Abstract
The molecular dialog between fungal pathogens and their plant hosts is governed by signals from the plant, secreted pathogen effectors and enzymes, and the plant immune system. There is an increasing awareness that nutritional factors are also central to fungal-plant interactions. Nutritional factors include carbon and nitrogen metabolism, local pH and redox state, and manipulation of host metabolism by secreted pathogen effectors. A diverse combination of approaches from genetics, biochemistry and fungal and plant cell biology addresses these questions, and a workshop whose abstracts accompany this note was held in 2018 to bring these together. Questions were asked about how the lifestyles and nutritional strategies of eukaryotic filamentous phytopathogens are related to the metabolic architectures and pathogenic processes affecting both plant hosts and their pathogens. The aim for future work will be to provide metabolism-based strategies for pathogen control.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrahamian, M., Ah-Fong, A. M. V., Davis, C., et al. (2016). Gene expression and silencing studies in Phytophthora infestans reveal infection-specific nutrient transporters and a role for the nitrate reductase pathway in plant pathogenesis. PLoS Pathogens, 12, e1006097. https://doi.org/10.1371/journal.ppat.1006097.
Ah-Fong, A. M. V., Shrivastava, J., & Judelson, H. S. (2017). Lifestyle, gene gain and loss, and transcriptional remodeling cause divergence in the transcriptomes of Phytophthora infestans and Pythium ultimum during potato tuber colonization. BMC Genomics, 18, 764. https://doi.org/10.1186/s12864-017-4151-2.
Ah-Fong, A. M. V., Kagda, M. S., Abrahamian, M., & Judelson, H. S. (2019). Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution. PLoS Pathogens, 15, e1007729. https://doi.org/10.1371/journal.ppat.1007729.
Anand, G., Waiger, D., Vital, N., Maman, J., Ma, L. J., & Covo, S. (2019). How does Fusarium oxysporum sense and respond to nicotinaldehyde, an inhibitor of the NAD+ salvage biosynthesis pathway? Frontiers in Microbiology, 10, 329. https://doi.org/10.3389/fmicb.2019.00329.
Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V., & Lukyanov, S. (2006). Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nature Methods, 3, 281–286. https://doi.org/10.1038/nmeth866.
Bi, F., Barad, S., Ment, D., Luria, N., Dubey, A., Casado, V., Glam, N., Mínguez, J. D., Espeso, E. A., Fluhr, R., & Prusky, D. (2016). Carbon regulation of environmental pH by secreted small molecules that modulate pathogenicity in phytopathogenic fungi. Molecular Plant Pathology, 17, 1178–1195. https://doi.org/10.1111/mpp.12355.
Chen, L.-Q., Hou, B.-H., Lalonde, S., Takanaga, H., Hartung, M. L., Qu, X. Q., Guo, W. J., Kim, J. G., Underwood, W., Chaudhuri, B., Chermak, D., Antony, G., White, F. F., Somerville, S. C., Mudgett, M. B., & Frommer, W. B. (2010). Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 468, 527–532. https://doi.org/10.1038/nature09606.
Chiang, Y.-M., Ahuja, M., Oakley, C. E., Entwistle, R., Asokan, A., Zutz, C., Wang, C. C., & Oakley, B. R. (2016). Development of genetic dereplication strains in Aspergillus nidulans results in the discovery of aspercryptin. Angewandte Chemie (International Ed. in English), 55, 1662–1665. https://doi.org/10.1002/anie.201507097.
de Assis, L. J., Manfiolli, A., Mattos, E., et al. (2018). Protein kinase a and high-osmolarity glycerol response pathways cooperatively control cell wall carbohydrate mobilization in Aspergillus fumigatus. MBio, 9. https://doi.org/10.1128/mBio.01952-18.
de Bruder Nascimento, A. C. M. O., Dos Reis, T. F., de Castro, P. A., et al. (2016). Mitogen activated protein kinases SakA(HOG1) and MpkC collaborate for Aspergillus fumigatus virulence. Molecular Microbiology, 100, 841–859. https://doi.org/10.1111/mmi.13354.
Dechant, R., Binda, M., Lee, S. S., Pelet, S., Winderickx, J., & Peter, M. (2010). Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. The EMBO Journal, 29, 2515–2526. https://doi.org/10.1038/emboj.2010.138.
Downes, D. J., Davis, M. A., Kreutzberger, S. D., Taig, B. L., & Todd, R. B. (2013). Regulation of the NADP-glutamate dehydrogenase gene gdhA in Aspergillus nidulans by the Zn(II)2Cys6 transcription factor LeuB. Microbiology, 159, 2467–2480. https://doi.org/10.1099/mic.0.071514-0.
Du, Y., Zhang, H., Hong, L., et al. (2013). Acetolactate synthases MoIlv2 and MoIlv6 are required for infection-related morphogenesis in Magnaporthe oryzae. Molecular Plant Pathology, 14, 870–884. https://doi.org/10.1111/mpp.12053.
Dubey, A. K., Barad, S., Luria, N., Kumar, D., Espeso, E. A., & Prusky, D. B. (2016). Cation-stress-responsive transcription factors SltA and CrzA regulate morphogenetic processes and pathogenicity of Colletotrichum gloeosporioides. PLoS One, 11, e0168561. https://doi.org/10.1371/journal.pone.0168561.
Engelsdorf, T., Horst, R. J., Pröls, R., Pröschel, M., Dietz, F., Hückelhoven, R., & Voll, L. M. (2013). Reduced carbohydrate availability enhances the susceptibility of Arabidopsis toward Colletotrichum higginsianum. Plant Physiology, 162, 225–238. https://doi.org/10.1104/pp.112.209676.
Etxebeste, O., & Espeso, E. A. (2019). Aspergillus nidulans in the post-genomic era: A top-model filamentous fungus for the study of signaling and homeostasis mechanisms. International Microbiology, 23, 5–22. https://doi.org/10.1007/s10123-019-00064-6.
Fernandes, T. R., Segorbe, D., Prusky, D., & Di Pietro, A. (2017). How alkalinization drives fungal pathogenicity. PLoS Pathogens, 13, e1006621. https://doi.org/10.1371/journal.ppat.1006621.
Fernandez, J., Marroquin-Guzman, M., Nandakumar, R., Shijo, S., Cornwell, K. M., Li, G., & Wilson, R. A. (2014a). Plant defence suppression is mediated by a fungal sirtuin during rice infection by Magnaporthe oryzae. Molecular Microbiology, 94, 70–88. https://doi.org/10.1111/mmi.12743.
Fernandez, J., Marroquin-Guzman, M., & Wilson, R. A. (2014b). Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae. PLoS Pathogens, 10, e1004354. https://doi.org/10.1371/journal.ppat.1004354.
Fernandez, J., Marroquin-Guzman, M., & Wilson, R. A. (2014c). Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annual Review of Phytopathology, 52, 155–174.
Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S., & Gurr, S. J. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186–194. https://doi.org/10.1038/nature10947.
Fotopoulos, V., Gilbert, M. J., Pittman, J. K., Marvier, A. C., Buchanan, A. J., Sauer, N., Hall, J. L., & Williams, L. E. (2003). The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiology, 132, 821–829. https://doi.org/10.1104/pp.103.021428.
Gebauer, P., Korn, M., Engelsdorf, T., Sonnewald, U., Koch, C., & Voll, L. M. (2017). Sugar accumulation in leaves of Arabidopsis sweet11/sweet12 double mutants enhances priming of the salicylic acid-mediated defense response. Frontiers in Plant Science, 8, 1378. https://doi.org/10.3389/fpls.2017.01378.
Gerstenmaier, L., Pilla, R., Herrmann, L., Herrmann, H., Prado, M., Villafano, G. J., Kolonko, M., Reimer, R., Soldati, T., King, J. S., & Hagedorn, M. (2015). The autophagic machinery ensures nonlytic transmission of mycobacteria. Proceedings of the National Academy of Sciences, 112, E687–E692. https://doi.org/10.1073/pnas.1423318112.
Giraldo, M. C., Dagdas, Y. F., Gupta, Y. K., Mentlak, T. A., Yi, M., Martinez-Rocha, A. L., Saitoh, H., Terauchi, R., Talbot, N. J., & Valent, B. (2013). Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nature Communications, 4, 1996. https://doi.org/10.1038/ncomms2996.
Henke, M. T., Soukup, A. A., Goering, A. W., McClure, R., Thomson, R. J., Keller, N. P., & Kelleher, N. L. (2016). New Aspercryptins, lipopeptide natural products, revealed by HDAC inhibition in Aspergillus nidulans. ACS Chemical Biology, 11, 2117–2123. https://doi.org/10.1021/acschembio.6b00398.
Hou, R., Jiang, C., Zheng, Q., Wang, C., & Xu, J. R. (2015). The AreA transcription factor mediates the regulation of deoxynivalenol (DON) synthesis by ammonium and cyclic adenosine monophosphate (cAMP) signalling in Fusarium graminearum. Molecular Plant Pathology, 16, 987–999. https://doi.org/10.1111/mpp.12254.
Huang, K., Caplan, J., Sweigard, J. A., Czymmek, K. J., & Donofrio, N. M. (2017). Optimization of the HyPer sensor for robust real-time detection of hydrogen peroxide in the rice blast fungus. Molecular Plant Pathology, 18, 298–307. https://doi.org/10.1111/mpp.12392.
Hughes, A. L. & Gottschling, D. E. (2012) An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature, 492, 261.
Judelson, H., & Ah-Fong, A. M. V. (2018). Exchanges at the plant-oomycete interface that influence disease. Plant Physiology, 2018, 00979. https://doi.org/10.1104/pp.18.00979.
Kane PM (2016) Proton transport and pH control in fungi. In: Advances in experimental medicine and biology. pp 33–68.
H. Kato, R. Mayama, R. Sekine AU (1994) Microconidium formation in Magnaporthe grisea. Ann Phytopath Soc Japan 60:175–185.
Lanver, D., Müller, A. N., Happel, P., Schweizer, G., Haas, F. B., Franitza, M., Pellegrin, C., Reissmann, S., Altmüller, J., Rensing, S. A., & Kahmann, R. (2018). The biotrophic development of Ustilago maydis studied by RNA-Seq analysis. Plant Cell, 30, 300–323. https://doi.org/10.1105/tpc.17.00764.
Leite, B., & Nicholson, R. L. (1992). Mycosporine-alanine: A self-inhibitor of germination from the conidial mucilage of Colletotrichum graminicola. Experimental Mycology, 16, 76–86. https://doi.org/10.1016/0147-5975(92)90043-Q.
Liu, X., Han, Q., Xu, J., Wang, J., & Shi, J. (2015). Acetohydroxyacid synthase FgIlv2 and FgIlv6 are involved in BCAA biosynthesis, mycelial and conidial morphogenesis, and full virulence in Fusarium graminearum. Scientific Reports, 5, 16315. https://doi.org/10.1038/srep16315.
Ma, L.-J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M. J., di Pietro, A., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Houterman, P. M., Kang, S., Shim, W. B., Woloshuk, C., Xie, X., Xu, J. R., Antoniw, J., Baker, S. E., Bluhm, B. H., Breakspear, A., Brown, D. W., Butchko, R. A., Chapman, S., Coulson, R., Coutinho, P. M., Danchin, E. G., Diener, A., Gale, L. R., Gardiner, D. M., Goff, S., Hammond-Kosack, K. E., Hilburn, K., Hua-van, A., Jonkers, W., Kazan, K., Kodira, C. D., Koehrsen, M., Kumar, L., Lee, Y. H., Li, L., Manners, J. M., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S. Y., Proctor, R. H., Regev, A., Ruiz-Roldan, M. C., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D. C., Turgeon, B. G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C. A., Kistler, H. C., & Rep, M. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature, 464, 367–373. https://doi.org/10.1038/nature08850.
Maheshwari, R. (1999). Microconidia of Neurospora crassa. Fungal Genetics and Biology, 26, 1–18.
Maor, U., Sadhasivam, S., Zakin, V., et al. (2017). The effect of ambient pH modulation on ochratoxin a accumulation by Aspergillus carbonarius. World Mycotoxin Journal, 10, 339–348. https://doi.org/10.3920/WMJ2017.2200.
Marroquin-Guzman, M., & Wilson, R. A. (2015). GATA-dependent glutaminolysis drives appressorium formation in Magnaporthe oryzae by suppressing TOR inhibition of cAMP/PKA signaling. PLoS Pathogens, 11, e1004851. https://doi.org/10.1371/journal.ppat.1004851.
Marroquin-Guzman, M., Hartline, D., Wright, J. D., Elowsky, C., Bourret, T. J., & Wilson, R. A. (2017a). The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease. Nature Microbiology, 2, 17054–17010. https://doi.org/10.1038/nmicrobiol.2017.54.
Marroquin-Guzman, M., Sun, G., & Wilson, R. A. (2017b). Glucose-ABL1-TOR signaling modulates cell cycle tuning to control terminal appressorial cell differentiation. PLoS Genetics, 13, e1006557. https://doi.org/10.1371/journal.pgen.1006557.
Masachis, S., Segorbe, D., Turrà, D., Leon-Ruiz, M., Fürst, U., el Ghalid, M., Leonard, G., López-Berges, M. S., Richards, T. A., Felix, G., & di Pietro, A. (2016). A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nature Microbiology, 1, 16043. https://doi.org/10.1038/nmicrobiol.2016.43.
Mellado, L., Arst, H. N., & Espeso, E. A. (2016). Proteolytic activation of both components of the cation stress–responsive Slt pathway in Aspergillus nidulans. Molecular Biology of the Cell, 27, 2598–2612. https://doi.org/10.1091/mbc.e16-01-0049.
Niño-Sánchez, J., Casado-Del Castillo, V., Tello, V., et al. (2016). The FTF gene family regulates virulence and expression of SIX effectors in Fusarium oxysporum. Molecular Plant Pathology, 17, 1124–1139. https://doi.org/10.1111/mpp.12373.
Nordzieke, D. E., Sanken, A., Antelo, L., Raschke, A., Deising, H. B., & Pöggeler, S. (2019). Specialized infection strategies of falcate and oval conidia of Colletotrichum graminicola. Fungal Genetics and Biology, 133, 103276. https://doi.org/10.1016/j.fgb.2019.103276.
Panaccione, D. G., Vaillancourt, L. J., & Hanau, R. M. (1989). Conidial Dimorphism in Colletotrichum graminicola. Mycologia, 81, 876. https://doi.org/10.2307/3760106.
Patkar, R. N., Ramos-Pamplona, M., Gupta, A. P., Fan, Y., & Naqvi, N. I. (2012). Mitochondrial β-oxidation regulates organellar integrity and is necessary for conidial germination and invasive growth in Magnaporthe oryzae. Molecular Microbiology, 86, 1345–1363. https://doi.org/10.1111/mmi.12060.
Peñalva, M. A., Tilburn, J., Bignell, E., & Arst, H. N. (2008). Ambient pH gene regulation in fungi: Making connections. Trends in Microbiology, 16, 291–300. https://doi.org/10.1016/j.tim.2008.03.006.
Prusky, D. B., & Wilson, R. A. (2018). Does increased nutritional carbon availability in fruit and foliar hosts contribute to modulation of pathogen colonization? Postharvest Biology and Technology, 145, 27–32.
Prusky, D., Alkan, N., Mengiste, T., & Fluhr, R. (2013). Quiescent and necrotrophic lifestyle choice during postharvest disease development. Annual Review of Phytopathology, 51, 155–176. https://doi.org/10.1146/annurev-phyto-082712-102349.
Reshkin, S. J., Greco, M. R., & Cardone, R. A. (2014). Role of pHi, and proton transporters in oncogene-driven neoplastic transformation. Philos Trans R Soc B Biol Sci, 369, 20130100–20130100. https://doi.org/10.1098/rstb.2013.0100.
Sakulkoo, W., Osés-Ruiz, M., Oliveira Garcia, E., et al. (2018). A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science (80- ) 359:1399–1403. https://doi.org/10.1126/science.aaq0892.
Segal, L. M., & Wilson, R. A. (2018). Reactive oxygen species metabolism and plant-fungal interactions. Fungal Genetics and Biology, 110, 1–9. https://doi.org/10.1016/j.fgb.2017.12.003.
Soriani, F. M., Malavazi, I., da Silva Ferreira, M. E., Savoldi, M., von Zeska Kress, M., de Souza Goldman, M. H., Loss, O., Bignell, E., & Goldman, G. H. (2008). Functional characterization of the Aspergillus fumigatus CRZ1 homologue, CrzA. Molecular Microbiology, 67, 1274–1291. https://doi.org/10.1111/j.1365-2958.2008.06122.x.
Spielvogel, A., Findon, H., Arst, H. N., Araújo-Bazán, L., Hernández-Ortíz, P., Stahl, U., Meyer, V., & Espeso, E. A. (2008). Two zinc finger transcription factors, CrzA and SltA, are involved in cation homoeostasis and detoxification in Aspergillus nidulans. The Biochemical Journal, 414, 419–429. https://doi.org/10.1042/BJ20080344.
Sukno, S. A., García, V. M., Shaw, B. D., & Thon, M. R. (2008). Root infection and systemic colonization of maize by Colletotrichum graminicola. Applied and Environmental Microbiology, 74, 823–832. https://doi.org/10.1128/AEM.01165-07.
Sun, G., Elowsky, C., Li, G., & Wilson, R. A. (2018). TOR-autophagy branch signaling via Imp1 dictates plant-microbe biotrophic interface longevity. PLoS Genetics, 14, e1007814. https://doi.org/10.1371/journal.pgen.1007814.
Sun G, Qi X, Wilson RA (2019) A feed-forward subnetwork emerging from integrated TOR- and cAMP/PKA-signaling architecture reinforces Magnaporthe oryzae appressorium morphogenesis. Mol plant microbe interact MPMI-10-18-0287-R. doi: https://doi.org/10.1094/MPMI-10-18-0287-R.
Sutton, P. N., Henry, M. J., & Hall, J. L. (1999). Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta, 208, 426–430. https://doi.org/10.1007/s004250050578.
Turrà, D., Segorbe, D., & Di Pietro, A. (2014). Protein kinases in plant-pathogenic fungi: Conserved regulators of infection. Annual Review of Phytopathology, 52, 267–288. https://doi.org/10.1146/annurev-phyto-102313-050143.
Vlaardingerbroek, I., Beerens, B., Schmidt, S. M., Cornelissen, B. J., & Rep, M. (2016). Dispensable chromosomes in Fusarium oxysporum f. sp. lycopersici. Molecular Plant Pathology, 17, 1455–1466. https://doi.org/10.1111/mpp.12440.
Vylkova, S. (2017). Environmental pH modulation by pathogenic fungi as a strategy to conquer the host. PLoS Pathogens, 13, e1006149. https://doi.org/10.1371/journal.ppat.1006149.
Wilson, R. A., & Talbot, N. J. (2009). Under pressure: Investigating the biology of plant infection by Magnaporthe oryzae. Nature Reviews. Microbiology, 7, 185–195. https://doi.org/10.1038/nrmicro2032.
Wilson, R. A., Jenkinson, J. M., Gibson, R. P., Littlechild, J. A., Wang, Z.-Y., & Talbot, N. J. (2007). Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. The EMBO Journal, 26, 3673–3685.
Wilson, R. A., Gibson, R. P., Quispe, C. F., Littlechild, J. A., & Talbot, N. J. (2010). An NADPH-dependent switch regulates plant infection by the rice blast fungus. Proceedings of the National Academy of Sciences of the United States of America, 21902. https://doi.org/10.1073/pnas.1006839107.
Zhang, H., Wu, Z., Wang, C., Li, Y., & Xu, J. R. (2014). Germination and infectivity of microconidia in the rice blast fungus Magnaporthe oryzae. Nature Communications, 5, 4518. https://doi.org/10.1038/ncomms5518.
Acknowledgements
We thank the US-Israel Binational Agricultural Research and Development Fund (BARD) for funding the workshop (number W-104-17).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
the author order is alphabetical, except for workshop co-chairs D.P., B.A.H. and R.A.W.
Electronic supplementary material
ESM 1
(MPG 49388 kb)
Rights and permissions
About this article
Cite this article
Prusky, D., de Assis, L.J., Baroncelli, R. et al. Nutritional factors modulating plant and fruit susceptibility to pathogens: BARD workshop, Haifa, Israel, February 25–26, 2018. Phytoparasitica 48, 317–333 (2020). https://doi.org/10.1007/s12600-020-00803-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12600-020-00803-w