Abstract
Brown root rot, caused by infection of the basidiomycete Phellinus noxius (Corner) G. Cunn., threatens many tree species in forests, orchards, and plantations of tropical regions. However, the precise physiological impairment of the trees with disease progression remains inadequately understood. Here, we chronicle the root decay, water relation, and physiological traits of leaves using artificially inoculated seedlings of two tree species of different leafing habits, semi-deciduous Bischofia javanica Blume and evergreen Rhaphiolepis umbellata (Thunb.) Makino. Stomatal closure seemed to be the primary reaction, without either species exhibiting a decrease in root hydraulic conductance associated with hyphae invasion or change in stem water potential. Compared with R. umbellata, B. javanica with highly sensitive stomatal response, alleviated the deterioration in carboxylation from hyphae invasion by thermal dissipation of excessive energy. These physiological responses were detected earlier than the appearance of visible disease symptoms. Although there were some differences in chlorophyll fluorescence (ChlF) response between the two species, our results have demonstrated that decreases in stomatal conductance and changes in ChlF, possibly depending on the species' leafing habit are some of the initial physiological responses of trees during the early phase of brown root rot infection.
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The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aguadé, D., Poyatos, R., Gómez, M., Oliva, J., & Martínez-Vilalta, J. (2015). The role of defoliation and root rot pathogen infection in driving the mode of drought-related physiological decline in Scots pine (Pinus sylvestris L.). Tree Physiology, 35(3), 229–242. https://doi.org/10.1093/treephys/tpv005
Akiba, M., Ota, Y., Tsai, I. J., Hattori, T., Sahashi, N., & Kikuchi, T. (2015). Genetic differentiation and spatial structure of Phellinus noxius, the causal agent of brown root rot of woody plants in Japan. PLoS ONE, 10(10), e0141792. https://doi.org/10.1371/journal.pone.0141792
Ann, P.-J., Chang, T.-T., & Ko, W.-H. (2002). Phellinus noxius brown root rot of fruit and ornamental trees in Taiwan. Plant Disease, 86(8), 820–826. https://doi.org/10.1094/PDIS.2002.86.8.820
Arai, K., Shimizu, S., Miyajima, H., & Yamamoto, Y. (1989). Castaneiolide, abscisic acid and monorden, phytotoxic compounds isolated from fungi (Macrophoma castaneicola and Didymosporium radicicola) cause “black root rot disease” in chestnut trees. Chemical & Pharmaceutical Bulletin, 37(10), 2870–2872. https://doi.org/10.1248/cpb.37.2870
Berger, S., Papadopoulos, M., Schreiber, U., Kaiser, W., & Roitsch, T. (2004). Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiologia Plantarum, 122(4), 419–428. https://doi.org/10.1111/j.1399-3054.2004.00433.x
Berger, S., Sinha, A. K., & Roitsch, T. (2007). Plant physiology meets phytopathology: Plant primary metabolism and plant-pathogen interactions. Journal of Experimental Botany, 58(15–16), 4019–4026. https://doi.org/10.1093/jxb/erm298
Brummer, M., Arend, M., Fromm, J., Schlenzig, A., & Oßwald, W. F. (2002). Ultrastructural changes and immunocytochemical localization of the elicitin quercinin in Quercus robur L. roots infected with Phytophthora quercina. Physiological and Molecular Plant Pathology, 61(2), 109–120. https://doi.org/10.1006/pmpp.2002.0419
Christen, D., Schönmann, S., Jermini, M., Strasser, R. J., & Défago, G. (2007). Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. Environmental and Experimental Botany, 60(3), 504–514. https://doi.org/10.1016/j.envexpbot.2007.02.003
Chung, C.-L., Huang, S.-Y., Huang, Y.-C., Tzean, S.-S., Ann, P.-J., Tsai, J.-N., et al. (2015). The genetic structure of Phellinus noxius and dissemination pattern of brown root rot disease in Taiwan. PLoS ONE, 10(10), e0139445. https://doi.org/10.1371/journal.pone.0139445
Chung, C.-L., Lee, T. J., Akiba, M., Lee, H.-H., Kuo, T.-H., Liu, D., et al. (2017). Comparative and population genomic landscape of Phellinus noxius: A hypervariable fungus causing root rot in trees. Molecular Ecology, 26(22), 6301–6316. https://doi.org/10.1111/mec.14359
Cornic, G., & Fresneau, C. (2002). Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Annals of Botany, 89 Spec No, 887–894. https://doi.org/10.1093/aob/mcf064
Fleischmann, F., Koehl, J., Portz, R., Beltrame, A. B., & Osswald, W. (2005). Physiological changes of Fagus sylvatica seedlings infected with Phytophthora citricola and the contribution of its elicitin “citricolin” to pathogenesis. Plant Biology, 7(6), 650–658. https://doi.org/10.1055/s-2005-872891
Fleischmann, F., Schneider, D., Matyssek, R., & Osswald, W. F. (2002). Investigations on net CO2 assimilation, transpiration and root growth of Fagus sylvatica infested with four different Phytophthora species. Plant Biology, 4(2), 144–152. https://doi.org/10.1055/s-2002-25728
Fukuda, K. (1997). Physiological process of the symptom development and resistance mechanism in pine wilt disease. Journal of Forest Research, 2(3), 171–181. https://doi.org/10.1007/BF02348216
Galindo-Castañeda, T., Brown, K. M., Kuldau, G. A., Roth, G. W., Wenner, N. G., Ray, S., et al. (2019). Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize. Plant, Cell & Environment, 42(11), 2999–3014. https://doi.org/10.1111/pce.13615
Han, Q., Kagawa, A., Kabeya, D., & Inagaki, Y. (2016). Reproduction-related variation in carbon allocation to woody tissues in Fagus crenata using a natural 13C approach. Tree Physiology, 36(11), 1343–1352. https://doi.org/10.1093/treephys/tpw074
Han, Q., Kawasaki, T., Nakano, T., & Chiba, Y. (2008). Leaf-age effects on seasonal variability in photosynthetic parameters and its relationships with leaf mass per area and leaf nitrogen concentration within a Pinus densiflora crown. Tree Physiology, 28(4), 551–558. https://doi.org/10.1093/treephys/28.4.551
Hubbard, R. M., Ryan, M. G., Stiller, V., & Sperry, J. S. (2001). Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell & Environment, 24(1), 113–121. https://doi.org/10.1046/j.1365-3040.2001.00660.x
Ishida, A., Nakano, T., Harayama, H., Yazaki, K., Osone, Y., Kawarasaki, S., et al. (2009). Ecophysiological traits in leaves and stems of plants growing dry-ridge sites on the Bonin Islands. Ogasawara Research, 34, 1–7 [in Japanese with English summary]. https://cir.nii.ac.jp/crid/1370567187529019782
Kitao, M., Lei, T. T., Koike, T., Kayama, M., Tobita, H., & Maruyama, Y. (2007). Interaction of drought and elevated CO2 concentration on photosynthetic down-regulation and susceptibility to photoinhibition in Japanese white birch seedlings grown with limited N availability. Tree Physiology, 27(5), 727–735. https://doi.org/10.1093/treephys/27.5.727
Kitao, M., Lei, T. T., Koike, T., Tobita, H., & Maruyama, Y. (2003). Higher electron transport rate observed at low intercellular CO2 concentration in long-term drought-acclimated leaves of Japanese mountain birch (Betula ermanii). Physiologia Plantarum, 118(3), 406–413. https://doi.org/10.1034/j.1399-3054.2003.00120.x
Kojima, M., Kamada-Nobusada, T., Komatsu, H., Takei, K., Kuroha, T., Mizutani, M., et al. (2009). Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: An application for hormone profiling in Oryza sativa. Plant & Cell Physiology, 50(7), 1201–1214. https://doi.org/10.1093/pcp/pcp057
Lehmann, S., Serrano, M., L’Haridon, F., Tjamos, S. E., & Metraux, J.-P. (2015). Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry, 112, 54–62. https://doi.org/10.1016/j.phytochem.2014.08.027
Leinonen, I., & Jones, H. G. (2004). Combining thermal and visible imagery for estimating canopy temperature and identifying plant stress. Journal of Experimental Botany, 55(401), 1423–1431. https://doi.org/10.1093/jxb/erh146
Long, S. P., & Bernacchi, C. J. (2003). Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany, 54(392), 2393–2401. https://doi.org/10.1093/jxb/erg262
Luque, J., Cohen, M., Savé, R., Biel, C., & Álvarez, I. F. (1999). Effects of three fungal pathogens on water relations, chlorophyll fluorescence and growth of Quercus suber L. Annals of Forest Science, 56(1), 19–26. https://doi.org/10.1051/forest:19990103
Martínez-Ferri, E., Zumaquero, A., Ariza, M. T., Barceló, A., & Pliego, C. (2016). Nondestructive detection of white root rot disease in avocado rootstocks by leaf chlorophyll fluorescence. Plant Disease, 100(1), 49–58. https://doi.org/10.1094/PDIS-01-15-0062-RE
Maurel, M., Robin, C., Capron, G., & Desprez-Loustau, M.-L. (2001). Effects of root damage associated with Phytophthora cinnamomi on water relations, biomass accumulation, mineral nutrition and vulnerability to water deficit of five oak and chestnut species. Forest Pathology, 31(6), 353–369. https://doi.org/10.1046/j.1439-0329.2001.00258.x
Merrill, W. (1992). Mechanisms of resistance to fungi in woody plants: A historical perspective. In R. A. Blanchette & A. R. Biggs (Eds.), Defense Mechanisms of Woody Plants Against Fungi (pp. 1–12). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-662-01642-8_1
Nicole, M. R., Geiger, J. P., & Nandris, D. (1992). Defense of angiosperm roots against fungal invasion. In R. A. Blanchette & A. R. Biggs (Eds.), Defense Mechanisms of Woody Plants Against Fungi (pp. 181–206). Berlin Heidelberg: Springer. https://doi.org/10.1007/978-3-662-01642-8_10
Oliva, J., Stenlid, J., & Martínez-Vilalta, J. (2014). The effect of fungal pathogens on the water and carbon economy of trees: Implications for drought-induced mortality. The New Phytologist, 203(4), 1028–1035. https://doi.org/10.1111/nph.12857
Parke, J. L., Oh, E., Voelker, S., Hansen, E. M., Buckles, G., & Lachenbruch, B. (2007). Phytophthora ramorum colonizes tanoak xylem and is associated with reduced stem water transport. Phytopathology, 97(12), 1558–1567. https://doi.org/10.1094/PHYTO-97-12-1558
R Core Team. (2021). R: A language and environment for statistical computing. Vienna, Austria. https://www.R-project.org/
Robert, H. (1986). Effects of root pathogens on plant water relations. In P. G. Ayres & L. Boddy (Eds.), Water, Fungi and Plants (pp. 241–265). Cambridge University Press.
Sahashi, N., Akiba, M., Ishihara, M., Miyazaki, K., & Kanzaki, N. (2010). Cross inoculation tests with Phellinus noxius isolates from nine different host plants in the Ryukyu islands, southwestern japan. Plant Disease, 94(3), 358–360. https://doi.org/10.1094/PDIS-94-3-0358
Sahashi, N., Akiba, M., Ishihara, M., Ota, Y., & Kanzaki, N. (2012). Brown root rot of trees caused by Phellinus noxius in the Ryukyu Islands, subtropical areas of Japan. Forest Pathology, 42(5), 353–361. https://doi.org/10.1111/j.1439-0329.2012.00767.x
Sahashi, N., Akiba, M., Ota, Y., Masuya, H., Hattori, T., Mukai, A., et al. (2015). Brown root rot caused by Phellinus noxius in the Ogasawara (Bonin) Islands, southern Japan - current status of the disease and its host plants. Australasian Plant Disease Notes, 10(1), 33. https://doi.org/10.1007/s13314-015-0183-0
Sahashi, N., Akiba, M., Takemoto, S., Yokoi, T., Ota, Y., & Kanzaki, N. (2014). Phellinus noxius causes brown root rot on four important conifer species in Japan. European Journal of Plant Pathology, 140(4), 869–873. https://doi.org/10.1007/s10658-014-0503-9
Salleo, S., Nardini, A., Pitt, F., & Gullo, M. A. L. (2000). Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.). Plant, Cell & Environment, 23(1), 71–79. https://doi.org/10.1046/j.1365-3040.2000.00516.x
Shimizu, M., Ishida, A., & Hogetsu, T. (2005). Root hydraulic conductivity and whole-plant water balance in tropical saplings following a shade-to-sun transfer. Oecologia, 143(2), 189–197. https://doi.org/10.1007/s00442-004-1797-7
Shinozaki, Y., Hao, S., Kojima, M., Sakakibara, H., Ozeki-Iida, Y., Zheng, Y., et al. (2015). Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. The Plant Journal, 83(2), 237–251. https://doi.org/10.1111/tpj.12882
Stewart, J. E., Kim, M.-S., Ota, Y., Sahashi, N., Hanna, J. W., Akiba, M., et al. (2020). Phylogenetic and population genetic analyses reveal three distinct lineages of the invasive brown root-rot pathogen, Phellinus noxius, and bioclimatic modeling predicts differences in associated climate niches. European Journal of Plant Pathology, 156(3), 751–766. https://doi.org/10.1007/s10658-019-01926-5
Sun, Y., Wang, M., Li, Y., Gu, Z., Ling, N., Shen, Q., & Guo, S. (2017). Wilted cucumber plants infected by Fusarium oxysporum f. sp. cucumerinum do not suffer from water shortage. Annals of Botany, 120(3), 427–436. https://doi.org/10.1093/aob/mcx065
Takahashi, Y., Matsushita, N., & Hogetsu, T. (2010). Spatial distribution of Raffaelea quercivora in xylem of naturally infested and inoculated oak trees. Phytopathology, 100(8), 747–755. https://doi.org/10.1094/PHYTO-100-8-0747
Torres, M. A., Jones, J. D. G., & Dangl, J. L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiology, 141(2), 373–378. https://doi.org/10.1104/pp.106.079467
Tyree, M. T., & Zimmermann, M. H. (2002). Xylem structure and the ascent of sap (2nd ed.). Springer-Verlag Berlin Heidelberg. https://doi.org/10.1007/978-3-662-04931-0
Watanabe, M., Hoshika, Y., Inada, N., Wang, X., Mao, Q., & Koike, T. (2013). Photosynthetic traits of Siebold’s beech and oak saplings grown under free air ozone exposure in northern Japan. Environmental Pollution, 174, 50–56. https://doi.org/10.1016/j.envpol.2012.11.006
Wiedemuth, K., Müller, J., Kahlau, A., Amme, S., Mock, H.-P., Grzam, A., et al. (2005). Successive maturation and senescence of individual leaves during barley whole plant ontogeny reveals temporal and spatial regulation of photosynthetic function in conjunction with C and N metabolism. Journal of Plant Physiology, 162(11), 1226–1236. https://doi.org/10.1016/j.jplph.2005.01.010
Yamashita, N., Koike, N., & Ishida, A. (2002). Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. Plant, Cell & Environment, 25(10), 1341–1356. https://doi.org/10.1046/j.1365-3040.2002.00907.x
Yazaki, K., Kuroda, K., Nakano, T., Kitao, M., Tobita, H., Ogasa, M. Y., & Ishida, A. (2015). Recovery of physiological traits in saplings of invasive Bischofia tree compared with three species native to the Bonin Islands under successive drought and irrigation cycles. PLoS ONE, 10(8), e0135117. https://doi.org/10.1371/journal.pone.0135117.s001
Yazaki, K., Takanashi, T., Kanzaki, N., Komatsu, M., Levia, D. F., Kabeya, D., et al. (2018). Pine wilt disease causes cavitation around the resin canals and irrecoverable xylem conduit dysfunction. Journal of Experimental Botany, 69(3), 589–602. https://doi.org/10.1093/jxb/erx417
Acknowledgements
We thank Dr Y. Takahashi and Dr M. Komatsu of the Forestry and Forest Products Research Institute for the observation of pathogen hyphae by fluorescence microscopy, Ms. M. Ishikawa for the preparation and propagation of seedlings, and Prof. E. Maruta of Kanagawa University for the measurement of stomatal conductance. We also appreciate the valuable comments given by Dr M. Kitao and Dr H. Tobita of the Forestry and Forest Products Research Institute helped improve the overall quality of this manuscript.
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This work was supported by JSPS KAKENHI grant no. JP16H04948, 21H02241 and 21H02225.
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YK: experimental design, conducting experimental procedures, analysis, and writing the manuscript. FK: conducting physiological measurement, and analysis of root morphologies. ZC: conducting microscopy observations. DL: review of analyses and writing the manuscript. AM: incubating and inoculating pathogens. SS-T and IA: experimental design and measurement of root hydraulic conductance. KM, TY, and SH: measurement of the content of ABA. MY and OY: experimental design. SN: experimental design, incubating and inoculating pathogens, writing the manuscript. YK and FK should be considered joint first authors.
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Kenichi Yazaki and Fuku S. Kimura contributed equally to this study and both are first authors.
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Yazaki, K., Kimura, F.S., Zhang, C. et al. Physiological responses of seedlings to the invasion of brown root rot hyphae differ between semi-deciduous Bischofia javanica Blume and evergreen Rhaphiolepis umbellata (Thunb.) Makino. Eur J Plant Pathol 168, 147–166 (2024). https://doi.org/10.1007/s10658-023-02740-w
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DOI: https://doi.org/10.1007/s10658-023-02740-w