Abstract
Biotrophic fungi are one group of heterogeneous organisms and these fungi differ in their traits like mode of nutrition, types of reproduction, and dispersal systems. Generally, based on the nutritional mode, fungi are classified into three broad categories, viz. biotrophs, necrotrophs, and hemi-biotrophs. Biotrophs derive their nutrients and energy from living plant cells and survive within the interstitial space of the cells. Biotrophic fungi cause serious crop diseases but are highly challenging to investigate and develop a treatment strategy. Blumeria (Erysiphe) graminis, Uromyces fabae, Ustilago maydis, Cladosporium fulvum, Puccinia graminis, and Phytophthora infestans are some of the significant biotrophic fungi that affect mainly plants. One among the biotrophic fungus, Pneumocystis jirovecii (Taphrinomycotina subphylum of the Ascomycota) exclusively a human pathogen, can cause lung diseases such as “pneumocystis.” Biotrophic fungus widely parasitizing Solanaceae family crops (Tomato and potato) has done massive damage to the crops and has led to economic impact worldwide. During infection and for nutrient absorption, biotrophs develops external appendages such as appressoria or haustoria. The hyphae or appressorium adheres to the plant cell wall and collapses the layers for their nutrient absorption. The pathogen also secretes effector molecules to escape from the plant defense mechanism. Later, plants activate their primary and secondary defense mechanisms; however, the pathogen induces virulence genes to escape the host immune responses. Obligate biotrophic fungi pathogenicity has not been fully understood at the molecular level because of the complex interaction, recognition, and signaling with the host. This review summarizes the mechanism of infection in the host, and immune response to emphasize the understanding of the biotrophic fungal biology and pathogenesis in crops. Thus, the detailed review will pave the way to design methods to overcome the resistance of biotrophic fungi and develop disease-free crops.
Similar content being viewed by others
Data Availability
Not applicable.
Abbreviations
- RNAi:
-
RNA interference
- ADK:
-
adenosine kinases
- APM:
-
adaptive penetration mediated
- PCD:
-
programmed cell death
- PAMPs:
-
pathogen-associated molecular patterns
- ROS:
-
reactive oxygen species
- Cf-Avr4:
-
chitin-binding lectins
- HIGS:
-
host-induced gene silencing
- VIGS:
-
virus-induced gene silencing
- NMR:
-
nuclear magnetic resonance
- AVR50:
-
avirulent 50
- Sr35, Sr50:
-
stem rust resistance genes
- PTI:
-
PAMP-triggered immunity
- ETI:
-
Effector- triggered immunity
- NBS-LRRs:
-
nucleotide-binding site leucine-rich repeats
References
Pandey, P., Irulappan, V., Bagavathiannan, M. V., & Senthil-Kumar, M. (2017). Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Frontiers in Plant Science, 8, 537. https://doi.org/10.3389/fpls.2017.00537
Tel-Aviv University (2012). Manual. Department of Molecular Biology and Ecology of Plants, p. 298.
Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, A., Soanes, D. M., Stüber, K., Themaat, E. V. L. V., Brown, J. K. M., Butcher, S. A., Gurr, S. J., Lebrun, M. H., Ridout, C. J., Lefert, P. S., Talbot, N. J., Ahmadinejad, N., Ametz, C., Barton, G. R., Benjdia, M., Bidzinski, P., Bindschedler, L. V., Both, M., Brewer, M. T., Davidson, L. C., Davidson, M. M. C., Collemare, J., Cramer, R., Frenkel, O., Godfrey, O., Harriman, J., Hoede, C., King, B. C., Klages, S., Kleemann, J., Knoll, D., Koti, P. S., Kreplak, J., López-Ruiz, F. J., Lu, X., Maekawa, T., Mahanil, S., Micali, C., Milgroom, M. G., Montana, G., Noir, S., O’Connell, R. J., Oberhaensli, S., Parlange, F., Pedersen, C., Quesneville, H., Reinhardt, R., Rott, M., Sacristán, S., Schmidt, S. M., Schön, M., Skamnioti, P., Sommer, H., Stephens, A., Takahara, H., Christensen, H. T., Vigouroux, M., WeBling, R., Wicker, T., & Panstruga, R. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science, 330, 1543–1545.
Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ashraf, M., Ahmed, N., & Zhang, L. (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Frontiers in Plant Science, 10, 1068. https://doi.org/10.3389/fpls.2019.01068
Kemen, E., & Jones, J. D. G. (2012). Obligate biotroph parasitism: Can we link genomes to life-styles? Trends in Plant Science, 17, 448–457.
Mendgen, K., & Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends in Plant Science, 7, 352–356.
Oliver, R. P., & Ipcho, S. V. S. (2004). Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology, 5, 347–352.
Divon, H. H., & Fluhr, R. (2006). Nutrition acquisition strategies during fungal infection of plants. Federation of European Microbiological Societies, Blackwell Publishing Ltd.
de Wit, P. J. G. M. (2007). Visions and reflections. How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences, 64, 2726–2732.
Delaye, L., Guzmán, G. G., & Heil, M. (2013). Endophytes versus biotrophic and necrotrophic pathogens are fungal life-styles evolutionarily stable traits? Fungal Diversity, 60, 125–135.
Pandey, D., Rajendran, S. R. C. K., Sajeesh, M. G. P. K., & Kumar, A. (2016). Plant defense signaling and responses against necrotrophic fungal pathogens. Journal of Plant Growth Regulation, 35, 1–16.
Laluk, K., & Mengiste, T. (2010). Necrotroph attacks on plants: Wanton destruction or covert extortion? Arabidopsis Book, 8, e0136.
Schulze-Lefert, P., & Panstruga, R. (2003). Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annual Review of Phytopathology, 41, 641–667.
Green, J. R., Pain, N. A., Cannell, M. E., Jones, G. L., Leckie, C. L., McCready, S., Endgen, K., Mitchell, A. J., Callow, J. A., & O’Connell, R. J. (1995). Analysis of differentiation and development of the specialised infection structures formed by biotrophic fungal plantpathogens using monoclonal antibodies. Canadian Journal of Botany, 73(Suppl.), S408–S417.
Heath, M. C., & Skalamera, D. (1997). Cellular interactions between plants and biotrophic fungal parasites. Advances in Botanical Research, 24, 196–225.
Agrios, G. N. (2005). Plant Pathology (5th ed.). Elsevier Academic Press.
Hann, D. R., Gimenez-Ibanez, S., & Rathjen, J. P. (2010). Bacterial virulence effectors and their activities. Current Opinion in Plant Biology, 13, 388–393.
Staskawicz, B. J., Mudgett, M. B., Dangl, J. L., & Galan, J. E. (2001). Common and contrasting themes of plant and animal diseases. Science, 292, 2285–2289.
Oliver, R. P., Henricot, B., & Segers, G. (2000). Cladosporium fulvum, cause of leaf mould of tomato. In J. W. Kronstad (Ed.), Fungal Pathogen (pp. 65–92). Kluwer.
Both, M., Csukai, M., Stumpf, M. P. H., & Spanu, P. D. (2005). Gene expression profiles of B. graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. The Plant Cell, 17, 2107–2122.
Gao, F. K., Dai, C. C., & Liu, X. Z. (2010). Mechanism of fungal endophytes in plant protection against pathogens. African Journal of Microbiology Research, 4, 1346–1351.
Parniske, M. (2000). Intracellular accommodation of microbes by plants: A common developmental program for symbiosis and disease? Current Opinion in Plant Biology, 3, 320–328.
Meadows, R. (2011). Why biotrophs can’t live alone. PLOS Pathogens, 9, 1–2.
Kabbage, M., Yarden, O., & Dickman, M. B. (2015). Pathogenic attributes of Sclerotinia sclerotiorum: Switching from a biotrophic to necrotrophic lifestyle. Plant Science, 233, 53–60.
de Wit, P. J. G. M., Burgt, A. V. D., Kmen, B. O., Stergiopoulos, I., Abd-Elsalam, K., Aert, A. L., Bahkali, A. H., Beenen, H. G., Chettri, P., Cox, M. P., Datema, E., de Vries, R., Dhillon, B., Ganley, A. R., Griffiths, S. A., Guo, Y., Hamelin, R. C., Henrissat, B., Kabir, M. S., Jashni, M. K., Kema, G., Klaubauf, S., Lapidus, A., Levasseur, A., Lindquist, E., Mehrabi, R., Ohm, R. A., Owen, T. J., Salamov, A., Schwelm, A., Schijlen, E., Sun, H., Burg, H. A. V. D., van Ham, R. C. H. J., Zhang, S., Goodwin, S. B., Grigoriev, I. V., Collemare, J., & Bradshaw, R.E. (2012). The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and life-styles but also signatures of common ancestry. PLOS Genetics, 8, 1–22.
Latijnhouwers, M., de Wit, P. J. G. M., & Govers, F. (2003). Oomycetes and fungi: Similar weaponry to attack plants. Trends in Microbiology, 11, 462–469.
Horbach, R., Quesada, A. R. N., Knogge, W., & Deising, H. B. (2011). When and how to kill a plant cell: Infection strategies of plant pathogenic fungi. Journal of Plant Physiology, 168, 51–62.
Ding, Y., Chen, Y., Yan, B., Liao, H., Dong, M., Meng, X., Wan, H., & Qian, W. (2021). Host-induced gene silencing of a multifunction gene Sscnd1enhances plant resistance against Sclerotinia sclerotiorum. Frontiers in Microbiology, 12, 693334. https://doi.org/10.3389/fmicb.2021.693334
Guzman, G. G., & Heil, M. (2014). Life histories of hosts and pathogens predict patterns in tropical fungal plant diseases. New Phytologist, 201, 1106–1120.
Petriacq, P., Stassen, J. H. M., & Ton, J. (2016). Spore density determines infection strategy by the plant pathogenic fungus Plectosphaerella cucumerina. Plant Physiology, American Society of Plant Biologists.
Dickman, M. B., & de Figueiredo, P. (2011). Comparative pathobiology of fungal pathogens of plants and animals. PLOS Pathogens, 7, 177–184.
Koeck, M., Hardham, A. R., & Dodds, P. N. (2011). The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiology, 13, 1849–1857.
Heath, M. C. (1997). Signaling between pathogenic rust fungi and resistant or susceptible host plants. Annals of Botany, 80, 713–720.
Govrin, E. M., & Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology, 10, 751–757.
Gueddari, N. E. E., Rauchhaus, U., Moerschbacher, B. M., & Deising, H. (2002). Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytologist, 156, 103–112.
Munch, S., Lingner, U., Floss, D. S., Ludwig, N., Sauer, N., & Deising, H. B. (2008). The hemibiotrophic life-style of Colletotrichum species. Journal of Plant Physiology, 165, 41–51.
Kämper, J., Kahmann, R., Bölker, M., Ma, L. J., Brefort, T., Saville, B. J., Banuett, F., Kronstad, J. W., Gold, S. E., & Müller, O. (2006). Insights from the genome of the bio-trophic fungal plant pathogen Ustilago maydis. Nature, 444, 97.
Djamei, A., Schipper, K., Rabe, F., Ghosh, A., Vincon, V., et al. (2011). Metabolic priming by a secreted fungal effector. Nature, 478, 395–398.
Penninckx, I. A. M. A., Thomma, B. P. H. J., Buchala, A., Métraux, J. P., & Broekaert, W. F. (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell, 10, 2103–2113.
Idnurm, A., & Howlett, B. J. (2001). Pathogenicity genes of phytopathogenic fungi. Molecular Plant Pathology, 2, 241–255.
Triplett, L. R., Shidore, T., Long, J., Miao, J., Wu, S., et al. (2016). AvrRxo1 is a bifunctional type III secreted effector and toxin-antitoxin system component with homologs in diverse environmental contexts. PLoS One1, 11, e0158856.
Bari, R., & Jones, J. D. (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology, 69, 473–488.
Atkinson, M. M., Midland, S. L., Sims, J. J., & Keen, N. T. (1996). Syringolide 1 triggers Ca2+influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiology, 112, 297–302.
Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology, 44, 41–60.
Nemri, A., Saunders, D. G. O., Anderson, C., Upadhyaya, N. M., Win, J., Lawrence, G., Jones, D., Kamoun, S., Ellis, J., & Dodds, P. (2014). The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Frontiers in Plant Science, 5, 98.
Sonah, H., Deshmukh, R. K., & Bélanger, R. R. (2016). Computational prediction of effector proteins in fungi: Opportunities and challenges. Frontiers in Plant Science, 7.
Sharpee, W. C., & Dean, R. A. (2016). Form and function of fungal and oomycete effectors. Fungal Biology Reviews.
Torres, M. A., Jones, J. D. G., & Dangl, J. L. (2006). Reactive oxygen species signaling in re-sponse to pathogens. Plant Physiology, 141, 373–378.
Stergiopoulos, I., & de Wit, P. J. G. M. (2009). Fungal effector proteins. Annual Review of Phytopathology, 47, 233–263.
Haueisen, J., Moeller, M., Eschenbrenner, C. J., Grandaubert, J., Seybold, H., & Adamiak, H. (2017). Extremely flexible infection programs in a fungal plant pathogen (p. 229997). bioRxiv
Xu, Q., Tang, C., Wang, L., Zhao, C., Kang, Z., & Wang, X. (2020). Haustoria – arsenals during the interaction between wheat and Puccinia striiformis f. sp. tritici. Molecular Plant Pathology, 21, 83–94.
Misas Villamil, J. C., Mueller, A. N., Demir, F., Meyer, U., Ökmen, B., Schulze Hüynck, J., Breuer, M., Dauben, H., Win, J., Huesgen, P. F., & Doehlemann, G. (2019). A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif. Nature Communications, 10, 1576.
Nirmala, J., Drader, T., Lawrence, P. K., Yin, C., Hulbert, S., Steber, C. M., Steffenson, B. J., Szabo, L. J., Von Wettstein, D., Kleinhofs, A., Concerted action of two avirulent spore effectors activates Reaction to P. graminis 1 (Rpg1)-mediated cereal stem rust resistance. Proceedings of the National Academy of Sciences, 108, 14676–14681.
Tonukari, N. J., Scott-Craig, J. S., Walton, J. D. (2000). The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence in maize. Plant Cell, 12, 237–247
Rogers, L. M., Kim, Y. K., Guo, W., González-Candelas, L., Li, D., Kolattukudy, P. E. (2000) Requirement for either a host- or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proceedings of the National Academy of Sciences of the United States of America, 97, 9813–9818.
Jaswal, R., Kiran, K., Rajarammohan, S., Dubey, H., Singh, P. K., Sharma, Y., Deshmukh, R., Sonah, H., Gupta, N., Sharma, T. R., Ahmed, H., Howton, T. C., Sun, Y., Weinberger, N., Belkhadir, Y., Mukhtar, M. S., Mascia, T., Nigro, F., Abdallah, A., Ferrara, M., De Stradis, A., Faedda, R., Palukaitis, P., Gallitelli, D., Hussain, H. A., Khaliq, S., Ashraf, A., Anjum, U., Men, S. A., S., & Wang, L. (2011). (2020). Effector Biology of Biotrophic Plant Fungal Pathogens: Current Advances and Future Prospects. Microbiological Research, 241, 126567.
Pennington, H. G., Jones, R., Kwon, S., Bonciani, G., Thieron, H., Chandler, T., Luong, P., Morgan, S. N., Przydacz, M., Bozkurt, T., Bowden, S., Craze, M., Wallington, E. J., Garnett, J., Kwaaitaal, M., Panstruga, R., Cota, E., & Spanu, P. D. (2019). The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathogens, 15(3), e1007620.
Ahmed, H., Howton, T. C., Sun, Y., Weinberger, N., Belkhadir, Y., & Mukhtar, M. S. (2018). Network biology discovers pathogen contact points in host protein-protein interactomes. Nature Communications, 9(1), 2312.
Hu, Y., Liang, Y., Zhang, M., Tan, F., Zhong, S., Li, X., Gong, G., Chang, X., Shang, J., Tang, S., Li, T., & Luo, P. (2018). Comparative transcriptome profiling of Blumeria graminis f. sp. tritici during compatible and incompatible interactions with sister wheat lines carrying and lacking Pm40. PLoS One, 13(7), e0198891.
Mascia, T., Nigro, F., Abdallah, A., Ferrara, M., De Stradis, A., Faedda, R., Palukaitis, P., & Gallitelli, D. (2014). Gene silencing and gene expression in phytopathogenic fungi using a plant virus vector. Proceedings of the National Academy of Sciences of the United States of America, 111(11), 4291–4296.
Salcedo, A., Rutter, W., Wang, S., Akhunova, A., Bolus, S., Chao, S., Anderson, N., De Soto, M. F., Rouse, M., Szabo, L., Bowden, R. L., Dubcovsky, J., & Akhunov, E. (2017). Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science (New York, N.Y.), 358(6370), 1604–1606.
Hussain, H. A., Hussain, S., Khaliq, S., Ashraf, A., Anjum, U., Men, S. A., S., & Wang, L. (2018). Chilling and Drought Stresses in Crop Plants: Implications, Cross Talk, and Potential Management Opportunities. Frontiers in Plant Science, 9, 393.
Singla, J., & Krattinger, S. G. (2016). Biotic stress resistance genes in wheat Wrigley C., Corke H., Seetharaman K., Faubion J. (Eds.), Encyclopedia of Food Grains (vol. 2, pp. 388–392).
Babak, M, Amin, M, & Yoshihiro, I (2019). Chap. 19 - Physiological Responses to Stress, Postharvest Physiology and Biochemistry of Fruits and Vegetables (405–423). Woodhead Publishing.
A. Z., & Bluhm, B. H. (2017). The genome sequence of Bipolaris cookei reveals mechanisms of pathogenesis underlying target leaf spot of sorghum. Scientific Reports, 7(1), 17217.
Mendgen, K., Hahn, M., & Deising, H. (1996). Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annual Review of Phytopathology, 34, 367–386.
Maffi, D., Iriti, M., Pigni, M., Vannini, C., & Faoro, F. (2011). Uromyces appendiculatus infection in BTH-treated bean plants: ultrastructural details of a lost fight. Mycopathologia, 171(3), 209–221.
Mims, C. W., & Vaillancourt, L. J. (2002). Ultrastructural Characterization of Infection and Colonization of Maize Leaves by Colletotrichum graminicola, and by a C. graminicola Pathogenicity Mutant. Phytopathology, 92(7), 803–812.
Gebremichael, D. E., Haile, Z. M., Negrini, F., Sabbadini, S., Capriotti, L., Mezzetti, B., & Baraldi, E. (2021). RNA Interference Strategies for Future Management of Plant Pathogenic Fungi: Prospects and Challenges. Plants (Basel, Switzerland), 10(4), 650.
Author information
Authors and Affiliations
Contributions
All authors contributed equally.
Corresponding author
Ethics declarations
Ethical Approval
Not applicable.
Consent to Participate
All authors has their consent to participate.
Consent to Publish
All authors has their consent to publish their work.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fei, W., Liu, Y. Biotrophic Fungal Pathogens: a Critical Overview. Appl Biochem Biotechnol 195, 1–16 (2023). https://doi.org/10.1007/s12010-022-04087-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-022-04087-0