Noninvasive Phenotyping of Plant-Pathogen Interaction: Consecutive In Situ Imaging of Fluorescing Pseudomonas syringae, Plant Phenolic Fluorescence, and Chlorophyll Fluorescence in Arabidopsis Leaves

. 2019 ; 10 () : 1239. [epub] 20191015

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31681362

Plant-pathogen interactions have been widely studied, but mostly from the site of the plant secondary defense. Less is known about the effects of pathogen infection on plant primary metabolism. The possibility to transform a fluorescing protein into prokaryotes is a promising phenotyping tool to follow a bacterial infection in plants in a noninvasive manner. In the present study, virulent and avirulent Pseudomonas syringae strains were transformed with green fluorescent protein (GFP) to follow the spread of bacteria in vivo by imaging Pulse-Amplitude-Modulation (PAM) fluorescence and conventional binocular microscopy. The combination of various wavelengths and filters allowed simultaneous detection of GFP-transformed bacteria, PAM chlorophyll fluorescence, and phenolic fluorescence from pathogen-infected plant leaves. The results show that fluorescence imaging allows spatiotemporal monitoring of pathogen spread as well as phenolic and chlorophyll fluorescence in situ, thus providing a novel means to study complex plant-pathogen interactions and relate the responses of primary and secondary metabolism to pathogen spread and multiplication. The study establishes a deeper understanding of imaging data and their implementation into disease screening.

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Aydi-Ben-Abdallah R., Jabnoun-Khiareddine H., Nefzi A., Daami-Remadi M. (2019). Growth promotion and Fusarium wilt suppression in tomato using endophytic bacteria recovered from two wild solanaceous species. Int. J. Adv. Agric. Sci. 4 (2), 01–16.

Barón M., Pineda M., Pérez-Bueno M. L. (2016). Picturing pathogen infection in plants. Z. Naturforsch. C 71 (9–10), 355–368. 10.1515/znc-2016-0134 PubMed DOI

Berger S., Sinha A. K., Roitsch T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. J. Exp. Bot. 58, 4019–4026. 10.1093/jxb/erm298 PubMed DOI

Bonfig K. B., Schreiber U., Gabler A., Roitsch T., Berger S. (2006). Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225, 1–12. 10.1007/s00425-006-0303-3 PubMed DOI

Bonfig K. B., Gabler A., Simon U. K., Luschin-Ebengreuth N., Hatz M., Berger S., et al. (2010). Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol. Plant 3 (6), 1037–1048. 10.1093/mp/ssq053 PubMed DOI

Bohnenkamp D., Kuska M. T., Mahlein A. K., Behmann J. (2019). Utilising pure fungal spore spectra as reference for a hyperspectral signal decomposition and symptom detection of wheat rust diseases on leaf scale. Plant Pathol. 68, 1188–1195. 10.1111/ppa.13020 DOI

Chaliha C., Rugen M. D., Field R. A., Kalita E. (2018). Glycans as modulators of plant defense against filamentous pathogens. Front. Plant Sci. 9, 928. 10.3389/fpls.2018.00928 PubMed DOI PMC

Carvalho C. P., Cardoso-Gustavson P., Rodrigues E., Braga M. R., Mercier H., Nievola C. C. (2019). Low temperature acclimation and de-acclimation of the subtropical bromeliad Nidularium minutum: implications of changes in the NO, sugar content and NR activity. Environ. Exp. Bot. 1159, 34–43. 10.1016/j.envexpbot.2018.12.004 DOI

Dong X., Wang M., Ling N., Shen Q., Guo S. (2016). Potential role of photosynthesis-related factors in banana metabolism and defense against Fusarium oxysporum f. sp. cubense. Environ. Exp. Bot. 129, 4–12. 10.1016/j.envexpbot.2016.01.005 DOI

Dong S., Beckles D. M. (2019). Dynamic changes in the starch–sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J. Plant Physiol. 234–235, 80–93. 10.1016/j.jplph.2019.01.007 PubMed DOI

Dobos O., Horvath P., Nagy F., Danka T., Viczián A. (2019). A deep learning-based approach for high-throughput hypocotyl phenotyping. bioRxiv, 1, 651729. 10.1101/651729 PubMed DOI PMC

Garavaglia B. S., Thomas L., Gottig N., Zimaro T., Garofalo C. G., Gehring C., et al. , (2010). Shedding light on the role of photosynthesis in pathogen colonization and host defense. Commun. Integr. Biol. 3, 382–384. 10.4161/cib.3.4.12029 PubMed DOI PMC

Ge Y., Wei M., Li C., Chen Y., Lv J., Meng K., et al. (2018). Reactive oxygen species metabolism and phenylpropanoid pathway involved in disease resistance against Penicillium expansum in apple fruit induced by ε-poly-L-lysine. J. Sci. Food Agric. 98, 5082–5088. 10.1002/jsfa.9046 PubMed DOI

Ghosal S., Blystone D., Singh A. K., Ganapathysubramanian B., Singh A., Sarkar S. (2018). An explainable deep machine vision framework for plant stress phenotyping. Proc. Natl. Acad. Sci. U. S. A. 115 (18), 4613–4618. 10.1073/pnas.1716999115 PubMed DOI PMC

Großkinsky D. B., Albacete A., Jammer A., Remele K., v. d. Graaff E., Pfeifhofer H., et al. (2014). A rapid phytohormone and phytoalexin screening method for physiological phenotyping. Mol. Plant 7, 1053–1056. 10.1093/mp/ssu015 PubMed DOI

Großkinsky D. K., Tafner R., Moreno M. V., Stenglein S. A., De Salamone I. E. G., Nelson L. M., et al. (2016. a). Cytokinin production by Pseudomonas fluorescens G20-18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis . Sci. Rep. 6, 23310. 10.1038/srep23310 PubMed DOI PMC

Großkinsky D. K., van der Graaff E., Roitsch T. (2016. b). Regulation of abiotic and biotic stress responses by plant hormones. Plant pathogen resistance biotechnology 131, 131–147. 10.1002/9781118867716.ch7 DOI

Großkinsky D. K., Syaifullah S. J., Roitsch T. (2017). Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants. J. Exp. Bot. 69 (4), 825–844. 10.1093/jxb/erx333 PubMed DOI

Gutierrez-Arellano C., Mulligan M. (2018). A review of regulation ecosystem services and disservices from faunal populations and potential impacts of agriculturalisation on their provision, globally. Nat. Conserv. 30, 1. 10.3897/natureconservation.30.26989 DOI

Giorgetti L., Giorgi G., Cherubini E., Gervasi P. G., Della Croce C. M., Longo V., et al. (2018). Screening and identification of major phytochemical compounds in seeds, sprouts and leaves of Tuscan black kale Brassica oleracea (L.) ssp acephala (DC) var. sabellica L. Nat. Prod. Res. 32 (14), 1617–1626. 10.1080/14786419.2017.1392953 PubMed DOI

Hideg E., Schreiber U. (2007). Parallel assessment of ROS formation and photosynthesis in leaves by fluorescence imaging. Photosyn. Res. 92, 103–108. 10.1007/s11120-007-9146-4 PubMed DOI

Jammer A., Gasperl A., Luschin-Ebengreuth N., Heyneke E., Chu H., Cantero-Navarro E., et al. (2015). Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J. Exp. Botany. 22, 5531–5542. 10.1093/jxb/erv228 PubMed DOI

Jing X., Wang H., Gong B., Liu S., Wei M., Ai X., et al. (2018). Secondary and sucrose metabolism regulated by different light quality combinations involved in melon tolerance to powdery mildew. Plant Physiol. Biochem. 124, 77–87. 10.1016/j.plaphy.2017.12.039 PubMed DOI

Kanwar P., Jha G. (2018). Alterations in plant sugar metabolism: signatory of pathogen attack. Planta 28, 1–4. 10.1007/s00425-018-3018-3 PubMed DOI

Kuska M. T., Behmann J., Grosskinsky D. K., Roitsch T., Mahlein A. K. (2018). Screening of barley resistance against powdery mildew by simultaneous high-throughput enzyme activity signature profiling and multispectral imaging. Front. Plant Sci. 9, 1074. 10.3389/fpls.2018.01074 PubMed DOI PMC

Kuska M. T., Behmann J., Namini M., Oerke E. C., Steiner U., Mahlein A. K. (2019). Discovering coherency of specific gene expression and optical reflectance properties of barley genotypes differing for resistance reactions against powdery mildew. PLoS One 14 (3), e0213291. 10.1371/journal.pone.0213291 PubMed DOI PMC

Lu Y., Yao J. (2018). Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int. J. Mol. Sci. 19, 3900. 10.3390/ijms19123900 PubMed DOI PMC

Liu X., Chen Y., Zhong M., Chen W., Lin Q., Du H. (2019). Isolation and pathogenicity identification of bacterial pathogens in bleached disease and their physiological effects on the red macroalga Gracilaria lemaneiformis . Aquat. Bot. 153, 1–7. 10.1016/j.aquabot.2018.11.002 DOI

Lozoya-Pérez N. E., Casas-Flores S., Martínez-Álvarez J. A., López-Ramírez L. A., Lopes-Bezerra L. M., Franco B., et al. (2018). Generation of Sporothrix schenckii mutants expressing the green fluorescent protein suitable for the study of host–fungus interactions. Fungal Biol. 122, 1023–1030. 10.1016/j.funbio.2018.07.004 PubMed DOI

Mahlein A. K., Alisaac E., Al Masri A., Behmann J., Dehne H. W., Oerke E. C. (2019). Comparison and combination of thermal, fluorescence, and hyperspectral imaging for monitoring Fusarium head blight of wheat on spikelet scale. Sensors 19, 2281. 10.3390/s19102281 PubMed DOI PMC

Maxwell K., Johnson G. N. (2000). Chlorophyll fluorescence—a practical guide. J. Exp. Bot. 51, 659–668. 10.1093/jexbot/51.345.659 PubMed DOI

Murchie E. H., Lawson T. (2013). Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J. Exp. Bot. 64 (13), 3983–3998. 10.1093/jxb/ert208 PubMed DOI

Ökmen B., Doehlemann G. (2014). Inside plant: biotrophic strategies to modulate host immunity and metabolism. Curr. Opin. Plant Biol. 20, 19–25. 10.1016/j.pbi.2014.03.011 PubMed DOI

Parente A. F., Silva-Pereira I., Baldani J. I., Tibúrcio V. H., Báo S. N., De-Souza M. T. (2008). Construction of Bacillus thuringiensis wild-type S76 and Cry-derivatives expressing a green fluorescent protein: two potential marker organisms to study bacteria-plant interactions. Can. J. Microbiol. 54, 786–790. 10.1139/W08-061 PubMed DOI

Pérez-Bueno M. L., Pineda M., Francisco M. C., Barón M. (2016). Multicolor fluorescence imaging as a candidate for disease detection in plant phenotyping. Front. Plant Sci. 7, 1790. 10.3389/fpls.2016.01790 PubMed DOI PMC

Pineda M., Pérez-Bueno M. L., Barón M. (2018). Detection of bacterial infection in melon plants by classification methods based on imaging data. Front. Plant Sci. 9, 164. 10.3389/fpls.2018.00164 PubMed DOI PMC

Pineda M., Bautista R., Martínez-Cruz J., Pérez-Bueno M. L., Barón M., Pérez-García A. (2019). RNA-seq analysis and fluorescence imaging of melon powdery mildew disease reveal an orchestrated reprogramming of host physiology. Sci. Rep. 9 (1), 7978. 10.1038/s41598-019-44443-5 PubMed DOI PMC

Polonio Á., Pineda M., Bautista R., Martínez-Cruz J., Pérez-Bueno M. L., Barón M., et al. (2019). RNA-seq analysis and fluorescence imaging of melon powdery mildew disease reveal an orchestrated reprogramming of host physiology. Sci. Rep. 9 (1), 7978. 10.1038/s41598-019-44443-5 PubMed DOI PMC

Preston G. M. (2000). Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol. Plant Pathol. 1, 263–275. 10.1046/j.1364-3703.2000.00036.x PubMed DOI

Proestos C., Zoumpoulakis P., Sinanoglou V. J. (2018). Isolation and characterization of phenolic compounds from selected foods of plant origin using modern spectroscopic approaches. Stud. Nat. Prod. Chem. 57, 203–220. 10.1016/B978-0-444-64057-4.00007-7 DOI

Quemada M., Gabriel J., Zarco-Tejada P. (2014). Airborne hyperspectral images and ground-level optical sensors as assessment tools for maize nitrogen fertilization. Remote Sens. (Basel) 6, 2940–2962. 10.3390/rs6042940 DOI

Rosa E., Woestmann L., Biere A., Saastamoinen M. (2018). A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore. Oikos 127, 1539–1549. 10.1111/oik.05437 DOI

Raacke I. C., von Rad U., Mueller M. J., Berger S. (2006). Yeast increases resistance in Arabidopsis against Pseudomonas syringae and Botrytis cinerea by salicylic acid–dependent as well as –independent mechanisms. Mol. Plant Microbe Interact. 19, 1138–1146. 10.1094/MPMI-19-1138 PubMed DOI

Riedel M., Calmin G., Belbahri L., Lefort F., Götz M., Wagner S., et al. (2009). Green fluorescent protein (GFP) as a reporter gene for the plant pathogenic oomycete Phytophthora ramorum . J. Eukaryot. Microbiol. 56, 130–135. 10.1111/j.1550-7408.2008.00376.x PubMed DOI

Rolfe S. A., Scholes J. D. (2010). Chlorophyll fluorescence imaging of plant–pathogen interactions. Protoplasma 247 (3–4), 163–175. 10.1007/s00709-010-0203-z PubMed DOI

Sperschneider J. (2019). Machine learning in plant–pathogen interactions: empowering biological predictions from field-scale to genome-scale. New Phytol. 10.1111/nph.15771 PubMed DOI

Su T., Han M., Min J., Chen P., Mao Y., Huang Q., et al. (2018). Genome-wide survey of invertase encoding genes and functional characterization of an extracellular fungal pathogen-responsive invertase in Glycine max. Int. J. Mol. Sci. 19 (8), 2395. 10.3390/ijms19082395 PubMed DOI PMC

Tischler Y. K., Thiessen E., Hartung E. (2018). Early optical detection of infection with brown rust in winter wheat by chlorophyll fluorescence excitation spectra. Comput. Electron. Agr. 146, 77–85. 10.1016/j.compag.2018.01.026 DOI

Thakur M., Bhattacharya S., Khosla P. K., Puri S. (2018). Improving production of plant secondary metabolites through biotic and abiotic elicitation. J. Appl. Res. Med. Aromat. Plants. 12, 1–12. 10.1016/j.jarmap.2018.11.004 DOI

Trouvelot S., Héloir M. C., Poinssot B., Gauthier A., Paris F., Guillier C., et al. (2014). Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front. Plant Sci. 5, 592. 10.3389/fpls.2014.00592 PubMed DOI PMC

Torti S. D., Dearing M. D., Kursar T. A. (1995). Extraction of phenolic compounds from fresh leaves: a comparison of methods. J. Chem. Ecol. 21, 117–125. 10.1007/BF02036646 PubMed DOI

Wang K., Kang L., Anand A., Lazarovits G., Mysore K. S. (2007). Monitoring in planta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv. New Phytol. 174, 212–223. 10.1111/j.1469-8137.2007.01999.x PubMed DOI

West J. S., Canning G. G., Perryman S. A., King K. (2017). Novel technologies for the detection of Fusarium head blight disease and airborne inoculum. Trop. Plant Pathol. 42, 203–209. 10.1007/s40858-017-0138-4 PubMed DOI PMC

Xue C., Liu Z., Dai L., Bu J., Liu M., Zhao Z., et al. (2018). Changing host photosynthetic, carbohydrate, and energy metabolisms play important roles in Phytoplasma infection. Phytopathology 108 (9), 1067–1077. 10.1094/PHYTO-02-18-0058-R PubMed DOI

Yang Y., Jiang N., Lai Y. T., Chang Y. Y., Yang X., Sun H., et al. (2019). Green fluorescent probe for imaging His6-tagged proteins inside living cells. ACS Sens. 4, 1190–1196. 10.1021/acssensors.8b01128 PubMed DOI

Zaynab M., Fatima M., Abbas S., Sharif Y., Umair M., Zafar M. H., et al. (2018). Role of secondary metabolites in plant defense against pathogens. Microb. Pathog. 124, 198–202. 10.1016/j.micpath.2018.08.034 PubMed DOI

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