Endophytic Microorganisms as an Alternative for the Biocontrol of <i>Phytophthora</i> spp.

  1. José Bolivar-Anillo, Hernando
  2. E. González-Rodríguez, Victoria
  3. Reyes Almeida, Giovanna
  4. Izquierdo-Bueno, Inmaculada
  5. Moraga, Javier
  6. Carbú, María
  7. M. Cantoral, Jesús
  8. Garrido, Carlos
Libro:
Agro-Economic Risks of Phytophthora and an Effective Biocontrol Approach

Editorial: Intech Open

ISBN: 978-1-83969-654-1

Año de publicación: 2021

Tipo: Capítulo de Libro

DOI: 10.5772/INTECHOPEN.99696 GOOGLE SCHOLAR lock_openAcceso abierto editor

Objetivos de desarrollo sostenible

Resumen

The genus Phytophthora with more than 100 described species and 58 officially recognized, phylogenetically distributed in ten clades, are important pathogenic oomycete chromists that cause important diseases in agricultural crops, trees and forests worldwide. This genus is known as \"The Plant Destroyer” which causes great economic losses with costs between 2 and 7 billion dollars per year in agricultural systems and unquantifiable losses in natural ecosystems. The host plants of the genus Phytophthora can vary from a wide range in some species to only one host, however, the host plants of the new species are still being determined and therefore the range continues to expand, that makes control exceedingly difficult. Plant damage can range from alterations in roots, fruits, trunks, stems, foliage and crown to invasive processes in highly susceptible species. Considering the wide range of hosts and organs that can be affected by Phytophthora, the use of endophytic microorganisms for the biocontrol of this phytopathogen can be an alternative to avoid losses of both crops and forests worldwide. Endophytes are microorganisms that live inside plant tissues without causing disease under any circumstances. The fact that endophytic microorganisms are able to colonize an ecological niche similar to that of some plant pathogens qualifies them as potential biocontrol agents. This chapter describes the endophytic bacteria and fungi isolated from different plant species that have shown antagonistic activity against different species of Phytophthora, as well as the metabolites isolated from these microorganisms that have shown fungicide activity and other biocontrol strategies (enzyme production, siderophores, substrate competition, among others) against Phytophthora.

Referencias bibliográficas

  • Wang, T.; Gao, C.; Cheng, Y.; Li, Z.; Chen, J.; Guo, L.; Xu, J. Molecular diagnostics and detection of oomycetes on fiber crops. Plants2020, 9, 1-22, doi:10.3390/plants9060769.
  • Syed Ab Rahman, S.F.; Singh, E.; Pieterse, C.M.J.; Schenk, P.M. Emerging microbial biocontrol strategies for plant pathogens. Plant Sci.2018, 267, 102-111, doi:10.1016/j.plantsci.2017.11.012.
  • Covo, S. Genomic instability in fungal plant pathogens. Genes (Basel).2020, 11, doi:10.3390/genes11040421.
  • Corredor-Moreno, P.; Saunders, D.G.O. Expecting the unexpected: factors influencing the emergence of fungal and oomycete plant pathogens. New Phytol.2020, 225, 118-125, doi:10.1111/nph.16007.
  • Fones, H.N.; Bebber, D.P.; Chaloner, T.M.; Kay, W.T.; Steinberg, G.; Gurr, S.J. Threats to global food security from emerging fungal and oomycete crop pathogens. Nat. Food2020, 1, 332-342, doi:10.1038/s43016-020-0075-0.
  • Pandaranayaka, E.P.J.; Frenkel, O.; Elad, Y.; Prusky, D.; Harel, A. Network analysis exposes core functions in major lifestyles of fungal and oomycete plant pathogens. BMC Genomics2019, 20, 1-15, doi:10.1186/s12864-019-6409-3.
  • Roy, S.G.; Grünwald, N.J. The plant destroyer genus Phytophthora in the 21st century. Rev. Plant Pathol.2014, 6, 387-412.
  • Kroon, L.P.N.M.; Brouwer, H.; De Cock, A.W.A.M.; Govers, F. The genus Phytophthora anno 2012. Phytopathology2012, 102, 348-364, doi:10.1094/PHYTO-01-11-0025.
  • Gao, R.F.; Wang, J.Y.; Liu, K.W.; Yoshida, K.; Hsiao, Y.Y.; Shi, Y.X.; Tsai, K.C.; Chen, Y.Y.; Mitsuda, N.; Liang, C.K.; et al. Comparative analysis of Phytophthora genomes reveals oomycete pathogenesis in crops. Heliyon2021, 7, e06317, doi:10.1016/j.heliyon.2021.e06317.
  • de Andrade Lourenço, D.; Branco, I.; Choupina, A. Phytopathogenic oomycetes: a review focusing on Phytophthora cinnamomi and biotechnological approaches. Mol. Biol. Rep.2020, 47, 9179-9188, doi:10.1007/s11033-020-05911-8.
  • Hardham, A.R.; Blackman, L.M. Phytophthora cinnamomi. Mol. Plant Pathol.2018, 19, 260-285, doi:10.1111/mpp.12568.
  • Cline, E.T.; Farr, D.F.; Rossman, A.Y. A Synopsis of Phytophthora with Accurate Scientific Names, Host Range, and Geographic Distribution. Plant Heal. Prog.2008, 9, 32, doi:10.1094/php-2008-0318-01-rv.
  • Gibbs, J.N.; Lipscombe, M.A.; Peace, A.J. The impact of Phytophthora disease on riparian populations of common alder (Alnus glutinosa) in southern Britain. Eur. J. For. Pathol.1999, 29, 39-50, doi:10.1046/j.1439-0329.1999.00129.x.
  • Brasier, C.M.; Beales, P.A.; Kirk, S.A.; Denman, S.; Rose, J. Phytophthora kernoviae sp. nov., an invasive pathogen causing bleeding stem lesions on forest trees and foliar necrosis of ornamentals in the UK. Mycol. Res.2005, 109, 853-859, doi:10.1017/S0953756205003357.
  • Carbú, M.; González-Rodriguez, V. Garrido, C.; Husaini, C.; Cantoral, J. New biocontrol strategies for strawberry fungal pathogens. In Strawberry: Growth, Development and Disease; Amjad, H., Neri, D., Eds.; CABI: Boston, 2016; pp. 196-211.
  • Bardin, M.; Ajouz, S.; Comby, M.; Lopez-Ferber, M.; Graillot, B.; Siegwart, M.; Nicot, P.C. Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Front. Plant Sci.2015, 6, 1-14, doi:10.3389/fpls.2015.00566.
  • Bosso, L.; Scelza, R.; Varlese, R.; Meca, G.; Testa, A.; Rao, M.A.; Cristinzio, G. Assessing the effectiveness of Byssochlamys nivea and Scopulariopsis brumptii in pentachlorophenol removal and biological control of two Phytophthora species. Fungal Biol.2016, 120, 645-653, doi:10.1016/j.funbio.2016.01.004.
  • Bolívar-Anillo, H.J.; Garrido, C.; Collado, I.G. Endophytic microorganisms for biocontrol of the phytopathogenic fungus Botrytis cinerea. Phytochem. Rev.2019, 1-20, doi:10.1007/s11101-019-09603-5.
  • Lazarovits, G.; Turnbull, A.; Johnston-Monje, D. Plant Health Management: Biological Control of Plant Pathogens; Elsevier Ltd., 2014; Vol. 4; ISBN 9780080931395.
  • Ryan, R.P.; Germaine, K.; Franks, A.; Ryan, D.J.; Dowling, D.N. Bacterial endophytes: Recent developments and applications. FEMS Microbiol. Lett.2008, 278, 1-9, doi:10.1111/j.1574-6968.2007.00918.x.
  • Eljounaidi, K.; Lee, S.K.; Bae, H. Bacterial endophytes as potential biocontrol agents of vascular wilt diseases – Review and future prospects. Biol. Control2016, 103, 62-68, doi:10.1016/j.biocontrol.2016.07.013.
  • Zheng, Y.K.; Qiao, X.G.; Miao, C.P.; Liu, K.; Chen, Y.W.; Xu, L.H.; Zhao, L.X. Diversity, distribution and biotechnological potential of endophytic fungi. Ann. Microbiol.2016, 66, 529-542, doi:10.1007/s13213-015-1153-7.
  • Le Cocq, K.; Gurr, S.J.; Hirsch, P.R.; Mauchline, T.H. Exploitation of endophytes for sustainable agricultural intensification. Mol. Plant Pathol.2017, 18, 469-473, doi:10.1111/mpp.12483.
  • Ludwig-Müller, J. Plants and endophytes: equal partners in secondary metabolite production? Biotechnol. Lett.2015, 37, 1325-1334, doi:10.1007/s10529-015-1814-4.
  • Aly, A.H.; Debbab, A.; Kjer, J.; Proksch, P. Fungal endophytes from higher plants: A prolific source of phytochemicals and other bioactive natural products. Fungal Divers.2010, 41, 1-16, doi:10.1007/s13225-010-0034-4.
  • Morales-Cedeño, L.R.; Orozco-Mosqueda, M. del C.; Loeza-Lara, P.D.; Parra-Cota, F.I.; de los Santos-Villalobos, S.; Santoyo, G. Plant growth-promoting bacterial endophytes as biocontrol agents of pre- and post-harvest diseases: Fundamentals, methods of application and future perspectives. Microbiol. Res.2021, 242, 126612, doi:10.1016/j.micres.2020.126612.
  • Strobel, G. The emergence of endophytic microbes and their biological promise. J. Fungi2018, 4, doi:10.3390/jof4020057.
  • Bolívar-Anillo, H.; Orozco-Sanchez, C.; da Silva Lima, G.; Franco dos Santos, G. Endophytic Microorganisms Isolated of Plants Grown in Colombia: A Short Review. J. Microb. Biochem. Technol.2016, 08, 509-513, doi:10.4172/1948-5948.1000335.
  • Redman Regina, S.; Dunigan David, D.; Rodriguez Rusty, J. Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol.2001, 151, 705-716.
  • Orozco-Mosqueda, M. del C.; Santoyo, G. Plant-microbial endophytes interactions: Scrutinizing their beneficial mechanisms from genomic explorations. Curr. Plant Biol.2021, 25, 100189, doi:10.1016/j.cpb.2020.100189.
  • Latz, M.A.C.; Jensen, B.; Collinge, D.B.; Jørgensen, H.J.L. Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecol. Divers.2018, 11, 555-567, doi:10.1080/17550874.2018.1534146.
  • Hardoim, P.R.; van Overbeek, L.S.; Berg, G.; Pirttilä, A.M.; Compant, S.; Campisano, A.; Döring, M.; Sessitsch, A. The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes. Microbiol. Mol. Biol. Rev.2015, 79, 293-320, doi:10.1128/mmbr.00050-14.
  • Santoyo, G.; Moreno-Hagelsieb, G.; del Carmen Orozco-Mosqueda, M.; Glick, B.R. Plant growth-promoting bacterial endophytes. Microbiol. Res.2016, 183, 92-99, doi:10.1016/j.micres.2015.11.008.
  • Hong, C.E.; Park, J.M. Endophytic bacteria as biocontrol agents against plant pathogens: current state-of-the-art. Plant Biotechnol. Rep.2016, 10, 353-357, doi:10.1007/s11816-016-0423-6.
  • Bolívar-Anillo, H.J.; González-Rodríguez, V.E.; Cantoral, J.M.; García-Sánchez, D.; Collado, I.G.; Garrido, C. Endophytic Bacteria Bacillus subtilis, Isolated from Zea mays, as Potential Biocontrol Agent against Botrytis cinerea. Biology. 2021, 10(6), 492; https://doi.org/10.3390/biology10060492.
  • Shelake, R.M.; Pramanik, D.; Kim, J.Y. Exploration of plant-microbe interactions for sustainable agriculture in CRISPR era. Microorganisms2019, 7, 1-32, doi:10.3390/microorganisms7080269.
  • Afzal, I.; Shinwari, Z.K.; Sikandar, S.; Shahzad, S. Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiol. Res.2019, 221, 36-49, doi:10.1016/j.micres.2019.02.001.
  • El-Sayed, A.S.A.; Akbar, A.; Iqrar, I.; Ali, R.; Norman, D.; Brennan, M.; Ali, G.S. A glucanolytic Pseudomonas sp. associated with Smilax bona-nox L. displays strong activity against Phytophthora parasitica. Microbiol. Res.2018, 207, 140-152, doi:10.1016/j.micres.2017.11.018.
  • Wang, Y.; Zeng, Q. gui; Zhang, Z. bin; Yan, R. ming; Zhu, D. Antagonistic bioactivity of an endophytic bacterium H-6. African J. Biotechnol.2010, 9, 6140-6145, doi:10.5897/AJB10.258.
  • Zhao, L.F.; Xu, Y.J.; Lai, X.H. Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Brazilian J. Microbiol.2018, 49, 269-278, doi:10.1016/j.bjm.2017.06.007.
  • Melnick, R.L.; Zidack, N.K.; Bailey, B.A.; Maximova, S.N.; Guiltinan, M.; Backman, P.A. Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biol. Control2008, 46, 46-56, doi:10.1016/j.biocontrol.2008.01.022.
  • Khalaf, E.M.; Raizada, M.N. Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Front. Microbiol.2018, 9, 1-18, doi:10.3389/fmicb.2018.00042.
  • Misk, A.; Franco, C. Biocontrol of chickpea root rot using endophytic actinobacteria. BioControl2011, 56, 811-822, doi:10.1007/s10526-011-9352-z.
  • Bhusal, B.; Mmbaga, M.T. Biological control of Phytophthora blight and growth promotion in sweet pepper by Bacillus species. Biol. Control2020, 150, 104373, doi:10.1016/j.biocontrol.2020.104373.
  • Agisha, V.N.; Kumar, A.; Eapen, S.J.; Sheoran, N.; Suseelabhai, R. Broad-spectrum antimicrobial activity of volatile organic compounds from endophytic Pseudomonas putida BP25 against diverse plant pathogens. Biocontrol Sci. Technol.2019, 29, 1069-1089, doi:10.1080/09583157.2019.1657067.
  • Kollakkodan, N.; Anith, K.N.; Nysanth, N.S. Endophytic bacteria from Piper colubrinum suppress Phytophthora capsici infection in black pepper (Piper nigrum L.) and improve plant growth in the nursery. Arch. Phytopathol. Plant Prot.2020, 0, 1-23, doi:10.1080/03235408.2020.1818493.
  • Iqrar, I.; Shinwari, Z.K.; El-Sayed, A.S.A.F.; Ali, G.S. Exploration of microbiome of medicinally important plants as biocontrol agents against Phytophthora parasitica. Arch. Microbiol.2021, doi:10.1007/s00203-021-02237-2.
  • Munjal, V.; Nadakkakath, A.V.; Sheoran, N.; Kundu, A.; Venugopal, V.; Subaharan, K.; Rajamma, S.; Eapen, S.J.; Kumar, A. Genotyping and identification of broad spectrum antimicrobial volatiles in black pepper root endophytic biocontrol agent, Bacillus megaterium BP17. Biol. Control2016, 92, 66-76, doi:10.1016/j.biocontrol.2015.09.005.
  • Alsultan, W.; Vadamalai, G.; Khairulmazmi, A.; Saud, H.M.; Al-Sadi, A.M.; Rashed, O.; Jaaffar, A.K.M.; Nasehi, A. Isolation, identification and characterization of endophytic bacteria antagonistic to Phytophthora palmivora causing black pod of cocoa in Malaysia. Eur. J. Plant Pathol.2019, 155, 1077-1091, doi:10.1007/s10658-019-01834-8.
  • Cheffi, M.; Bouket, A.C.; Alenezi, F.N.; Luptakova, L.; Belka, M.; Vallat, A.; Rateb, M.E.; Tounsi, S.; Triki, M.A.; Belbahri, L. Olea europaea l. Root endophyte bacillus velezensis oee1 counteracts oomycete and fungal harmful pathogens and harbours a large repertoire of secreted and volatile metabolites and beneficial functional genes. Microorganisms2019, 7, 1-29, doi:10.3390/microorganisms7090314.
  • Abraham, A.; Philip, S.; Jacob, M.K.; Narayanan, S.P.; Jacob, C.K.; Kochupurackal, J. Phenazine-1-carboxylic acid mediated anti-oomycete activity of the endophytic Alcaligenes sp. EIL-2 against Phytophthora meadii. Microbiol. Res.2015, 170, 229-234, doi:10.1016/j.micres.2014.06.002.
  • Ngo, V.A.; Wang, S.L.; Nguyen, V.B.; Doan, C.T.; Tran, T.N.; Tran, D.M.; Tran, T.D.; Nguyen, A.D. Phytophthora antagonism of endophytic bacteria isolated from roots of black pepper (Piper nigrum L.). Agronomy2020, 10, 1-15, doi:10.3390/agronomy10020286.
  • Segaran, G.; Sathiavelu, M. Fungal endophytes: A potent biocontrol agent and a bioactive metabolites reservoir. Biocatal. Agric. Biotechnol.2019, 21, 101284, doi:10.1016/j.bcab.2019.101284.
  • Fouda, A.H.; Hassan, S.E.D.; Eid, A.M.; Ewais, E.E.D. Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Ann. Agric. Sci.2015, 60, 95-104, doi:10.1016/j.aoas.2015.04.001.
  • Hanada, R.E.; Pomella, A.W. V.; Costa, H.S.; Bezerra, J.L.; Loguercio, L.L.; Pereira, J.O. Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol.2010, 114, 901-910, doi:10.1016/j.funbio.2010.08.006.
  • Mitchell, A.M.; Strobel, G.A.; Moore, E.; Robison, R.; Sears, J. Volatile antimicrobials from Muscodor crispans, a novel endophytic fungus. Microbiology2010, 156, 270-277, doi:10.1099/mic.0.032540-0.
  • Mathew, S.K.; Mary, C.F.G.; Gopal, K.S.; Girija, D. Antagonistic Activity of Endophytic Trichoderma against Phytophthora Rot of Black Pepper (Piper nigrum L.). J. Biol. Control2011, 25, 48-50, doi:10.18311/jbc/2011/3840.
  • Bae, H.; Roberts, D.P.; Lim, H.S.; Strem, M.D.; Park, S.C.; Ryu, C.M.; Melnick, R.L.; Bailey, B.A. Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol. Plant-Microbe Interact.2011, 24, 336-351, doi:10.1094/MPMI-09-10-0221.
  • Miles, L.A.; Lopera, C.A.; González, S.; de García, M.C.C.; Franco, A.E.; Restrepo, S. Exploring the biocontrol potential of fungal endophytes from an Andean Colombian Paramo ecosystem. BioControl2012, 57, 697-710, doi:10.1007/s10526-012-9442-6.
  • Tellenbach, C.; Sumarah, M.W.; Grünig, C.R.; Miller, J.D. Inhibition of Phytophthora species by secondary metabolites produced by the dark septate endophyte Phialocephala europaea. Fungal Ecol.2013, 6, 12-18, doi:10.1016/j.funeco.2012.10.003.
  • Park, Y.H.; Chung, J.Y.; Ahn, D.J.; Kwon, T.R.; Lee, S.K.; Bae, I.; Yun, H.K.; Bae, H. Screening and characterization of endophytic fungi of Panax ginseng Meyer for biocontrol activity against ginseng pathogens. Biol. Control2015, 91, 71-81, doi:10.1016/j.biocontrol.2015.07.012.
  • Terhonen, E.; Sipari, N.; Asiegbu, F.O. Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol. Control2016, 99, 53-63, doi:10.1016/j.biocontrol.2016.04.006.
  • Sreeja, K.; Anandaraj, M.; Bhai, R.S. In vitro evaluation of fungal endophytes of black pepper against Phytophthora capsici and Radopholus similis. J. Spices Aromat. Crop.2016, 25, 113-122.
  • Wang, G.; Liu, Z.; Lin, R.; Li, E.; Mao, Z.; Ling, J.; Yang, Y.; Yin, W.B.; Xie, B. Biosynthesis of Antibiotic Leucinostatins in Bio-control Fungus Purpureocillium lilacinum and Their Inhibition on Phytophthora Revealed by Genome Mining. PLoS Pathog.2016, 12, 1-30, doi:10.1371/journal.ppat.1005685.
  • Sánchez-Ortiz, B.L.; Sánchez-Fernández, R.E.; Duarte, G.; Lappe-Oliveras, P.; Macías-Rubalcava, M.L. Antifungal, anti-oomycete and phytotoxic effects of volatile organic compounds from the endophytic fungus Xylaria sp. strain PB3f3 isolated from Haematoxylon brasiletto. J. Appl. Microbiol.2016, 120, 1313-1325, doi:10.1111/jam.13101.
  • Sánchez-Fernández, R.E.; Sánchez-Fuentes, R.; Rangel-Sánchez, H.; Hernández-Ortega, S.; López-Cortés, J.G.; Macías-Rubalcava, M.L. Antifungal and antioomycete activities and modes of action of isobenzofuranones isolated from the endophytic fungus Hypoxylon anthochroum strain Gseg1. Pestic. Biochem. Physiol.2020, 169, 104670, doi:10.1016/j.pestbp.2020.104670.