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Comments on the use of biocontrol agents against plant- parasitic nematodes

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 International Journal of PharmTech Research
CODEN (USA): IJPRIF, ISSN: 0974-4304, ISSN(Online): 2455-9563
Vol.9, No.12, pp 352-359, 2016

Comments on the use of biocontrol agents against plant-

parasitic nematodes

Mahfouz M. M. Abd-Elgawad
Plant Pathology Department, Nematology Laboratory, National Research Centre,
Dokki, Post Code 12622, Cairo, Egypt.

Abstract : Plant-parasitic nematodes (PPN) undoubtedly represent a serious threat to the world
economy. Growing dissatisfaction with chemical nematicides due to environmental issues
obstructing the use of traditional chemicals has created re-directions in the type and choice of
applicable nematicides. The role of different beneficial microorganisms ranks high as
environmentally friendly biological alternatives to synthetic nematicides. However, in order to
maximize the benefit from these biocontrol agents against PPN, a few issues and/or
shortcomings in experimentations and applications against PPN have been reviewed herein. It
should be highlighted that an evaluation of biocontrol agent efficacy, based on nematode-egg
mass index (EI) is better than that based on gall index (GI) because the former index measure
nematode fecundity. Moreover, El does not measure nematode reproduction adequately because
it does not quantify the eggs produced. Nematode eggs may be a better parameter of sedentary
nematode reproduction than GI, EI or other developmental stages. Possible weak links in a
nematode’s life-cycle that can be targeted for biocontrol by fungal or bacterial antagonists are
illustrated herein in more details. Many researchers study the effects of biocontrol agents on
their targets of PPN exclusively but the efficacy of these agents on crop yields and/or plant
growth parameters as the crux of the matter should also be considered. Moreover, such an
efficacy is mainly based on PPN parameters but measuring accumulations and/or activities of
pathogenesis-related proteins and other relevant compounds could be used as fast and accurate
biochemical markers or components of systemic resistance in plants against PPN infection and
reproduction.
Key words: Plant-parasitic nematodes, biocontrol, induced resistance, markers, mode of action.

Introduction
Plant-parasitic nematodes (PPN) are responsible for great losses in crop production systems
worldwide. Abd-Elgawad and Askary (2015)1 reported an average worldwide crop loss of 12.6%
which equaled $215.77 billion annual yield loss due to these nematodes for only the top 20 life-
sustaining crops based on the 2010-2013 production figures and prices. Moreover, 14.45% or $142.47
billion was an average annual yield loss in the subsequent group of food or export crops. These figures
are astonishing, and the authentic figure, when more crops throughout the world are considered,
probably exceeds such estimations. On the other hand, numerous relevant and challenging issues have
been demonstrating the desperate need of human beings to provide more and better food for an over-
populated world. Abd-Elgawad (2014a)2 stressed the importance of such issues due to reduced number
of effective nematicides available and limitation in their use because of environmental and health
hazards, renewable manifestation of resistance-breaking nematode pathotypes on many important
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 353

crops, climate change, increased adoption of intensive agriculture, and potential occurrence of
quarantine-nematodes. Therefore, nematode management and research should be more oriented to
offer better control of PPN in an environmentally and economically beneficial manner.

In Egypt, as a case in point, such loss estimates due to PPN on 80 crops, 15 of which are ‘life
sustaining’, were reported by Abd-Elgawad (2014b)3 as L.E. 15.85 (= $2.30) billion annually for
2011-2012 production season and prices. Considerable crop losses of vegetables, fruits, and field crops
were apparent. For example, such estimates for vegetables only are shown in Table 1. Likewise,
numerical estimates of yield losses in other crops such as citrus and legumes are staggering. Therefore,
solving PPN problems warrant a lot of more efforts and backup. In this respect, continuous research on
different aspects of PPN, especially those factors relevant to crop damage and nematode control, is in
progress. As root-knot nematodes (RKN), Meloidogyne spp., are among the main important pests
causing serious yield losses, such studies are essential for determining their appropriate control
strategies. Recently, RKN damage was examined on sugar beet varieties by Youssef et al. (2016)4, on
sunflower by Korayem et al. (2016)5 and on cowpea by El-Nagdi and Youssef (2016)6. Different
management tactics of these nematodes via host-plant resistance, chemical control, biological control,
crop rotation and other cultural practices are in progress7 , 8 . Despite the importance of any of these
tactics, accelerating public concern about overuse of synthetic chemical pesticides has urged
researchers to direct a lot of their investigations to biological control agents as safe alternatives to
these chemicals with a clear aim at avoiding their health hazards and environmental pollution. Many
researchers and stakeholders are addressing such a goal through the development of biocontrol agents
as environmentally friendly biological alternatives. For instance, evaluation of soil amended with
biological control agents and/or compost for controlling the citrus nematode, Tylenchulus
semipenetrans, and fusarium dry root rot was carried out by El-Mohamedy et al. (2016)9 on sour
orange and by Hammam et al. (2016)10 on Volkamer lime.

Yet, in order to maximize the benefit from this biocontrol approach, I’d like to review and
discuss herein some issues and/or shortcomings in experimentations against PPN and offer my point
of view towards PPN-management philosophy and applications of biological control agents.

1. Adequate nematode parameters

Extensive research has been conducted on the use of pathogenic or non-pathogenic microorganisms
(bacteria, fungi viruses and nematodes) against different species and populations of PPN. For example,
McKenry and Anwar (2007)11 found that avirulent M. incognita populations induced systemic resistance against
virulent populations of M. arenaria infecting harmony grape rootstocks. Similarly, pre-inoculated avirulent
strains of two nematode species (i.e., Meloidogyne incognita and Bursaphelenchus xylophilus) could induce
systemic resistance against M. hapla and B. xylophilus in tomato and pine plants as reported by Ogallo and
McClure (1995)12 and Kosaka et al. (2001)13, respectively. Different nematode parameters are used for such
experimentations. These parameters may include nematode reproduction ratio/factor. A reproduction factor is
the outcome of dividing the final nematode population (Pf), by the initial inoculum density of nematodes (Pi).
One or more developmental stages of the targeted nematode species are usually considered as Pf.
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 354

Table 1. Summary of annual yield losses in vegetables due to damage by plant parasitic nematodes in
Egypt* as estimated by Abd-Elgawad 3.

Varieties Loss Actual Price Actual loss Loss

(%) production (L.E./ton) (metric tons) (Million
(metric tons) L.E.)
Tomato 12% 8571050 1500 1168779.5 1753.17
Squash 20% 559598 1000 139899.5 139.9
Green bean 7% 251279 3000 18913.44 56.74
Dry bean 7% 69486 5000 5230.13 26.15
Green cowpea 10% 24277 3000 2697.44 8.09
Dry cowpea 10% 12950 5000 1438.89 7.19
Green pea 12% 180631 4000 24631.5 98.53
Dry pea 12% 124 6000 16.91 0.10
Cabbage 9% 638227 500 63121.35 31.56
Cauliflower 5% 171088 500 9004.63 4.50
Eggplant 20% 1193642 1000 298410.5 298.41
Pepper 22% 650554 2000 183489.59 366.98
Okra 13% 97108 3500 14510.39 50.79
Jew's mallow 6% 80316 1000 5126.55 5.13
Spinach 10% 39413 2500 4379.22 10.95
Mallow 8% 2161 1000 187.91 0.19
Artichokes 10% 387704 1500 43078.22 64.62
Taro 6% 118759 2000 7580.36 15.16
Radish 10% 12000 800 1333.33 1.07
Turnip 8% 32779 500 2850.35 1.43
Lettuce 12% 93661 2000 12771.96 25.54
Carrot 13% 179291 2000 26790.61 53.58
Parsley 8% 88487 1000 7694.52 7.69
Arugula 7% 52281 1000 3935.13 3.94
Egyptian leek 10% 31223 1000 34692.22 34.69
Sweet Potato 7% 319427 750 24042.89 18.03
Strawberry 12% 242297 2000 33040.5 66.08
Beet 10% 3518 2000 390.89 0.78
Pumpkin 17% 1256 1200 257.25 308.7
Watermelon 14% 1874710 1200 305185.35 366.22
Cucumber 15% 587612 1500 103696.24 155.54
Armenian cucumber 15% 50568 1400 8923.76 12.49

Cantaloupe 15% 854204 1500 150741.88 226.11

Melon 15% 89927 1400 15869.47 22.22
Shahad 15% 62716 1600 11067.53 17.71
Potato 8% 4758040 2000 413742.61 827.49
water melon pulp 10% 67274 4500 7474.89 33.64
seeds
*Based on 2011-2012 total Egyptian production figures and prices on wholesaling basis; not retail.

For RKN, different nematode parameters have been in use such as nematode gall index (GI), egg mass
index (El), eggs, and/or nematode developmental stages within roots and soil for such experimentations. I’d like
to stress that an evaluation of biocontrol agent efficacy, based on EI is better than that based on GI because the
former index measures nematode fecundity. Moreover, El does not measure nematode reproduction adequately
because it does not quantify the eggs produced. Dababat and Sikora (2007)14 used number of M. incognita galls
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 355

and egg masses per root system in order to assess resistance induced by the mutualistic endophyte, Fusarium
oxysporum strain 162, toward M. incognita on tomato. Nematode eggs may be a better parameter of sedentary
nematode reproduction than galls and egg masses or other developmental stages. Standardized screening
protocols for plant-nematode resistance usually depend on such an accurate measure15,16 but this application
should also be considered while evaluating biocontrol agents against RKN.

2. Modes of action of biocontrol agents vs. weak links in nematodes’ life-cycle

Although these modes of action have recently been reviewed17, further research should reveal
more attributes for each of their mechanisms involved in the nematode control. This is especially
important for virulence mechanisms of microorganisms such as fungi18 and bacteria19 against PPN.
For example, the modes of action of nematophagous bacteria may be through: parasitizing, producing
toxins, antibiotics, enzymes, competing for nutrients, inducing systemic resistance of plants, and
promoting plant health20. So, nematophagous bacteria could be grouped based on their modes of
action. If so, they can be broadly grouped into parasitic bacteria and non-parasitic rhizobacteria21; but
they may also split to contain six categories: obligate parasitic bacteria (Pasteuria spp.), opportunistic
parasitic bacteria, rhizobacteria, cry protein-forming bacteria, endophytic bacteria, and symbiotic
bacteria20,22. Furthermore, Sikora et al. (2007)23 mentioned three main modes of action employed by
bacterial endophytes for the biocontrol of phytonematodes. These are: 1) preventive colonization; 2)
immediate antagonism via toxic metabolites; or 3) induced systemic resistance (ISR)24. While
nematophagous fungi have various virulence mechanisms to manage PPN, predatory and egg-parasitic
fungi are the most promising agents due to their readiness for laboratory production, nematode control
potential, ability to adapt to different agroecosystems and possible subjection to multitude of studies18.

Each of these mechanisms affects one or more of the weak links in a nematode’s life-cycle.
Sikora et al. (2007)23 mentioned nine possible weak links in a nematode’s life-cycle that can be
targeted for biocontrol by fungal or bacterial antagonists. I’d like to add herein two new links to
comply with recent nematological philosophy in terms of using more available research tools for
accurate details of nematode data and their interpretations. The new important links are nematode
persistence in soil and nematode development (Fig. 1). These weak links could generally be explained
by Dababat and Sikora (2007)14 who found that inoculation of tomato plants with the non-pathogenic
fungal endophyte Fusarium oxysporum strain 162 resulted in a significant reduction of Meloidogyne
incognita infection; due in part to induced resistance after fungal inoculation. For clarification of the
two new links, suppressiveness of soils, for instance, to Meloidogyne arenaria race 1 in a peanut field
located near Williston, Levy County, Florida, USA, was observed by Dickson et al. (1994)25 over a
period of several years of crop production; indicating poor nematode persistence in soil. Also, Orion et
al. (1980)26 indicated that higher concentration of ammonia released during the decomposition, by
bacteria, of organic additives/amendments could inhibit the complete development of syncytium which
is necessary for the nematode development, since syncytium is the food supplier for the root-knot
nematode. Moreover, in order to bring PPN populations below a threshold level, it is also important to
note that these biocontrol agents may have a determined specificity against definite stages or species
of the nematodes. Eventually, determining which stage in the life-cycle of a nematode species/strain is
the best target for biocontrol tactics necessitates carefully conceived and well carried out
experimentation.
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 356

Fig. 1. The pathozone of soil surrounding the root system of young plants, and eleven possible weak links
in a nematode’s life-cycle that can be targeted for biological control by fungal or bacterial antagonists,
modified from Sikora et al., 23.

3. Effects of biocontrol agents on plant growth parameters

Although investigating the effects of biocontrol agents on their targets of PPN are usually the
direct objectives of nematode management studies, we should consider the efficacy of these agents on
crop yields and/or plant growth parameters as the crux of the matter. In other words, the former effects
are of course desirable. Valid as they are, the relationships of these agents with their surroundings are
frequently complicated by many other factors that can favor or disfavor such effects on PPN and plant
growth parameters. To name but few of these factors are the carry-over stress effects from one
crop/year to the next, cyclic nematode population growth, the interaction between pest and plant
stresses and the capacity for vigorous trees/plants to support (tolerate) larger populations than those
with a limited number, of severely infected roots and consequently disorganized vascular system.

Since biocontrol agents have been gaining more consideration as novel, safe and potential tools
to provide major benefits for PPN management, their consistent and skillful performance should be
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 357

addressed. Therefore, they should fit with a range of complex intrinsic (microbial), external (host and
environmental) and most importantly, integrated factors. These factors make up the specific context in
which biocontrol agents are used27. Accommodating each of these factors is an essential step towards
enhancing the level and reliability of their activity not only against PPN but also to attain crop yield
increase. If properly handled, these factors can also act synergistically with such agents to increase
consistency and efficacy. Rational management decisions can be made only by analyzing the
interactions naturally occurring among host plant-nematode target-soil–microbial control agent-
environment; a five-party interaction (Dong and Zhang, 2006)28. Therefore, nematode population
levels may affect fruit yields differently under various conditions29. Thus, the most sustainable method
to PPN control should integrate several tools and tactics via integrated pest management (IPM). With
better and sound tackling of these interactions, biocontrol of nematodes should be more fine-tuned via
strain selection and improvement (e.g. for compatibility with agrochemicals and interaction with other
biotic and abiotic factors), mass production, formulation, packaging, successful wide-scale testing and
field application of biocontrol agents. Efficient quality control and standardization, registration, and
sound market assessment (product efficacy, cost, profit margins, shelf-life, ease-of-use, market
acceptance, product coverage and stability) should be pursued to contribute to both development of
efficacious biocontrol for PPN and yield increase. These issues and technical advances in their
production and utilization will provide further opportunities to integrate the use of biocontrol agents in
management programs of nematode pests.

4. Induced plant resistance

Systemic resistance can be induced via different approaches. Defense mechanisms in induced
plants can be directly activated after infection by pathogens including fungi30, bacteria31, and
nematodes12 or after treatments by chemicals such as salicylic acid, benzothiadiazole and 2,6-
dichloroisonicotinic acid32, or following challenge of the induced tissue by parasites33. The latter case
is known as priming which occurs in systemic acquired resistance (SAR), induced systemic resistance
(ISR), and mycorrhiza-induced resistance (MIR). The molecular mechanisms of priming are based on
epigenetic modifications that suppress or enhance the transcription of key regulators of the immune
system. Changes in methylation and acetylation status of DNA and histones have been associated with
the activation of immune related genes in plants. Therefore, a combination of epigenetic control
mechanisms and an abundance of signals are probably to be at the base of long-lasting immune
memory in plants33,34. For example, the addition of the nonpathogenic endophytic Fusarium
oxysporum strain 162 to the inducer side of the split-root system of tomato plants resulted in a
significant reduction of Meloidogyne incognita penetration in the responder side of the split-root
system, and in reduced production of galls and egg masses, 2 and 5 weeks after nematode inoculation,
respectively14. Consequently, the authors14 concluded that induced resistance was an important
component of the overall mode of action of non-pathogenic endophytic F. oxysporum on tomato plants
and a factor that influences plant based changes in nematode behavior. Interestingly, induction of
resistance against many pathogens has frequently been correlated with the synthesis and accumulation
of salicylic acid, jasmonic acid, pathogenesis-related proteins, and enzymes such as catalase and
peroxidase in different plant species33,35. Yet, some references have not considered such correlations.
Therefore, I’d like to emphasize the need to measure also accumulations and/or activities of these
compounds as fast and accurate biochemical markers or components of systemic resistance in plants
rendering them less suitable for PPN infection and reproduction.

Acknowledgement

This study was supported in part by the US-Egypt Project cycle 17 (no. 172) and NRC In-house
project entitled ‘Pesticide alternatives against soilborne pathogens attacking legume cultivation in
Egypt’.
Mahfouz M. M. Abd-Elgawad /International Journal of PharmTech Research, 2016,9(12): 352-359. 358

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