Plant-Parasitic Nematodes: Nature's Most Successful Plant Parasite - International Journal of Research ...
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
International Journal of Research and Review
Vol.7; Issue: 3; March 2020
Website: www.ijrrjournal.com
Review Article E-ISSN: 2349-9788; P-ISSN: 2454-2237
Plant-Parasitic Nematodes: Nature’s Most
Successful Plant Parasite
Yogendra Kumar1, Bindhya Chal Yadav2
1
Assistant Professor, Department of Botany, Govt Degree College Nanauta, Saharanpur
2
Assistant Professor, Department of Botany, Govt PG College Fatehabad, Agra
Corresponding Author: Yogendra Kumar
ABSTRACT economic thresholds. The RKN causes root
galling, however, the degree of galling may
Nematodes are thread-like roundworms that live depend on the interaction between the plant and
in a wide range of environments including soil the RKN species.
and fresh and salt water. There are species of
nematodes that feed on fungi, bacteria, Keywords: Nematode, root-knot, Meloidogyne
protozoans, other nematodes, and plants. They PPN
can also parasitize insects, humans, and animals.
Nematodes that feed on plant parts are called INTRODUCTION
plant parasitic nematodes (PPN) and are Plant parasitic nematodes are the
ubiquitous in agricultural soils. The life cycle of nature’s most successful of all parasites.
a nematode includes eggs, juveniles and adults, These nematodes have been reported from
and they can overwinter at any of these stages.
all terrains from all continents. Some of the
Crop damage is the result of a complex
interaction of the environment, initial nematode members are adapted to survive on coldest
populations at planting, the pathogenicity of the of the temperature. Ability to survive of any
nematode species and the ability of the plant to plants makes them most difficult to control.
tolerate nematode feeding. Most PPNs feed by The biology of these enigmatic worms are
piercing and killing root cells with needle-like slowly beginning to unfold. Most of the
structures called stylets. Nematodes that utilize information about these tiny worm is
this type of feeding include lesion, lance, obtained from one of the most extensively
needle, sting, stunt, and sting nematodes. Some studies nematode Caenorhabditis elegans, a
of the most economically damaging nematodes free living nematode. Still the parasitic
like the root knot nematode (RKN) enter roots arsenal of these plant parasitic nematodes
and establish a permanent feeding site where
remains largely unknown. ESTs studies and
they complete their life cycles without killing
the cells around them. Symptoms associated also the complete genomic sequences
with nematode infection are similar to those allowed scientist to peep in to the secret
caused by impaired root growth and function; world of these nematodes. Members of the
therefore they may resemble abiotic stress like phylum Nematoda (round worms) have
drought and nutritional deficiencies as well as been in existence for an estimated one
biotic factors like stem and root rots. General billion years, making them one of the most
symptoms from nematodes include yellowing, ancient and diverse types of animals on
stunting, and wilting, accompanied by a yield earth (Wang et al. 1999). They are thought
decline. In the case of SCN, signs of infection to have evolved from simple animals some
are white-to-pale-yellow female bodies present 400 million years before the "Cambrian
in roots that can be seen with the naked eye.
explosion" of invertebrates able to be
Nonetheless, above ground symptoms are not
always obvious and infections can go fossilized (Poinar 1983). The two nematode
undetected until populations are well-beyond classes, the Chromadorea and Enoplea, have
International Journal of Research and Review (ijrrjournal.com) 379
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
diverged so long ago, over 550 million years intestine ends at the rectum in the female
that it is difficult to accurately know the age nematode and the cloaca in the male.
of the two lineages of the phylum Attached to the pharynx are three - five
NEMATODE BIOLOGY salivary glands which produce secretions
The study of nematode biology has that may be emitted from the stylet and that
led to a dramatic increase in understanding assist the nematode in plant invasion and
of how all animals function. In fact, the parasitism. The nematode pharynx is
bacterial-feeding nematode, Caenorhabditis muscular and specialized areas can contract
elegans, is one of the best-understood and expand the esophageal lining. The
animals on earth. The fate of every cell in C. expansion and contraction of the pharynx
elegans development has been carefully muscles allow the nematode to pump food
mapped. It was the first animal to have its into its intestine through its stylet or eject
DNA sequence completely deciphered, and secretions from its salivary glands into and
it is amenable to detailed genetic analysis. around plant cells. In rhabditidan
The study of C. elegans has led to new nematodes, the esophageal muscles are
insights into the details of animal localized in a muscular organ called the
development, neurobiology, behavior, and metacorpus. In enoplean nematodes, the
has been of great value in biomedical esophageal muscles are more spread out and
research as well as in the understanding of do not form a compact pumping organ. In
nematode biology (Riddle et al. 1997). The the middle to posterior of the nematode are
reason nematodes are so useful for the reproductive organs. Nematode species
biological research is due to their simple often have both males and females, but it is
anatomy and transparent bodies. Nematodes not uncommon for plant nematodes to
are simple animals, often only containing reproduce asexually by parthenogenesis. In
1000 cells or less. Nematodes in all or part females the reproductive organs are used as
of their life cycle are worm-shaped traits for identification because the number
(vermiform), although some species become of ovaries and the position of the vulva in
swollen and rounded in later life stages. The the female nematode's body are easily seen
basic body plan of a nematode is a tube under the light microscope. Male nematodes
within a tube. They have an outer skin or have one or two testes and they are easily
cuticle that is secreted from an inner identified by the presence of spicules.
hypodermis. The muscles are attached Spicules are copulatory structures that are
longitudinally to the nematode’s used during mating to guide the sperm into
hypodermis, allowing them to move only in the vagina of the female nematode.
the dorsal ventral direction (snake-like The common plant-parasitic
movement). Inside the nematode there is an nematode genera are fairly easy to identify
inner tube, the alimentary canal, which runs to that level using a standard compound
inside the nematode from head to tail. microscope. Identification of nematodes to
Between the alimentary canal and the body the species level often requires detailed
wall is fluid that provides pressure against morphological analysis, growth of the
the wall to maintain body shape and allow nematode on different host plants, or DNA
movement. At the head of a plant-parasitic or isozyme analysis. Common
nematode is a hollow mouth spear (like a morphological features used in nematode
hypodermic needle) called a stylet. The identification include the mouth cavity
nematode uses this stylet to puncture plant (presence or absence and shape of a stylet),
cells, to withdraw food and also to secrete the shape and overlap of the pharyngeal
protein and metabolites that aid the glands with the intestine, size and shape of
nematode in parasitizing the plant. The the nematode body at the adult stage, size of
stylet is connected to the pharynx that, in the head, tail, and number and position of
turn, is connected to the intestine. The ovaries in the female. More subtle
International Journal of Research and Review (ijrrjournal.com) 380
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
characters may include number of lines on muscles. Nematode muscles are arranged
the nematode’s cuticle or the presence or along the longitudinal axis of the worm,
absence of pore-like sensory organs. An thus allowing the body of the nematode to
excellent guide to nematode identification is move only in a sinusoidal (snake-like)
“Plant-Parasitic Nematodes: a Pictorial Key motion. Nematodes have no defined
to Genera” by William F. Mai et al., 1996. respiratory or circulatory systems; they
Plant-parasitic nematodes occur in depend on diffusion of water, gasses and
all sizes and shapes. The typical nematode metabolites in and out of their semi-
shape is a long and slender worm-like permeable body walls and internal transport
animal, but often the adult animals are by mixing of the pseudocoelomic fluid as
swollen and no longer even resemble the nematode moves. This lack of
worms. Plant-parasitic nematodes range respiratory/ circulatory systems prevents
from 250 um to 12 mm in length, averaging nematodes from becoming larger in cross
1 mm, to about 15-35 um in width. While sectional area, but does not limit their
nematodes may look dramatically different, length. The largest nematode found thus far
they all share some common features. was more than 7 meter long and 1 cm in
Nematodes often look segmented because of diameter. Sorry, no giant nematodes; they
the numerous annulations (accordion-like are only in the movies. Nematodes have a
transverse grooves) on the cuticle that allow sophisticated nervous system and sensory
the nematode to bend without kinking, but organs to help them find their host plant, to
in fact nematodes are unsegmented and have locate specific plant cell types, and to mate
no replication of body parts throughout the and reproduce.
worm. Like most higher animals nematodes HOW THE NEMATODE SURVIVE IN
possess bilateral symmetry, but with a NATURE
superimposed trilateral and hexalateral One might think of soil as a safe
symmetry. Developmentally, nematodes are environment, but to a microscopic nematode
triploblastic, containing three body layers it is a hostile world filled with danger. A
(ectoderm, mesoderm and endoderm) in the nematode must contend with voracious
embryo. Most higher organisms are predators, changes in soil temperature and
tripoblastic and have a coelom, a body moisture, and the death of its host plant. For
cavity surrounded by mesoderm. Nematodes a nematode population to survive, it must be
have a body cavity that is not totally able to circumvent these obstacles.
surrounded by mesoderm, so they are Nematodes evade these biotic and abiotic
pseudocoelomic. obstacles by employing a combination of
Nematodes are evolutionarily related behavioral and physiological survival
to insects, and one feature they have in strategies. While all nematodes feed on
common is the requirement to molt between other organisms, the soil is filled with
juvenile stages. All nematodes undergo four bacteria, fungi and other nematodes that
molts from the juvenile to the adult phase of would gladly consume a nutrient-rich plant-
their life cycle. They have four juvenile parasitic nematode. In fact, the study of
stages and an adult stage. In many nematode predators and pathogens is an
nematodes the first molt usually occurs in important area of study in nematology
the egg and it is the second-stage juvenile because nematode predators can be used (in
that hatches. While all nematodes undergo theory) to control populations of plant-
four molts, molting is not required for parasitic nematodes. While nematodes do
growth of the nematode as it is in insects possess a thick cuticle that may provide
because of the elasticity of the nematode some protection from predation, this type of
cuticle. Nematodes do not have a skeleton, defense is easily breached by specialized
but they do have a hypodermis which nematode pathogens. The most common
functions as a flexible support for their method plant nematodes use to evade
International Journal of Research and Review (ijrrjournal.com) 381
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
predation is by living inside plant tissue or While nematodes are motile animals,
by limiting their mobility in the soil most are able to move no more than a meter
environment. By spending less time moving through the soil within their lifetime.
in the soil, a nematode can reduce its chance However, this lack of long distance
of "running into" a predator or pathogen. crawling does not mean nematodes cannot
Some plant nematodes spend most of their rapidly spread from field to field. Farm
time in the soil (ectoparasites) and others equipment and even muddy shoes
are mostly contained within the plant tissue contaminated with nematode-infested soil
(endoparasites). Nematodes that live inside can rapidly disperse nematodes. The
plants have some degree of protection from movement of water during floods and
predation, but they risk death if their host irrigation can disperse nematodes over long
plant succumbs to disease. In contrast, distances. Likewise the movement of
nematodes that move from host to host nematode infected plants, seeds, and bulbs
reduce the risk of perishing with their host, can give nematodes international tickets to
but have a greater chance of encountering a travel the world if plant quarantine officials
predator or pathogen. are not careful. The ability of nematodes to
Nematode survival is not impacted form environmentally resistant stages makes
only by biotic factors, but also by abiotic their dissemination even easier, since dried
ones such as temperature and water nematodes can be blown with the wind or
availability. The onset of winter or the plant debris over large geographical regions.
drying of the soil can be disastrous for a Even migrating birds are suspected to be
nematode. Interestingly, many nematodes able to carry nematodes along their flight
are well adapted to abiotic stress and are paths, assisting the nematodes in their quest
capable of cryptobiosis (hidden life): the for new homes. Essentially any process that
ability to enter a state of suspended moves soil or plant tissue has the ability to
metabolic activity during unfavorable disperse plant nematodes, making them
environmental conditions (drying, heat, difficult plant pathogens to quarantine.
cold). While not all nematode are capable of PLANT AND PARASITIC
cryptobiosis, the ones that are can often INTERACTION
survive for years in a cryptobiotic state Nematodes feed on all parts of the
awaiting favorable conditions that will plant, including roots, stems, leaves, flowers
trigger their revival. The ability of and seeds. Nematodes feed from plants in a
nematodes to undergo cryptobiosis is one variety of ways, but all use a specialized
reason some nematode species are very spear called a stylet. Note the differences in
difficult to eradicate from a field. stylet length and shape. The size and shape
Although cryptobiosis is a useful of the stylet is used to classify nematodes
survival strategy, not all nematodes can and also can be used to infer their mode of
enter such a survival stage. Instead, some feeding. All three nematodes in Figure 4 are
nematodes have adapted to feed upon many ectoparasites,
different plant species, thus avoiding the but Belonolaimus and Longidorus feed deep
disaster of losing a host plant. Nematodes within the roots using their long stylets,
with a broad host range can feed upon while Helicotylenchus feeds on the exterior
weeds and wild plants making their of the root or partially burrows into the root
eradication virtually impossible. By using a to feed using its short stout stylet.
complex network of behavioral and Often nematodes withdraw the
biochemical protections nematodes are able contents of plant cells, killing them. When
to survive and prosper in what would seem this type of feeding occurs, large lesions are
to us to be hostile environments. formed in the plant tissue. Some nematodes
DISTRIBUTION OF NEMATODES IN do not kill the plant cells they feed upon but
FIELDS “trick” the plant cells to enlarge and grow,
International Journal of Research and Review (ijrrjournal.com) 382
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
thus producing one or more nutrient-rich funnel or moist chambers to collect
feeding cells for the nematode. These nematodes that will exit the tissues. Most
feeding cells enable long term feeding plant parasitic nematodes are soilborne root
associations, and form by repeated nuclear pathogens, but a few species feed primarily
division in the absence of cell division upon shoot tissues. The majority of plant
(giant cells) or by the incorporation of parasitic nematode species are in the class
adjacent cells into a syncytium formed by Chromodorea, order Rhabditida (formerly
the breakdown of neighboring cell walls. placed in the order Tylenchida).
Collectively, nematodes can feed on almost
any plant cell type, and form a variety of ECTOPARASITIC NEMATODE
feeding cell types. The number of feeding The first feeding type is the
cells can vary from one to a half dozen ectoparasitic mode, in which the nematode
depending on the nematode species. Many remains outside of the plant and uses its
plant-parasitic nematodes feed on the roots stylet to feed from the cells of the plant
of plants. The feeding process damages the roots. Nematodes that use this strategy can
plant's root system and reduces the plant's graze on numerous plants, making it easier
ability to absorb water and nutrients. for them to switch hosts, but their added
Typical nematode damage symptoms are a mobility makes them very susceptible to
reduction of root mass, a distortion of root environmental fluctuations and predators.
structure and/or enlargement of the roots. Ectoparasitic nematodes can have extremely
Nematode damage of the plant's root system long stylets, which assist them in feeding
also provides an opportunity for other plant deep within the plant root on nutrient rich
pathogens to invade the root and thus plant cells. Some of these nematodes induce
further weakens the plant. Direct damage to the plant to form an enlarged cell(s) that the
plant tissues by shoot-feeding nematodes nematode feeds from for an extended period
includes reduced vigor, distortion of plant of time. Note, in all life cycle diagrams in
parts, and death of infected tissues this article the abbreviation J=juvenile and
depending upon the nematode species. The the number refers to the stage of the
aboveground symptoms of nematode nematode and M=molt and refers to how
damage to roots are relatively nondescript, many molts the nematode has completed.
including nutrient deficiency, incipient wilt, SEMI ENDO-PARASITIC NEMATODE
stunting, poor yield and sometimes plant Nematodes that feed as semi-
death. Few diagnostic signs and symptoms endoparasites are able to partially penetrate
of plant damage by nematodes exist except the plant and feed at some point in their life
root galls, cysts, "nematode wool," and seed cycle. Usually the head of the nematode
galls. Thus, damage to crops by root- penetrates into the root and allows the
infesting nematodes often goes unnoticed by nematode to form a permanent feeding cell.
growers. Field patterns of nematode damage These nematodes swell and do not move
to roots begin in a small area and spreads once they have entered into the
radially from the initial infection site, often endoparasitic phase of their life cycle. By
assisted by farm equipment. The only way giving up their mobility, the nematodes risk
to accurately diagnose nematode disease is death if their host plant dies, but they also
to sample soil and plant material from benefit from forming a permanent feed site,
suspected sites and extract nematodes for which increases their nutrient uptake and
analysis. Nematodes are extracted from the reproductive potential. A typical nematode
soil by floating them in water to remove with this life cycle is Rotylenchulus
heavy soil particles and then catching the reniformis, the reniform (kidney-shaped)
floating nematodes on sieves with fine pore nematode. This nematode hatches from the
sizes. Plant tissues infected with motile egg as a J2, then quickly molts in the soil to
nematodes can be incubated in a Baermann the adult stage without feeding. The anterior
International Journal of Research and Review (ijrrjournal.com) 383
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
end of an adult female enters the plant root knot nematodes (Meloidogyne). In these
and forms a feeding cell. After mating, the nematodes, the J2 invades the plant near the
female lays its eggs outside of the root in a tip of a root and migrates through the tissue
gelatinous egg mass Maggenti (1981). to the developing vascular cells. These
Another nematode with a similar feeding nematodes are completely embedded in the
strategy is Tylenchulus semipenetrans, the root during their initial stages of
citrus nematode, although the juvenile development, but later the cyst nematodes
stages of this nematode do feed as protrude from the root. The J2 nematodes
ectoparasites. As is common in biological inject secretions into and around the plant
systems, it is often difficult to precisely cells to stimulate the formation of large
classify animals due to variation in their feeder cell(s), which they non-destructively
behavior. True to this rule, several species feed on throughout their life cycle. Feeding
of ectoparasitic nematodes cells of root-knot nematodes (giant cells)
(e.g. Helicotylenchus) are also capable of form by repeated nuclear division in the
partially penetrating the root and feeding. absence of cell division. Feeding cells of
However, we do not classify these cyst nematodes form by the incorporation of
nematodes as semi-endoparasites because neighboring cells into a syncytium formed
they do not exhibit a consistent by the breakdown of neighboring cell walls.
endoparasitic feeding behavior. Once the feeding cells are formed, the
MIGRATORY EDNO-PARASITIC juvenile nematode rapidly becomes
NEMATODE sedentary because their somatic muscles
Migratory endoparasitic nematodes atrophy. The juveniles feed, enlarge and
spend much of their time migrating through molt three times to the adult stage. The large
root tissues destructively feeding on plant feeding cells formed by these nematodes
cells. These nematodes cause massive plant plug the vascular tissue of the plant making
tissue necrosis because of their migration it susceptible to water stress. Female
and feeding. When they feed from the plant, sedentary endoparasites enlarge
they simply suck out the plant cell considerably into a saclike shape and are
cytoplasm using their stylet, killing the plant capable of laying large numbers of eggs.
cell and moving ahead of the lesion. They Eggs are typically laid outside the nematode
make no permanent feeding cells. In a in a gelatinous egg mass, but in cyst
typical life cycle, the nematode hatches nematodes most eggs are retained inside the
from the egg as a second-stage juvenile and female body. Both types of nematode have
starts feeding on the plant. The nematodes the same basic feeding strategy, but many
feed, molt and reproduce primarily within cyst nematodes have an obligate sexual
the plant tissue. All motile stages are cycle, whereas the most common species of
capable of feeding from the plant and they root-knot nematodes reproduce largely by
are able to move into the soil in search of parthenogenesis.
new roots to invade. Because these
nematodes create extensive wounds in the REFERENCES
plant root, secondary infection by bacteria 1. Barker, K.R., G.A. Pederson, and G.L.
and fungi can often occur, further damaging Windham. 1998. Plant and Nematode
the root system (Zunke 1991). Interactions. ASA, CSSA, and SSSA,
Madison, WI.
SEDENTARY ENDO-PARASITIC 2. Bird, A.F. and J. Bird. 1991. The Structure
NEMATODE of Nematodes, Second edition. Academic
The most damaging nematodes in Press Inc. London.
the world have a sedentary endoparasitic life 3. Blaxter, M.L., P. De Ley, J.R. Garey, L.X.
style. The two main nematodes in this group Liu, P. Scheldeman, A. Vierstraete, J.R.
are the cyst nematodes Vanfleteren, L.Y. Mackey, M. Dorris, L.M.
(Heterodera and Globodera) and the root- Frisse, J.T. Vida, K.W. Thomas, K.W. 1998.
International Journal of Research and Review (ijrrjournal.com) 384
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
A molecular evolutionary framework for the Management of the Soybean Cyst
phylum nematoda. Nature 392:71-75. Nematode. R.D. Riggs and J.A. Wrather,
4. Campbell, J.F. and H.K. Kaya. 1999. How eds. American Phytopathological Society,
and why a parasitic nematode jumps. Nature St. Paul, MN.
397: 485-486. 18. Poinar, G.O., A. Acra, and F. Acra. 1994.
5. Chen, Z.X., and D.W. Dickson. 2004. Earliest fossil nematode (Mermithidae) in
Nematology: Advances and Perspectives Cretaceous Lebanese amber. Fundamental
Vol. 1: Nematode Morphology, Physiology and Applied Nematology 17:475-477.
and Ecology. CABI:Walllingford. 19. Poinar, G.O. 1983. The Natural History of
6. Chen, Z.X., S.Y. Chen, and D.W. Dickson. Nematodes. Prentice Hall, Englewood
2004. Nematology: Advances and Cliffs, NJ.
Perspectives Vol. II: Nematode 20. Powers, T.O., T.S. Harris, and B.C. Hyman,
Management and Utilization. B.C. 1993. Mitochondrial DNA sequence
CABI:Wallingford. divergence among Meliodogyne incognita,
7. Fisher, J.M. and D.J. Raski. 1967. Feeding Romanomermis culicivorax, Ascaris suum,
of Xiphinema index and X. diversicaudatum. and Caenorhabditis elegans. Journal of
Proceeding of the Helminthological Society Nematology 25:564-572.
of Washington 34:68-72. 21. Riddle, D.L., T. Blumenthal, B.J. Meyer,
8. Hewitt, W.B., D.J. Raski, and A.C. Goheen. J.R. Priess (eds). 1997. C. elegans II. Cold
1958. Nematode vector of soil-borne fanleaf Spring Harbor Monograph Series 33. Cold
virus of grape vine. Phytopathology 48:586- Spring Harbor Laboratory Press. Plainview,
595. NY.
9. Hesling, J.J. and H.R. Wallace, H.R. 1961. 22. Riggs, R.D., and J.A. Wrather. 1992.
Observations on the biology of Biology and Management of the Soybean
chrysanthemum eelworm Aphelenchoides Cyst Nematode. American
ritzemabosi (Schwartz) Steiner in florists Phytopathological Society, St. Paul, MN.
chrysanthemum. I. Spread of eelworm 23. Sasser, J.N. and C.C. Carter. 1985. An
infestation. Annals of Applied Biology advanced Treatise on Meloidogyne. North
49:195-209. Carolina State University Graphics, Raleigh,
10. Hooper, D.J. 1972. Ditylenchus dipssaci. NC.
Commonwealth Institute of Helminthology 24. Sasser, J.N. and D.W. Freckman. 1987. A
Descriptions of Plant Parasitic Nematodes, world perspective on nematology: the role
Set 1, No. 14, St. Albans, England. of the society. Pages 7-14 in: Vistas on
11. Lee, D.L. 2002. The Biology of Nematodes. Nematology, J.A. Veech and D.W. Dickson,
Tayor & Francis; New York eds. Society of Nematologists, Inc.
12. Maggenti, A. 1981.General Nematology. Hyattsville, MD.
Springer-Verlag, New York, NY. 25. Siddiqi, M.R., 2000. Tylenchida. CABI:
13. Mai, W.F., P.G. Mullin, H.H. Lyon, K. Wallingford.
Loeffler. 1996. Plant-parasitic nematodes: a 26. Shurtleff, M.C., and C.W. Averre. 2000.
pictorial key to genera. Cornell University Diagnosing Plant Diseases Caused by
Press, Ithaca, NY. Nematodes. APS Press: Minneapolis
14. Mamiya, Y. 1983. Pathology of the pine 27. Southey, J.F. 1972. Anguina tritici.
wilt disease caused by Bursaphelenchus Commonwealth Institute of Helminthology
xylophilus. Annual Review of Descriptions of Plant Parasitic Nematodes,
Phytopathology 21: 201-220. Set 1, No. 13, pp.1-4. St. Albans, England.
15. Manum, S.B., M.N. Bose, R.T. Sayer, R.T., 28. Starr, J.L., J. Bridge, and R. Cook. 2002.
S. Bostrom. 1994. A nematode Plant resistance to parasitic nematodes.
(Captivonema-Cretacea Gen ET SP-N) Oxford University Press; Oxford
preserved in a clitellate cocoon wall from 29. Thomas, K.W., J.T. Vida, L.M. Frisse, M.
the Early Cretaceous. Zoologica Scripta. 23: Mundo, J.G. Baldwin. 1997. DNA sequence
27-31. from formalin-fixed nematodes: integrating
16. Perry, R.N. and M. Moens. 2006. Plant molecular and morphological approaches to
Nematology. CABI: Wallingford. taxonomy. Journal of Nematology 29:250-
17. Noel, G.R. 1992. History, Distribution, and 254.
Economics. Pages 1-13 in: Biology and
International Journal of Research and Review (ijrrjournal.com) 385
Vol.7; Issue: 3; March 2020Yogendra Kumar et.al. Plant-Parasitic nematodes: nature’s most successful plant parasite
30. Viglierchio, D.R. 1991. The World of 33. Whitehead, A.G. 1998. Plant Nematode
Nematodes. AgAccess, Davis, CA. Control. CAB International, New York. NY.
31. Wang, D.Y.-C., S. Kumar, and B.S. Hedges. 34. Zunke, U. 1991. Observations on the
1999. Divergence time estimates for the invasion and endoparasitic behavior of the
early history of animal phyla and the origin root lesion nematode Pratylenchus
of plants, animals and fungi. Proceedings of penetrans. Journal of Nematology 22:309-
the Royal Society of London B 266: 163- 320.
171.
32. Wharton, D.A. 1986. A Functional Biology How to cite this article: Kumar Y, Yadav BC.
of Nematodes. The John Hopkins University Plant-parasitic nematodes: nature’s most
Press, Baltimore, MD. successful plant parasite. International Journal
of Research and Review. 2020; 7(3): 379-386.
******
International Journal of Research and Review (ijrrjournal.com) 386
Vol.7; Issue: 3; March 2020You can also read
