Plümer, L., Steiner, U., & Oerke, E.-C. (2013). Development of spectral indices for detecting and identifying plant diseases. Remote Sensing of Environment, 128, 21–30. https://doi.org/10.1016/J.RSE.2012.09.019.

    Article  Google Scholar 

  • Mahlein, A.-K., Steiner, U., Dehne, H.-W., & Oerke, E.-C. (2010). Spectral signatures of sugar beet leaves for the detection and differentiation of diseases. Precision Agriculture, 11(4), 413–431. https://doi.org/10.1007/s11119-010-9180-7.

    Article  Google Scholar 

  • Marín-Ortiz, J. C., Gutierrez-Toro, N., Botero-Fernández, V., & Hoyos-Carvajal, L. M. (2019). Linking physiological parameters with visible/near-infrared leaf reflectance in the incubation period of vascular wilt disease. Saudi Journal of Biological Sciences. https://doi.org/10.1016/j.sjbs.2019.05.007.

  • Martinelli, F., Scalenghe, R., Davino, S., Panno, S., Scuderi, G., Ruisi, P., et al. (2015). Advanced methods of plant disease detection. A review. Agronomy for Sustainable Development, 35(1), 1–25. https://doi.org/10.1007/s13593-014-0246-1.

    Article  Google Scholar 

  • Martínez-Martínez, V., Gomez-Gil, J., Machado, M. L., & Pinto, F. A. C. (2018). Leaf and canopy reflectance spectrometry applied to the estimation of angular leaf spot disease severity of common bean crops. PLoS One, 4(13), 1–18.

  • Mattos, C. R. R., Garcia, D., Pinard, F., & Le Guen, V. (2003). Variabilidade de isolados de Microcyclus ulei no sudeste da Bahia. Fitopatologia Brasileira, 28(5), 502–507. https://doi.org/10.1590/S0100-41582003000500006.

    Article  Google Scholar 

  • Merzlyak, M. N., Gitelson, A. A., Chivkunova, O. B., & Rakitin, V. Y. U. (1999). Non-destructive optical detection of pigment changes during leaf senescence and fruit ripening. Physiologia Plantarum, 106(1), 135–141. https://doi.org/10.1034/j.1399-3054.1999.106119.x.

    Article  CAS  Google Scholar 

  • Miguel, A. A., de Oliveira, L. E. M., Cairo, P. A. R., & de Oliveira, D. M. (2007). Photosynthetic behaviour during the leaf ontogeny of rubber tree clones[Hevea brasiliensis (wild. Ex. Adr. de Juss.) Muell. Arg.], in Lavras, MG. Ciência e Agrotecnologia, 31(1), 91–97. doi:https://doi.org/10.1590/S1413-70542007000100014.

  • Peñuelas, J., Filella, I., & Gamon, J. A. (1995a). Assessment of photosynthetic radiation-use efficiency with spectral reflectance. New Phytologist, 131, 291–296. https://doi.org/10.1111/j.1469-8137.1995.tb03064.X.

    Article  Google Scholar 

  • Peñuelas, J., Baret, F., & Filella, I. (1995b). Semiempirical indices to assess carotenoids/chlorophyll a ratio from leaf spectral reflectance. Photosynthetica, 31(2), 221–230.

    Google Scholar 

  • Pietrzykowski, E., Stone, C., Pinkard, E., & Mohammed, C. (2006). Effects of Mycosphaerella leaf disease on the spectral reflectance properties of juvenile Eucalyptus globulus foliage. Forest Pathology, 36(5), 334–348. https://doi.org/10.1111/j.1439-0329.2006.00459.x.

    Article  Google Scholar 

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Team, C. (2014). Linear and nonlinear mixed effects models. R Package Version (Vol. 3).

  • R. Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for statistical Computing. http://www.r-project.org/

  • Richardson, A. D., Duigan, S. P., & Berlyn, G. P. (2002). An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist, 153(1), 185–194. https://doi.org/10.1046/j.0028-646X.2001.00289.x.

    Article  CAS  Google Scholar 

  • Rivano, F., Martinez, M., Cevallos, V., & Cilas, C. (2010). Assessing resistance of rubber tree clones to Microcyclus ulei in large-scale clone trials in Ecuador: A less time-consuming field method. European Journal of Plant Pathology, 126(4), 541–552. https://doi.org/10.1007/s10658-009-9563-7.

    Article  Google Scholar 

  • Rivano, F., Mattos, C. R. R., Cardoso, S. E. A., Martinez, M., Cevallos, V., Le Guen, V., & Garcia, D. (2013). Breeding Hevea brasiliensis for yield, growth and SALB resistance for high disease environments. Industrial Crops and Products, 44, 659–670. https://doi.org/10.1016/j.indcrop.2012.09.005.

    Article  Google Scholar 

  • Sterling, A., & Melgarejo, L. M. (2014). Variación temporal a Microcyclus ulei en los clones de caucho FX 3864 y FX 4098 en condiciones controladas. Revista Colombiana de Biotecnología, 16(2), 158–168. https://doi.org/10.15446/rev.colomb.biote.v16n2.47249.

    Article  Google Scholar 

  • Sterling, A., & Melgarejo, L. M. (2018). Leaf gas exchange and chlorophyll a fluorescence in Hevea brasiliensis in response to Pseudocercospora ulei infection. Physiological and Molecular Plant Pathology, 103, 143–150. https://doi.org/10.1016/j.pmpp.2018.07.006.

    Article  CAS  Google Scholar 

  • Sterling, A., & Rodríguez, C. (2018). Estrategias de Manejo para las principales enfermedades y plagas del cultivo del caucho con énfasis en la amazonia colombiana. Bogotá: Instituto Amazónico de Investigaciones Científicas SINCHI.

  • Sterling, A., Galindo-Rodríguez, L. C., Suárez-Córdoba, Y. D., Velasco-Anacona, G., Andrade-Ramírez, T., & Gómez-Torres, A. K. (2019). Early assessing performance and resistance of Colombian rubber tree genotypes under high south American leaf blight pressure in Amazon. Industrial Crops and Products, 141, 111775. https://doi.org/10.1016/j.indcrop.2019.111775.

    Article  CAS  Google Scholar 

  • Zhang, M., Liu, X., & O’Neill, M. (2002). Spectral discrimination of Phytophthora infestans infection on tomatoes based on principal component and cluster analyses. International Journal of Remote Sensing, 23(6), 1095–1107. https://doi.org/10.1080/01431160110106078.

    Article  Google Scholar 

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Acknowledgments

The authors acknowledge the financial support for Armando Sterling’s PhD thesis and this research provided by Colciencias (contract RC No.746 -2011), the Instituto Amazónico de Investigaciones Científicas Sinchi, the Universidad Nacional de Colombia, the Universidad de la Amazonía and the Asociación de Reforestadores y Cultivadores de Caucho del Caquetá Asoheca, and Christopher King for his English edition of this manuscript.

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  1. Laboratorio de Fitopatología, Instituto Amazónico de Investigaciones Científicas Sinchi, Facultad de Ciencias Básicas, Universidad de la Amazonía, Florencia, 180001, Colombia

    Armando Sterling

  2. Departamento de Biología, Facultad de Ciencias, Laboratorio de Fisiología y Bioquímica Vegetal, Universidad Nacional de Colombia, Sede Bogotá, Colombia

    Armando Sterling & Luz Marina Melgarejo

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  1. Armando Sterling
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Correspondence to Armando Sterling.

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Sterling, A., Melgarejo, L.M. Leaf spectral reflectance of Hevea brasiliensis in response to Pseudocercospora ulei. Eur J Plant Pathol 156, 1063–1076 (2020). https://doi.org/10.1007/s10658-020-01961-7

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