Aphelenchoides oryzae

 

Contents

 

Rev 06/13/2022

Rice White-tip Nematode Classification Hosts
Morphology and Anatomy Life Cycle
Return to Aphelenchoides Menu Economic Importance Damage
Distribution Management
Return to Aphelenchoididae Menu Feeding  References
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Classification:

      Tylenchida
       Aphelenchina
         Aphelenchoidea
          Aphelenchoididae
           Aphelenchoidinae

        Aphelenchoides oryzae Yokoo, 1948

Syonyms

Originally described as the causal agent of white tip of rice by Yokoo (1948) and later synonumized with A. besseyi  by Allen (1952)

 Recently proposed as reinstated bu Subbotin et al., 2021).

However, the classification of A. besseyi based on morphological characters is not well supported by an integrated approach including both molecular and phylogenetic analysis. Ratherr, A. besseyi sensu lato appears to be a species complex with several cryptic species that are not well delimited by morphology (Subbotin et al., 2021).

Species delimitation among A. besseyi sensu lato. populations is important for phytosanitary purposes and for the selection of crop cultivars resistant to these nematodes. For example, A. besseyi sensu stricto parasitizes only strawberry (Olivieria et al., 2019). whereas A. besseyi sensu lato has a much wider host range. Conseqquently, Subbotin et al (2021) proposed the reinstatemnt of A. oryzae, which was originally described by Yokoo (1948) as the causal agent of white tip of rice but later synonymized with A, besseyi by Allen (1952)..  Subbotin et al., (2021) also proposed A. pseudobesseyi  and A. pseudogoodeyi for variants of A. besseyi sensu lato that infect cotton and soybeans (Scheck, 2021)..

 


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Morphology and Anatomy:


Drawings by M.W. Allen, photographs by P. Mullin
Aphelenchoides besseyi is characterized by a large metacorpus (median bulb), and esophageal glands usually overlapping dorsally. 

Dorsal esophageal gland opens into lumen of esophagus in metacorpus, just anterior to the pump chamber.

Subventral esophageal glands open into lumen of esophagus in metacorpus, posterior to the pump chamber.

 

From Franklin and Siddiqi, 1972

The nematode has a slender stylet with small, distinct knobs.  

The tail has a terminal spike or mucro.

Females:  0.66-0.75 mm long and slender.  

Males:  are as numerous as females.  

Male reproductive structures have no bursa and the spicules have the typical rose-thorn shape of the genus (Franklin and Siddiqi, 1972). 

 

Reported median body size for this species (Length mm; width micrometers; weight micrograms) - Click:

 

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Distribution:

Aphelenchoides besseyi sensu lato  is widely distributed and occurs in most rice growing areas (Ou, 1985).  The known distribution of A. besseyi on rice includes; Australia, Ceylon, Comoro Islands, Cuba, El Salvador, Hungary, India, Indonesia, Italy, Japan, Madagascar, Mexico, Pakistan, Philippines, Taiwan, Thailand, former USSR, and in most countries of central and West Africa (Ou, 1972; Franklin and Siddiqi, 1972).   Aphelenchoides besseyi has also been reported as the causal agent of false angular leafspot of beans in Costa Rica (Barrantes et al., 2006; Salas and Vargas, 1984).

Aphelenchoides besseyi was first found in Japan in 1915.  In the USA the disease was first noticed in the southern United States in 1935 but was attributed to a nutrient deficiency (Ou, 1972).  

Aphelenchoides besseyi sensu lato has been reported in many Southern U.S. states that produce rice.

White tip disease caused by Aphelenchoides besseyi, is an economic problem in many countries.  Recent detections of this nematode in California have sparked the concern of California's rice industry. 

From 1959 to 1996, A. besseyi was detected only twice in California by CDFA Nematologists: once in 1959, in a quarantine strawberry sample originating in Oregon, and the second time in 1963 in a fungal culture collected in Butte county.  Attempts to find the nematode again from the same field were unsuccessful.  A  survey of the state by CDFA for the presence or absence of A. besseyi in California paddy rice was initiated in 1997.  It was intended that this survey would provide a sound basis for certifying California paddy rice free of A. besseyi, and thereby, eliminate the requirement by the government of Turkey for methyl bromide treatments of export shipments.  Sampling was designed to detect the presence of the nematode at the county or rice growing region level and 170 samples were collected. 

During the 1997 survey, one confirmed and three suspected findings of A. besseyi resulted in four samples collected from two counties.  These samples tested negative when examined a second time.  However, the government of Turkey required that batches of rice intended for shipment to that country should be sampled and certified to be free of the nematode.  Between 1998 and 2001, A. besseyi has been found in three such export loads.  Those shipments were rejected, resulting in millions of dollars in losses.

Aphelenchoides besseyi was detected in paddy rice shipments, once each in 2001 and 2002, and in 11 samples in 2005.  It has been detected only in the northern counties (Butte and Sutter), and continues its status as a quarantine pest of very limited distribution in California (J. Chitambar, CDFA, personal communication).
 

 

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Economic Importance:

A-rated pest in California Nematode Pest Rating System.

At the state level there are no formal quarantine regulations implemented against A. besseyi.  There are no prohibitions for the import of rice seed into California from other states within the US.  At the federal level, federal regulations have prohibited the import of seed and paddy rice into the US since November 23, 1933.  Milled rice can enter California. 

Paddy rice exported to Turkey requires certification for freedom from A. besseyi according to the Turkish Government pest control requirements.  In compliance with the Turkish government, certification is given on a per shipment basis; each shipment has to be sampled and found free of A. besseyi before it can be certified and shipped to Turkey.  

False angular leafspot of beans is considered an important emergent disease of beans in Costa Rica.  In many areas of Costa Rica beans are grown in rotation with rice (Barrantes et al., 2006).

Although A. besseyi is widely distributed in Brazil, economic losses have rarely been reported. However, the frequent association of A. besseyi with forage grass seeds in Brazil represents a phytosanitary barrier for export to many countries. In addition, other morphologically similar but non-pathogenic Aphelenchoides species are also associated with forage grass seeds, leading to difficulty in attaining a robust diagnosis (de Jesus et al., 2016).

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Feeding:

Mainly ectoparasitic on buds.  

Feeds at leaf tips and growing points in rice.  

May feed endoparasitically in leaf mesophyll.

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Hosts:

Rice is the most important host world wide.  

On strawberry A. besseyi is the causal agent of 'summer dwarf' or 'crimp' in the United States and Australia.  

Other host plants include; onion, garlic, sweet corn, sweet potato, soybean, yan chinese cabbage, sugar cane, horseradish, lettuce, millet, many grasses, orchids, wishbone, chrysanthemum, marigold, mexican sunflower, african violets, rubber plant, Hibiscus brachenridgii,  and hydrangea (Franklin and Siddiqi, 1972). Aphelenchoides besseyi has also been reported as the causal agent of false angular leafspot of beans in Costa Rica (Barrantes et al., 2006; Salas and Vargas, 1984).

 

The following are listed as hosts in various literature sources:

Chrysanthemum maximum Ramond. Max Daisy Setaria italica Beauvois.    Foxtail Millet
Chrysanthemum X morifolium Ramat. Florist's Mum Setaria viridis  Green Foxtail
Coleus blumei Benth.   Painted Nettle Tagetes sp. L. Marigold
Cyperus iria    Umbrella Sedge Tithonia diversifolia A. Gray
Dahlia pinnata Cav.   Dahlia Torenia fournieri Linden
Digitaria sanguinalis Scop. Hairy Crabgrass Vanda sp. v. X  var   Kapoho
Erechtites praealta Raf.   Vanda sp. v. X  var   Trimerrill
Fragaria X ananassa  Strawberry Vanda sp. v. X  var   Rose Marie
Hydrangea macrophylla Ser.   French Hydrangea Vanda sp. v. X  var   Miss Deun
Impatiens balsamina L.   Garden Balsam Vanda sp. v. X  var   Miss Joaquim
Oryza sativa L.   Rice Vanda sp. v. X  var   Puna
Panicum miliaceum L. Broom-Corn Millet Zinnia elegans Jacq. Zinnia
Pluchea odorata     

 

  
For an extensive host range list for this species, click

 

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Life Cycle:

Ecophysiological Parameters:

For Ecophysiological Parameters for this species, click If species level data are not available, click for genus level parameters

 

Aphelenchoides besseyi is a seed-borne ectoparasite rice. Nematodes in dry rice seeds are iin anhydrobiosis and are activated by rehydration. Hoshino and Togashi (2020) demonstrated that Survival rate in dry rice seeds was lower at 20 and 25�C than at −5 to 10�C after storage for 190 days. No nematodes survived a storage period of 1313 days at 20 and 25�C.

However, when rice seeds were held at 5�C, the survival rate of nematodes decreased during a period of 7315 days. In storage at −30�C, nematode survival was not affected during a period of 6485 days. After storage at −30�C for 6546 days, 96% of rice seeds germinated; 60-96% of seeds germinated after storage at 5�C for 6610-7373 days. Therefore, Hoshino and Togashi (2020) postulated that low temperature storage of rice seeds (between %C and -30C) would not signicicantly disrupt the pathogenicituy of A, besseyi on rice.

Anhydrobiotic in dry tissues, under hulls of rice grains; viable after 3 years. 

This nematode is not thought to survive long periods in soil between crops (Cralley and French, 1952).

This nematode is mainly ectoparasitic feeding on young tissue.  At the end of the growing season many nematodes are in a state of cryptobiosis under the hulls of seed (Taylor, 1969).  

Seed infected with Aphelenchoides besseyi is planted and the nematodes become active and are attracted to the meristematic areas.  During early growth, A. besseyi is found in low numbers within the folded leaf sheath, feeding ectoparasitically around the apical meristem (Todd and Atkins, 1958).  A rapid increase in nematode numbers takes place at late tillering and is associated with the reproductive phase of the plant.  Nematodes are able to enter the spikelets before anthesis and feed ectoparasitically on the plants reproductive structures.  As grain filling and maturation proceed, reproduction of the nematode ceases, although the development of third stage juveniles to adult continues until the hard dough stage.  

The population of nematodes is predominately adult female which are normally amphimictic, although parthenogenetic reproduction has been reported (Sudakova and Stoyakov, 1967).  

These nematodes coil and aggregate in the glume axis.  

The optimum temperature for oviposition and hatch is 30C. 

At 30C the life cycle is approximately 8-12 days and no development occurs below 13C (Sudakova, 1968).

Aphelenchoides besseyi slowly desiccate as kernel moisture is lost.  They become anhydrobiotic dormant, and are able to survive in a quiescent state on infested seed for long periods of time, from 8 months to 3 years (Cralley, 1949; Yoshi and Yamamoto, 1950).  Survival is enhanced by aggregation and a slow rate of drying (Huang and Huang, 1974), but the infectivity of the nematode is reduced as seed age increases (Cralley and French, 1952). 

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Damage:

Feeding at leaf tips in rice results in whitening of the top 3-5 cm of the leaf, leading to necrosis (described as "White Tip" of rice by Yokoo, 1948). There is also distortion of the flag leaf that encloses the panicle.
Photo from Society of Nematologists slide set, 1980.
Diseased plants are stunted, lack vigor and produce small panicles. Affected panicles show high sterility, distorted glumes and small and distorted kernels (Ou, 1972).
False angular leafspot of beans caused by Aphelenchoides besseyi.
Photograph from Barrantes et al., 2006

 
In the rice seed-bed, emergence of severely infected seedlings is delayed and germination is low. 

The most conspicuous symptoms occur at the tillering stage (Taylor, 1969). 

Yields of rice may be reduced 50%.

Experiments have shown that different varieties of rice are affected to different degrees of infestation.  Yields have been reported to be reduced by 17-54% in susceptible varieties and 24% in resistant (Atkins and Todd, 1959).

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Management:

Preventative Measures - Aphelenchoides besseyi infestations can be avoided by using nematode-free seeds and planting in nematode-free fields (Taylor, 1969; Hudma et al., 1994).

Host Plant Resistance, Non-hosts and Crop Rotation alternatives:

For plants reported to have some level of resistance to this species, click
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References:

Allen, M.W.  1952.  Taxonomic status of the bud and leaf nematodes related to Aphelenchoides fragariae (Ritzema Bos, 1891).  Proc. Helminth. Society of Washashington.  19:108-120.

Barrantes, W., Araya, C.M., Esquivel, A. 2006. Falsa mancha angular del frijol: una enfermedad que avanza en Costa RicaManejo Integrado de Plagas y Agroecologia (Costa Rica) No. 78, 2006

Bridge, J., M. Luc and R.A. Plowright.  1990. "Nematode parasites of  rice."  Pp. 69-108, M. Luc et al. (eds.), Plant parasitic nematodes in subtropical and tropical agriculture.  Wallingford, UK: CAB International.

Cheng, X., Xiang, Y., Xie, H., Xu, C.-L., Xie, T.-F., Zhang, C. & Li, Y. (2013). Molecular characterization and functions of fatty acid and retinoid binding protein gene (Ab-far-1) in Aphelenchoides besseyi. PLoS ONE 8, e66011.

Cralley, E.M.  1949. "White tip of rice."  Phytopathology.  39:5.

Cralley, E.M., and R.G. French.  1952.  "Studies on the control of white tip of rice."  Phytopathology.  42:6.

de Jesus, D.S., Gon�alves Oliveira, C.M., Roberts, D., Blok, V., Neilson, R.,  Prior, T., Balbino, H.M., MacKenzie, K.M. D�Arc de Lima Oliveira, R. 2016. Morphological and molecular characterisation of Aphelenchoides besseyi and A. fujianensis (Nematoda: Aphelenchoididae) from rice and forage grass seeds in Brazil. Nematology 18:337�356.

Franklin, M.T. and M.R. Siddiqi. 1972. Aphelenchoides besseyi. Commonwealth Institute of Helminthology Descriptions of Plant-parasitic Nematodes Set 1, No. 4.

Gergon, E.B. and J.C. Prot.  1993.  "Effect of benomyl and carbofuran on Aphelenchoides besseyi on rice."  Fundamentals of Applied Nematology.  6:563-566.

Gokte, N. and V. K. Mathur. 1993. Treatment schedule for denematization of seeds of Setaria italica and Panicum miliaceum infested with Aphelenchoides besseyi. Nematologica 39:274-276.

Goodey, J. B., M. T. Franklin, and D. J. Hooper. 1965. T. Goodey's: The Nematode Parasites of Plants Catalogued Under Their Hosts. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition

Hoshino, S. and Togashi, K. 2020. Effects of temperatures on survival of Aphelenchoides besseyi in prolonged storage of rice grains. Nematology 22:1169-1177.

Huelma, C.C., J.C. Prot, S.D. Merca, and T.W. Mew.  1994.  "Aphelenchoides besseyi in irrigated upland and lowland rice during dry  and wet season."  International Rice Research Notes.  19 (3):30.

Ibrahim, S. K., R. N. Perry and D. J. Hooper. 1994. Use of esterase and protein patterns to differentiate two new species of Aphelenchoides on rice from other species of Aphelenchoides and from

Ou, S.H.  1985.  Rice Diseases (2nd edition).  New England: Commonwealth Mycological Institute.

Pinheiro, F.P., R.P. Vianello, F.S. Ebeidalla, and R.C.V. Tenente.  1997.  "Thermal seed treatments to eradicate Aphelenchoides from Brachiaria dictyoneura."  Nematologia Brasilerira.  21 (1): 92-97.

Salas, LA; Vargas, E. 1984. El nematodo foliar Aphelenchoides besseyi Christie (Nematode: Aphelenchoididae) como causante de la falsa mancha angular del frijol de Costa Rica. Agronomía Costarricense 8:65-68

Sanwal, K.C.  1961. A key to the species of the nematode genus Aphelenchoides Fischer, 1894.  Canadian Journal of Zoology.  39:143-148.

Scheck, H.J. 2021. California Pest Rating Proposal for Aphelenchoides besseyi Christie, 1942 Strawberry summer crimp nematode. CDFA Sacramento, California, USA.

Subbotin, S.A., Oliveira, C.J., Alvarez-Ortega, S., Desaeger, J., Crow, W., Overstreet, C., Leany, R., Vau, S. and Inserra, R.H. 2021. The taxonomic status of Aphelenchoides besseyi Christie, 1942 (Nematoda: Aphelenchoididae) populations from the Southeastern USA, and description of Aphelenchoides pseudobesseyi sp. n. Nematology 23: 381-413

Taylor, A.L.  1969.  "Nematode parasites of rice."  Pp. 264-268, J.E. Peachey (ed.), Nematodes of Tropical Crops.  Albans, Herts, England: Commonwealth Bureau of Helminthology.

Tamura, I., and K. Kegasawa.  1958.  "Studies on the ecology of the rice nematode, Aphelenchoides besseyi Christie.  II.  On the parasitic ability of rice nematodes and their movement into hills."  Japanese Journal of Ecology.  8:37-42.

Templeton, G.E., T.H. Johnston and J.T. Daniel.  1971.  Benomyl controls rice white tip disease."  Phytopathology.  61:1522-1523.

Tenente, R.C.V., M.M.V.S. Wetzel, E. S. Manso, and A.S. Marques.  1994.  "Survival of Aphelenchoides besseyi in infested rice seeds stored under controlled conditions."  Nematologia Brasiliera.  18 (1): 85-92.

Tenente, R.C., and E.S. Manso.  1994.  "Chemical and heat treatments of  rice seeds infested with Aphelenchoides besseyi."  Nematologia Brasileira.  18 (1): 28-34.

Yokoo, T. 1948. [Aphelenchoides oryzae Yokoo n. sp. a nematode parasite to rice plant.] Annals of the Phytopathological Society of Japan 13, 40-43.

Yoshi, H., and S. Yamamoto.  1950.  "A rice nematode disease 'Sencha Shingane Byo'.  II. Hibernation of Aphelenchoides oryzae."  Journal of Faculty of Agriculture, Kyusha University.  9:223-233.

 


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Revised: June 13, 2022 .