Phosphites as alternative for the management of phytopathological problems

Yáñez-Juárez, Moisés Gilberto; López-Orona, Carlos Alfonso; Ayala-Tafoya, Felipe; Partida-Ruvalcaba, Leopoldo; Velázquez-Alcaraz, Teresa de Jesús; Medina-López, Raymundo; Yáñez-Juárez, Moisés Gilberto; López-Orona, Carlos Alfonso; Ayala-Tafoya, Felipe; Partida-Ruvalcaba, Leopoldo; Velázquez-Alcaraz, Teresa de Jesús; Medina-López, Raymundo

doi:10.18781/r.mex.fit.1710-7

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Revista mexicana de fitopatología

versión On-line ISSN 2007-8080versión impresa ISSN 0185-3309

Rev. mex. fitopatol vol.36 no.1 Texcoco ene./abr. 2018

https://doi.org/10.18781/r.mex.fit.1710-7

Review articles

Phosphites as alternative for the management of phytopathological problems

Moisés Gilberto Yáñez-Juárez¹

Carlos Alfonso López-Orona¹

Felipe Ayala-Tafoya¹^*

Leopoldo Partida-Ruvalcaba¹

Teresa de Jesús Velázquez-Alcaraz¹

Raymundo Medina-López¹

^¹ Facultad de Agronomía, Universidad Autónoma de Sinaloa. Carretera Culiacán-Eldorado Km 17.5, Aparatado Postal 25, CP. 80000, Culiacán, Sinaloa, México.

Abstract:

Phosphites are compounds derived from phosphorous acid used as an alternative for the control of phytoparasitic organisms and their effectiveness has been tested against protozoa, oomycetes, fungi, bacteria and nematodes; however, compared to conventional synthesized fungicides, phosphites are generally less effective at reducing damage by phytopathogens. The phosphite ion is easily transported in the plants via xylem and phloem, so it has been used in foliar application, drench of plant root and neck, injection trunk, through drip irrigation mixed in the nutrient solution in hydroponics, seed treatment, aerial application in low volume, or as treatment in immersion of seeds and fruits. The mechanisms of action involved in the prophylactic effects of phosphites are diverse and include the stimulation of biochemical and structural defense mechanisms in plants and direct action that restricts the growth, development and reproduction of phytopathogenic organisms.

Key words: potassium phosphite; biostimulant; control of phytopathogens

Resumen:

Los fosfitos son compuestos derivados del ácido fosforoso empleados como alternativa para el control de organismos fitoparásitos y su eficacia se ha probado contra protozoarios, oomycetes, hongos, bacterias y nematodos; sin embargo, en comparación con los fungicidas convencionales sintetizados, generalmente son menos eficaces para disminuir el daño por fitopatógenos. El ion fosfito es fácilmente transportado en las plantas vía xilema y floema, por lo que se ha utilizado en aplicación foliar, baño a la raíz y cuello de la planta, inyección al tronco, a través de riego por goteo mezclado en la solución nutritiva en hidroponía, tratamiento a semilla, aplicación aérea en bajo volumen o como tratamiento en inmersión de semillas y frutos. Los mecanismos de acción involucrados en los efectos profilácticos de los fosfitos son diversos e incluyen la estimulación de los mecanismos de defensa bioquímica y estructural en las plantas, además de la acción directa que restringe el crecimiento, desarrollo y reproducción de los organismos fitopatógenos.

Palabras clave: fosfito de potasio; bioestimulante; control de fitopatógenos

The irrational use of synthetic pesticides in agriculture increases problems of environmental pollution and public health, and decreases biodiversity in the agroecosystems as well as the development of resistant-phytopathogenic organisms. Furthermore, the current agricultural marketing requires products that are safe for consumers and created using low environmental impact processes. Thus, disease control based on the use of inorganic salts, which aside from being effective in managing crop diseases have minimum adverse consequences, becomes relevant. To this regard, ^{Deliopoulos et al. (2010)} reported that 34 different salts have been used for such purpose, and suggested that phosphite salts stand out because of their use frequency and control effectiveness.

Phosphites are oxyanions derived from phosphorous acid (H₃PO₃ ^-) regularly combined with non-metal cations, such as potassium, sodium, calcium or ammonia. The terms “phosphite” and “phosphonate” are commonly used in the literature to refer to salts derived from phosphorous acid, the same as “hydrogen phosphates”, “orthophosphites”, “phosphonic acid compounds” and “phosphorous acid compounds” (^{Deliopoulos et al., 2010}).

The chemical difference between phosphate (H₂PO₄ ^-) and phosphite (H₂PO₃ ^-) is an oxygen atom that is replaced by another of hydrogen (Figure 1). When oxygen is replaced, there is a profound difference in the way phosphates and phosphites behave in living organisms (^{McDonald et al., 2001}; ^{Achary et al., 2017}). Due to their structural similarity, phosphites are thought to be akin to phosphates. However, the use of phosphites as fungicides and biostimulants to control plant pathogens is widely accepted, but their use as a phosphorus source in plant nutrition is currently debated (^{Borza et al., 2014}; ^{Gómez-Merino and Trejo-Téllez, 2015}; ^{Alexandersson et al., 2016}; ^{Manna et al., 2016}). Such difference gives phosphites a greater mobility in soil and plant tissues, as well as a greater capacity to penetrate through leaves, stems and roots (^{Tkaczyk et al., 2016}).

Figure 1 Structure of the phosphate (A) and phosphite (B) group.

The use of phosphites in agriculture has been studied mainly because of their action to control phytoparasite organisms or as a nutrition source for cultivated plants (^{Gómez-Merino and Trejo-Téllez, 2015}; ^{Alexandersson et al., 2016}). The latter may occur only if phosphites are applied to soil and come into contact with bacteria that have the capacity to oxidize them to phosphates (^{McDonald et al., 2001}; ^{Manna et al., 2016}). However, since this is a very slow process that can take up to four months, it becomes impractical in agriculture (^{McDonald et al., 2001}; ^{Lovatt and Mikkelsen, 2006}).

In early 1930, researchers concluded that phosphites were not an efficient nutrition source for plants. However, 40 years later, phosphites returned to the agrochemicals market as an alternative for controlling plant diseases, when the French company Rhône-Poulenc offered the active ingredient fosetyl-aluminum to control mildews and diseases caused the Phytophthora genus (^{Tkaczyk et al., 2016}; ^{Achary et al., 2017}). Phosphites, as an alternative for controlling phytoparasite organisms, have been extensively studied and proven to be effective against protozoa, oomycetes, fungi, bacteria and phytoparasite nematodes (Table 1), as well as biostimulators (^{Gómez-Merino and Trejo-Téllez, 2015}) that reduce damages caused by weeds (^{Manna et al., 2016}; ^{Achary et al., 2017}) and UV-B radiation (^{Oyarburo et al., 2015}).

Table 1 Control of phytoparasite organisms using phosphites.

Organismo fitoparásito	Planta hospedante	Fosfito	Referencia
Protozoarios
Plasmodiophora brassicae	Brassica rapa	Potasio	Kammerich et al., 2014
Oomycetes
Peronospora destructor	Allium cepa	Potasio	Monsalve et al., 2012
P. manshurica	Glicine max	Potasio	Silva et al., 2011
P. parasitica	Brassica oleracea	Potasio	Becót et al., 2000
Phytophthora cinnamomi	Macadamia spp.	Potasio	Akinsanmi y Dreth, 2013
P. cinnamomi	Ananas comosus	Potasio	Anderson et al., 2012
Phytophthora infestans	Solanum tuberosum	Aluminio	Kromann et al., 2012
P. infestans	S. tuberosum	Calcio	Lobato et al., 2008
P. infestans	S. tuberosum	Potasio	Borza et al., 2017
P. infestans	S. tuberosum	Potasio	Kromann et al., 2012
P. infestans	S. tuberosum	Potasio	Liljeroth et al., 2016
P. nicotianae	Nicotiana tabacum	Potasio	Smillie et al., 1989
P. palmivora	Carica papaya	Potasio	Smillie et al., 1989
Plasmopara viticola	Vitis vinifera	Potasio	Pinto et al., 2012
Pseudoperonospora cubensis	Cucumis melo	Potasio	Méndez et al., 2010
Pythium aphanidermatum	C. sativus	Cobre	Abbasi y Lazarovits, 2006
P. irregulare	C. sativus	Cobre	Abbasi y Lazarovits, 2006
P. ultimum	C. sativus	Cobre	Abbasi y Lazarovits, 2006
P. ultimum	C. sativus	Potasio	Mofidnakhaei et al., 2016
Hongos
Alternaria alternata	Malus domestica	Potasio	Reuveni et al., 2003
Cercospora coffeicola	Coffea arabica	Potasio	Costa et al., 2014
Cochliobolus miyabeanus	Oryza sativa	Potasio	Nascimento et al., 2016
Colletotrichum gloeosporioides	C. arabica	Potasio	Ogoshi et al., 2013
C. gloeosporioides	Fragaria vesca	Potasio	MacKenzie et al., 2009
C. gloeosporioides	Malus domestica	Potasio	Araujo et al., 2010
Fusarium solani	Solanum tuberosum	Calcio	Lobato et al., 2008
F. solani	S. tuberosum	Potasio	Lobato et al., 2008
Fusicladium effusum	Carya illinoinensis	Potasio	Bock et al., 2012
Hemileia vastatrix	Coffea arabica	Potasio	Costa et al., 2014
Oidium sp.	Cucumis sativus	Potasio	Yáñez et al., 2012
Oidium sp.	C. sativus	Potasio	Yáñez et al., 2014
Penicillium digitatum	Citrus limon	Potasio	Cerioni et al., 2013
P. italicum	C. limon	Potasio	Cerioni et al., 2013
P. expansum	Malus domestica	Potasio	Amiri y Bompeix, 2011
P. expansum	Malus domestica	Potasio	Lai et al., 2017
Rhizoctonia solani	Solanum tuberosum	Calcio	Lobato et al., 2008
R. solani	S. tuberosum	Potasio	Lobato et al., 2008
Venturia inaequalis	S. tuberosum	Potasio	Percival et al., 2009
V. pirina	Pyrus communis	Potasio	Percival et al., 2009
Bacterias
Erwinia carotovora	Solanum tuberosum	Potasio	Lobato et al., 2011
E. amylovora	Pyrus malus	Potasio	Aćimović et al., 2015
Pseudomonas syringae pv. actinidiae	Actinidia deliciosa	Aluminio	Monchiero et al., 2015
Nematodos
Helicotylenchus spp.	Musa paradisiaca	Potasio	Quintero-Vargas y Castaño-Zapata, 2012
Heterodera avenae	Avena sativa	Potasio	Oka et al., 2007
Meloidogyne marylandi	Triticum aestivum	Potasio	Oka et al., 2007
Meloidogyne spp.	M. paradisiaca	Potasio	Quintero-Vargas y Castaño-Zapata, 2012
Pratylenchus bracyurus	Glycine max	Potasio	Dias-Areira et al., 2012
Pratylenchus bracyurus	Zea mays	Potasio	Dias-Areira et al., 2012
P. bracyurus	Zea mays	Manganeso	Puerari et al., 20015
Radopholus similis	M. paradisiaca	Potasio	Quintero-Vargas y Castaño-Zapata, 2012

Application methods

The phosphite ion is easily transported in plants via xylem and phloem (^{McDonald et al., 2001}; ^{Tkaczyk et al., 2016}), so it has been used in foliar applications (^{Rebollar-Alviter et al., 2010}; ^{Silva et al., 2011}; ^{Pagani et al., 2014}; ^{Yáñez et al., 2014}; ^{Liljeroth et al., 2016}; ^{Borza et al., 2017}), drench of plants root and neck (^{Oka et al., 2007}; ^{Akinsanmi and Dreth, 2013}), trunk injection (^{Bock et al., 2012}; ^{Akinsanmi and Drenth, 2013}: ^{Aćimović et al., 2015}; ^{Aćimović et al., 2016}) through drip irrigation mixed in a nutrient solution in hydroponics (^{Förster et al., 1998}), seed treatments (^{Abbasi and Lazarovits 2006}; ^{Lobato et al., 2008}), low-volume aerial applications (^{Hardy et al., 2001}) or as a treatment in seed and fruits immersion (^{Anderson et al., 2012}; ^{Cerioni et al., 2013}, ^{Borin et al., 2017}).

Effectiveness

The levels of effectiveness of phosphites to control phytoparasite organisms vary depending on the ion bonded to phosphite, application method, pathogen organism and host plant (Table 2; Figure 2). For example, mandarin orange fruits immersed in solutions containing calcium and potassium phosphites contributed to reduce 50% of fruits infected with citrus green mold caused by Penicillium digitatum (^{Cerioni et al., 2013}); also, soja plants treated with potassium phosphite showed up to 50% less damage by Peronospora manshurica than non-treated plants (^{Silva et al., 2011}). ^{Abbasi and Lazarovits (2006)} reported 80% less cucumber plants infected by Pythium spp. when seeds were treated by immersion in solutions containing copper phosphite. ^{Ogoshi et al. (2013)} obtained a 62.5% decrease in the severity of Colletotrichum gloeosporioides in coffee plants treated with potassium phosphite. In another experiment, 93% of papaya plants treated with potassium phosphite survived the attack of Phytophthora palmivora, but only 24% of non-treated plants survived (^{Vawdrey and Westerhuis, 2007}).

Table 2 Pathogen sensitivity to phosphites in potato (Taken from ^{Lobato et al., 2010}).

	Fosfito de calcio	Fosfito de potasio	Fosfito de cobre
Patógeno		mg mL^-1
Phytophthora infestans	0.09x	0.15	<0.04
Rhizoctonia solani	1.87	>3.56	1.04
Fusarium solani	1.29	>3.56	0.68
Streptomyces scabies	0.83	1.99	0.22

^xCompound concentration to inhibit 50% growth.

Figure 2 Incidence and severity of Pseudoperonospora cubensis (A and A´) and Sphaerotheca fuliginea (B and B´) in cucumber plants cultivated in the greenhouse.

Compared with conventional synthetic fungicides, phosphites are usually less effective to reduce damages caused by phytopathogens. ^{Méndez et al. (2010)} were able to reduce the damage caused by Pseudoperonospora cubensis in melon plants treated with chlorothalonil and mancozeb, but not in those that were treated with potassium phosphite (Figure 3). ^{Aćimović et al. (2016)} were also able to significantly reduce the incidence of Erwinia amylovora using streptomycin sulfate, compared with the incidence of the pathogen when they used potassium phosphite (Figure 4); the compounds were injected into apple tree trunks. ^{Meyer and Hausbeck (2013)} reported a significant decrease in the incidence of death squash plants infected by Phytophthora capsici when they were treated with fluopicolide, mandipropamid or dimethomorph fungicides, compared with the incidence of plants treated with potassium phosphite. In general, the reports on the effectiveness of phosphites and conventional fungicides in controlling phytoparasite organisms suggest that phosphites are less effective and could not replace fungicides at all, but that if they are included as part of an integrated pest management program they could help reduce the use of fungicides as well as the probability that the organisms develop resistance (^{Liljeroth et al., 2016}). ^{Méndez et al. (2010)} reported similar effectiveness against Pseudoperonospora cubensis in squash plants by alternately using chlorothalonil/mancozeb and potassium phosphite compared with the effectiveness when using only fungicides (Figure 3). ^{Liljeroth et al. (2016)} also reported that the protection against Phytophthora infestans in potato was similar using flluazinam, cyazofamid, mandipropamid, metalaxyl + flluazinam or flluopicolide + propamocarb at 100% of the recommended dose, or at 50% of the dose mixed with potassium phosphite.

Figure 3 Average area under the progress curve (ABCPE) from a treatment against Pseudoperonospora cubensis in cucumber plants (Developed by the authors with data from ^{Méndez et al., 2010}).

Figure 4 Control of Erwinia amylovora after two applications of a resistance inducer or antibiotics to trunks of apple trees (Developed by the authors with data from ^{Aćimović et al., 2016}).

Action mode

The action mechanisms involved in the prophylactic effects of phosphites include direct and indirect action. It has been stated that when the phosphite ion come into contact with phytopathogen organisms, it affects their growth and reproduction, because it influences the expression of genes that encode the synthesis of essential compounds in their cell structure and physiology (direct action). When the phosphite ion enters the plant tissue cells (indirect action) activates biochemical (production of: polysaccharides, proteins related to pathogenesis, phytoalexins, etc.) and structural defense (such as callose deposition) mechanisms that restrict pathogens penetration and survival in the plant (Figure 5).

Figure 5 Action mode of phosphites, schematic representation (developed by the authors using data from ^{Daniel and Guest, 2006}; ^{Jackson et al., 2000}; ^{King et al., 2010}; ^{Eshraghi et al., 2011}; ^{Olivieri et al., 2012}; ^{Cerioni et al., 2013}; ^{Dalio et al., 2014}).

Direct action

The addition of phosphites to the medium culture reduced mycelium growth, as well as the number of spore-generating structures and of produced and germinated spores (Figure 6). Thus, with this practice, we observed a growth decrease of Alternaria alternata (^{Reuveni et al., 2003}), Colletotrichum gloeosporioides (^{Araujo et al., 2010}), Fusarium culmorum and F. graminearum (^{Hofgaard et al., 2010}), Mycosphaerella fijiensis (^{Mogollón and Castaño, 2012}), Penicillium digitatum (^{Cerioni et al., 2013}), Phytophthora cinnamomi (^{Wilkinson et al., 2001}; Won et al., 2009; ^{King et al., 2010}), P. cinnamomi, P. palmivora and P. nicotianae (^{Smillie et al., 1989}), P. infestans (Bórza et al., 2014), P. plurivora (^{Dalio et al., 2014}) and Pythium aphanidermatum, P. ultimum, P. irregulare, P. myriotylum, P. torulosum, P. volutum and P. graminicola (^{Cook et al., 2009}). The decrease level in the microorganisms’ growth as a consequence of the phosphite ion is determined by the organism tested, amount of phosphite added to the culture medium, type of ion bonded to phosphite and pH produced by the culture medium (^{Lobato et al., 2010}).

Figure 6 Pythium aphanidermatum in Potato Dextrose Agar (PDA) culture medium (left) and distilled water (right). A and A´ without potassium phosphite; B and B´ with potassium phosphite.

The susceptibility of the microorganisms to the phosphite ion was demonstrated by ^{Wong et al. (2009)}, who determined the negative effect of phosphite and the positive effect of phosphate on Phythopthora cinnamomic growth, when grown in a culture medium enriched with salts containing each ion individually.

As for interspecific susceptibility, ^{Hofgaard et al. (2010)} were able to reduce Fusarium culmorum, F. graminearum and Microdochium majus mycelium growth by 60, 80 and 90%, respectively, using 10 μl ml^-1 of potassium phosphite. To inhibit Phytophthora infestans in vitro growth, ^{Lobato et al. (2010)} used a lower dose, followed by the dose used to inhibit Streptomyces scabies, Rhizoctonia solani and Fusarium solani growth.

The intraspecific susceptibility was studied by ^{Wilkinson et al. (2001)}, who determined that from 21 Phytophthora cinnamomi isolates collected in western Australia, 9% were susceptible, 82% intermediate susceptible and 9% tolerant. ^{Smillie et al. (1989)} showed Phytophthora cinnamomi, P. palmivora and P. nicotiana susceptibility to potassium phosphite, and explained that as the concentration of phosphite increased in the culture medium, the weight of the biomass produced by Phytophthora species decreased. ^{Cook et al. (2009)} also evaluated the concentration of phosphite and mefenoxan fungicide needed to inhibit 50% mycelium growth of eight Pythium aphanidermatum isolates, and reported that all the isolates were susceptible to both compounds, but that the concentrations of phosphite were higher than those of the fungicide.

On the other hand, the phosphate ion reduced pH in the culture medium at acidity levels that were associated with Phytophthora infestans, Rhizoctonia solani, Fusarium solani and Streptomyces scabies low growth (^{Lobato et al., 2010}). ^{Araujo et al. (2010)} reported a larger decrease in the diameter of Colletotrichum gloeosporioides colonies as well as in the growth speed index using formulations containing potassium phosphite, which reduced pH in the medium culture. Also, potassium phosphite affected Alternaria alternata (^{Reuveni et al., 2003}), Colletotrichum gloeosporioides (^{Ogoshi et al., 2013}), Penicillium digitatum (^{Cerioni et al., 2013}), P. expansum (^{Amiri and Bompeix, 2011}) and Peronospora parasitica (^{Becót et al., 2000}) spore germination, as well as Fusarium oxysporum f sp. cubense (^{Davis and Grant, 1996}), Mycosphaerella fijiensis (^{Mogollón y Castaño, 2012}), Peronospora sparsa (^{Hukkanen et al., 2008}), Phytophthora plurivora (^{Dalio et al., 2014}) and P. cinnamomi (^{Wong et al., 2009}) spore production.

The effect of phosphites added to a medium culture was explained by ^{King et al. (2010)}, who reported changes induced by potassium phosphite in the expression of the genes that encode protein synthesis and builds Phytophthora cinnamomi cells and cytoskeleton, which caused hyphae distortion and cell wall lysis.

Indirect action

The indirect action of the phosphite ion includes stimulation of structural and biochemical defense mechanisms in plants. ^{Pilbeam et al. (2011)} described lignin and suberine deposition around tissue damaged by Phytophthora cinnamomi in eucalyptus plants treated with potassium phosphite, which limited the pathogen’s development. ^{Olivieri et al. (2012)} reported an increased pectin content in periderm and cortex tissue and tubers from potato plants treated with potassium phosphite, a feature that improves resistance to different pathogens. ^{Jackson et al. (2000)} reported that the development of lesions caused by P. cinnamomi was highly restricted when they applied a high concentration of phosphite in Eucalyptus marginata tissue, and that the reduced number of lesions was associated with a significant increase of defense enzymes (4-coumarate coenzyme A ligase (4CL) and cinnamyl-alcohol dehydrogenase) and soluble phenols. ^{Daniel and Guest (2006)} demonstrated that when Arabidopsis thaliana plantlets were treated with potassium phosphite and inoculated with Phytophthora palmivora zoospores, the infected cells showed increased cytoplasmic activity, development of cytoplasmic aggregates, release of hydrogen peroxide, located cell death, and enhanced phenolic compounds accumulation. ^{Eshraghi et al. (2011)} also reported that when Arabidopsis thaliana plantlets were treated with potassium phosphite and inoculated with Phytophthora cinnamomi, the infected cells increased their production of calose and hydrogen peroxide.

Conclusions

Phosphites are effective compounds to control protozoa, oomycetes, fungi, bacteria and phytoparasite nematodes, but compared with synthetic conventional fungicides, they tend to be less effective. The effectiveness level of phosphites to solve phytopathological problems is associated with the problem organism, the host plant and the ion bonded to phosphite. Because of its efficient translocation in plant tissue, they can be applied to canopy, stems, roots or fruits. The action mechanisms involved in the prophylactic effects of phosphites are diverse and include the stimulation of biochemical and structural defense mechanisms in plants, besides the direct action that limits phytoparasite organisms’ growth, development and reproduction. Integrating phosphites as part of a phytopathological problems management program allows to reduce the number of fungicide applications as well as the probability that the organisms develop resistance.

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Received: October 31, 2017; Accepted: December 22, 2017

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